- Mar 2024
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Reply to the reviewers
1. General Statements
We thank the reviewers for their time and both thoughtful and constructive comments. Their specific points are addressed below but a general point that we would like to comment on is that in the original version it appears we did not make our model clear enough. The dogma in the field is that Rab7 is recruited to endosomes from a cytosolic pool via exchange with Rab5 (mediated by Mon1/Ccz1). Our work instead indicates that the majority of Rab7 is delivered to Dictyostelium phagosomes by fusion with other endocytic compartments. It was not our intention to imply there was no canonical recruitment of Rab7 from a cytosolic pool, and indeed we provide data to show this happens at a low level and discuss this in the manuscript. Nonetheless, we clearly over-stated the exclusivity of Rab7 recruitment to phagosomes via fusion at several points and our original model cartoon, and have tried to better explain or more nuanced model with multiple routes for Rab7 acquisition in this revision, including a completely redrawn model figure (Fig. 7).
2. Description of the planned revisions
Reviewer 1:
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The observation that macropinosomes undergo retrograde fusion with newly formed phagosomes to facilitate phagosome maturation is an interesting notion that challenges the traditional model. However, not all phagocytes exhibit a high level of macropinocytosis, and axenic Dictyostelium cells used in the study may be an exception. Thus, it remains unclear whether fusion with macropinosomes is universally required for phagosome maturation. WT Dictyostelium cells or axenic cells cultured under SorMC/Ka condition (Paschke et al., PLoS One, 2018) exhibit significantly reduced macropinocytosis. The authors could examine whether the accumulation of Rab7 and V-ATPase on large-sized phagosomes is delayed in these cells. These experiments may help broaden the applicability of the authors’ finding.
As our previous work (Buckley et al. PloS pathogens 2019) demonstrated that bacterially-grown PIKfyve mutants are also defective in bacterial killing and growth it is highly likely that cells also are defective in V-ATPase and Rab7 acquisition. However, we agree that formally testing this will further support our conclusions and improve the paper and should be quite straightforward.
We will therefore co-express GFP-V-ATPase and RFP-Rab7 in both Ax2 and non-axenic cells grown on bacteria and repeat our analysis of recruitment to phagosomes – with the caveat that non-axenic cells do not phagocytose large particles such as yeast (Bloomfield et al. eLife 2015), so the imaging and quantification will be more challenging in this case.
PIKfyve seems to play a specific role in the maturation of phagosomes but not macropinosomes. The differences may be driven by signaling from phagocytic receptors, as the author suggested. Alternatively, the large size of the yeast-containing phagosomes may require additional steps for efficient lysosomal delivery. The authors should consider examining whether PIKfyve is needed for the delivery of Rab7 and V-ATPase to phagosomes of comparable size to regular macropinosomes, such as those containing K. aerogenes or small beads. In addition, whether the process also involves fusion between phagosomes and macropinosomes should be verified.
Whilst it is possible that large size of yeast-containing phagosomes requires additional mechanisms to process them, our previous data demonstrate that PIKfyve is also required to kill much smaller bacteria such as Klebsiella and Legionella (Buckley et al. PloS pathogens 2019). Furthermore, in this paper we also showed that loss of PIKfyve disrupts phagosomal proteolysis using 3um beads, and showed that V-ATPase recruitment was reduced on purified phagosomes containing 1um beads. We therefore find consistent defects on phagosomes of different size, with different cargos. Nonetheless, the experiments above, observing V-ATPase and Rab7 in cells grown on bacteria should directly address this point.
As suggested, we will also perform a dextran pulse-chase prior to addition of bacteria to test if we can observe macropinocytic delivery to bacteria-containing phagosomes - perhaps using E. coli as their elongated shape may help phagosome visualisation.
In the previous study from the authors' group (Buckley et al., PLoS Pathog, 2019), it was shown that the accumulation of V-ATPase on phagosomes begins immediately after internalization in both PIKfyve mutant and WT, although V-ATPase accumulation reaches only half of the levels seen in WT. This partial accumulation of V-ATPase differs from the almost complete absence of Rab7 recruitment found in this study, which raises the question of whether there exists yet another population of fusogenic vesicles that are positive for V-ATPase but negative for Rab7. This could be checked by simultaneously examining the dynamics of V-ATPase and Rab7 during yeast phagocytosis in the PIKfyve mutant.
We agree with the referee that there are multiple pools of V-ATPase, and we show that there is both a very early PIKfyve-independent recruitment of both V-ATPase and Rab7 as well as a later and more substantial pool delivered in a PIKfyve-dependent manner. It is clear that V-ATPase and Rab7 do not always co-localise however - the clearest example being on the contractile vacuole, which has lots of V-ATPase but no Rab7 (the large bright magenta structure in Fig 2G.).
We suspect that the dramatically reduced, but not completely absent levels of both V-ATPase and Rab7 recruitment in the absence of PIKfyve are similar, but the challenges with imaging these very small low levels means we cannot formally exclude that there is a pool of V-ATPase vesicles that lack Rab7 which fuse to very early phagosomes. Nonetheless, as we will already be looking at V-ATPase and Rab7 in PIKfyve KO's in the experiments above will also attempt to unequivocally differentiate a pool of V-ATPase positive/Rab7 negative vesicles fusing with phagosomes.
Reviewer 2:
(1) The authors show that deletion of PIKfyve results "in an almost complete block in Rab7 delivery to phagosomes" (page 17) indicating that the delivery of Rab7 depends on fusion with Rab7-positive structures. This would suggest that the Rab7-GEF Mon1-Ccz1 is not localized to the membrane of the phagosomes. Could the authors test for the presence of Mon1-Ccz1 in either fluorescence microscopy experiments or on purified phagosomes to exclude the possibility of a "canonical" Rab7 recruitment by its GEF? If the GEF is found on phagosomal membranes it would indicate that a Rab-transition from Rab5 to Rab7 occurs on the phagosome during maturation, but on a low level. The later fusion event might be a homotypic fusion of two Rab7-positive compartments. The observed fusion events could still deliver the bulk of Rab7 and other endolysosomal proteins to the phagosome. If the Rab7-GEF is not found on phagosomes how do the authors envision that the organelle keeps its identity? Is it solely dependent on PI(3,5)P2? What is the fate of the Rab7-negative phagosome in ∆PIKfyve cells if Rab7 is not delivered to the membrane, is there degradation happening over longer periods of time?
This is an excellent suggestion, for which we thank the reviewer. Mon1 and Ccz1 are highly conserved, with clear Dictyostelium orthologues that have never been studied. Our model is that there is a small proportion of Rab7 driven by this canonical pathway so would expect Ccz1/Mon1 to coincide with loss of Rab5 and be unaffected by loss of PIKfyve - although subsequent Rab7 delivery would be lost. This is easy to test by cloning and expressing GFP-fusions of both Ccz1 and Mon1 and would be highly informative. Note we do not exclude canonical Rab7 recruitment in our model (see discussion), our data just indicate this has a minor contribution.
Reviewer 3:
The focus is on their manuscript is loading of Rab7 on phagosomes, but there's no indication about Rab7 activation (GTP-loading). Would the RILP-C33 probe work in Dictyostelium? If not possible, the activation state of Rab7 should still be discussed. Despite Rab7 on other organelles in PIKfyve-inhibited cells, is this active or not?
The GTP-loading status of Rab7 is a good question, although the general dogma is that membrane-localised Rabs are active. We will try the RILP-C33 probe in Dictystelium as suggested, but as these cells lack an endogenous RILP orthologue there is a high chance it will not work. Sadly, reliable tools to asses active Rab status are a general limitation for the field, so if the RILP-C33 probe does not work we will add this caveat to the discussion.
The authors need to better address the confusing kinetics of early Rab7 recruitment, followed by SnxA (Fig. 4G, same for VatM - Fig. 4I ) - which is counterintuitive if PIKfyve activity is required to recruit Rab7. How do the authors explain this? Are phagosomes prevented from acquiring Rab7 in PIKfyve deficient cells because of a defect on phagosomes or the endo-lysosomes loaded with Rab7 (but not active).
We believe this again relates to the over-simplification of our model. Our data indicate both PIKfyve dependent and independent Rab7 recruitment. In contrast to the abrupt recruitment of SnxA at ~120 seconds (Vines et al. JCB 2023), both Rab7 and VatM accumulate gradually over time starting from almost immediately following engulfment (Buckley et al. 2019, and Figure 2F). Our data indicate that the first stage of this is PIKfyve independent, and is responsible for ~10% of the total Rab7/V-ATPase accumulation by both the imaging in this paper, and Western blot for V-ATPase on purified phagosomes in Buckley et al. PLoS pathogens 2019. The arrival of some Rab7/V-ATPase prior to PI(3,5)P2 therefore supports our model where there are multiple sources of Rab7.
As the reviewer quite rightly points out, interpretation of the defects observed in the absence of PIKfyve becomes complex and we cannot completely differentiate between a defect on the phagosome, or the Rab7 compartments that fuse with them (or indeed both). In fact, we already note that small Rab7 compartments that we observe in wild-type cells are much more sparse in PIKfyve mutants. Therefore whilst the requirement for PI(3,5)P2 in the clustering and fusion of macropinosomes with phagosomes is clear, additional effects on the PI(3,5)P2-independent Rab7 compartments cannot be excluded.
The experiments above using the RILP-C33 active Rab7 biosensor as well as observation of the Mon1/Ccz complex should further clarify this, but we will also add further discussion of these points.
3. Description of the revisions that have already been incorporated in the transferred manuscript
Reviewer 1:
Minor comments.
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It is unclear how the experiment in Figure 3G was conducted. If microscopic analysis was involved, the corresponding images should be included.
We apologise that we overlooked this and have now added a full description in the materials and methods (P8 L16-21). Fluorescence measurements were performed using a plate reader, so there are no images.
Page 11-Line 2, the sentence "there was no obvious clustering around the nascent phagosome (Figure 2D)." It is Figure 2E, not Figure 2D.
Corrected.
There is an inconsistency regarding the description of fluorescent fusion proteins. For example, both GFP (RFP)-2xFyve and 2xFyve-GFP (RFP), as well as GFP-Rab5 and Rab5-GFP, were used. Typically, placing GFP (or RFP) before a gene suggests N-terminal tagging, while placing it after the gene implies C-terminal tagging. The authors should clarify the position of the fluorescent tag and ensure consistency in their descriptions.
We apologise for this oversight, and have been through and corrected all fusion protein references accordingly.
One of the videos was not referred in the manuscript or described in the Video legends. This video seems to correspond to Figure 5A, albeit with a different pseudo-color scheme.
This has been corrected. Video 7 does correspond to Fig 5A, and we have corrected the colour scheme to match and added references to the video in the text and figure legend.
Reviewer 2:
(2) In their abstract, the authors state that they "...delineate multiple subpopulations of Rab7-positive endosomes that fuse sequentially with phagosomes" (page 2, line 14,15). However, the data provides only evidence for V-ATPase or PI(3,5) P2-containing structures and the authors conclude to my understanding that macropinosomes are the main source for vesicular structures fusing with phagosomes. I would ask the authors to please be clear on the identity of the "Rab7-donor"-structures throughout the manuscript. Saying that they delineate multiple subpopulations of endosomes seems to be overstated.
We identify that macropinosomes are one source (subpopulation) of Rab7/PI(3,5)P2 vesicles but our data clearly show that they are the only source of Rab7 - there is clearly an additional early Rab positive / PI(3,5)P2-negative subpopulation of vesicles that cluster and fuse too at earlier stages. For example, in Figure 4F we co-express Rab7a/SnxA and show that whilst all the SnxA vesicles also contain Rab7 (and dextran), there is a clear separate population of small and early-fusing population of Rab7-containing vesicles that do not possess PI(3,5)P2. This is further validated in Figure 5B and C. To our mind this clearly demonstrates and defines different Rab7 endosomal populations, although we do not yet know the origins of the initial Rab7-positive/PI(3,5)P2 negative population - as discussed in our response to their point (3) below.
Minor points:
(1) The sentence "...which both deactivates and dissociates Rab5, and recruits and activates Rab7 on endosomes" is at least problematic as it suggests that Mon1-Ccz1 directly drives GTP-hydrolysis of Rab5 and dissociates it from the membrane. Indeed, Mon1-Ccz1 is shown to interfere with the positive feedback loop of the Rab5-GEF by interacting with Rabex (Poteryaev et al., 2010), so a rather indirect effect of Mon1-Ccz1. A GAP and the GDI are needed for Rab5 deactivation and dissociation from the membrane. How both are involved in the endosomal Rab-conversion is not clarified.
We have changed the text to better represent this complexity (P4 L4-6)
(2) Signals of RFP-labeled proteins are difficult to interpret throughout the experiments. What are the structures that show a strong accumulation of red signal in Fig. 1A,B, Fig 2G and Fig4A (20sec.) If these are fluorescently labeled proteins it would suggest that most of the proteins cluster/accumulate in the cell. Can the authors provide better images?
We appreciate that some of these reporters with multiple localisations can be difficult to interpret. This is major challenge for these sort of studies and main reason we use the large and easily-identified yeast containing phagosomes for quantification. In Fig. 1 the large structure is the large peri-nuclear cluster of Rab5 previously reported (Tu et al. JCB 2022). In Fig. 2G the bright structure is the recruitment of V-ATPase on the CV. Both these large structures easily distinguished from the phagosomal pool we are interested in. Whilst we would love to provide better images, this is simply not possible - both these other structures are unavoidable and we are already using some of the best microscopy methods available. We have however clarified the additional localisations seen in these images in the revised figure legends.
(3) On page 11 the authors state "...macropinosomes in ∆PIKfyve cells still appeared much larger. Quantification of their size and fluorescence intensity demonstrated that although macropinosomes started off the same size,...". This statement is not reflected in the data depicted in Fig. 3A,B. The size of the single labeled macropinosome appears to be larger in wildtype than in ∆PIKfyve cells from the beginning on. However, the quantification in Fig 3F is clear. So, are these bad examples in 3A,B, are they swapped or is this due to the additional expression of GFP-Rab7A? Could you please comment on the effect that the (over-)expression of GFP-tagged Rab-GTPases might have on the observations described in this paper in the discussion part?
As you can see from the error bars in Figure 3F, macropinosomes are extremely variable in size - ranging from ~0.2-5 microns in size in axenic Dicytostelium. The image in Figure 3B is therefore indicative of this heterogeneity, rather than being a "bad example". This is why we designed the experiment to quantify several hundred vesicles in order to make any conclusions - as well as doing it in the absence of any GFP-fusion expression.
Although we have not noticed any issues (enlarged vesicles are also clear in GFP-Rab7 expressing cells in Figure 1B), we do of course accept that GFP-Rab7 expression itself may have some detrimental effects on maturation and this is why we quantified macropinosome size in untransformed cells. We have clarified this in the results section (P12 L28).
(4) In Fig. 6E it is hard to distinguish if the dextran is accumulating inside the phagosome. I would suggest conducting a 3D reconstruction of these images to allow judging if macropinosomes fused with the phagosomes or if they cluster around the neck of the phagosome.
This would be nice, but not possible as these images are from single confocal sections, rather than a complete high-resolution Z-stack. We have however added an enlargement of both Figure 6D and E which we feel now more clearly shows the presence of dextran within the bounding PI(3)P membrane of the phagosome.
(5) In the discussion, the authors state that the small pool of "PIKfyve-independent Rab7" is "insufficient to for subsequent fusion with other Rab7A-positive compartments, further Rab7 enrichment, and lysosomal fusion." What is the rationale for this conclusion? Is it shown how many Rabs are necessary to induce a tethering and fusion event? It would be good to revise this part of the discussion also in respect of the first major point of my comments above.
Our data show that in the absence of PIKfyve, phagosomes still remove Rab5 and gain a small pool of Rab7 but progress no further. This is consistent with some block in the HOPS-mediated homotypic fusion of Rab7 compartments. However, we accept that this is not necessarily due to simply not having enough Rab's so have rephrased the discussion accordingly.
(6) The intention of the paragraph about phagosomal ion channels is for this reviewer somehow out of context. It is not clear to me how the authors relate this to their findings. It would be could to bring this into a broader context.
__ __We mention ion channels in the background as they represent the main class of PI(3,5)P2 effectors known so far. We feel this is important background context, even if our studies do not directly relate to this.
Reviewer 3:
Their disclosure and use of statistics is incomplete and/or inconsistent, and potentially wrong in some cases. For example, the authors disclose the number biological repeats in a few experiments (Fig. 3C, F) but not in the majority. Instead, they state the number of phagosomes without indicating biological repeats (eg. Fig. 2 and others). So, it is not possible to know if their data are reproducible. Despite not indicating independent experiments in some cases, they speak of SEM, which applies to mean of means from biological repeats. In other cases, none of this is disclosed (eg Fig. 3G). Often there is no indication of what statistical test was done OR if a statistical test was done (eg. Fig. 3G, Fig. 4, etc). I would recommend the authors review the excellent resource paper published in JCB on SuperPlots to better follow statistical expectations. This is essential to improve reproducibility and confidence in their observations.
We apologise if this was unclear for the referee, but we have tried to be clear in each case. The confusion likely lies in the definition of a biological repeat, which depends on the type of experiment. For quantification of phagocytic events over time, we feel it reasonable to take each individual event (each from an individual organism) as a biological repeat. This is because events are relatively rare and taken from multiple different movies, and it is not technically possible to film both mutants and controls simultaneously. In all these sort of experiments (e.g. Figure 2) we have shown standard deviation, which indicates the reproducibility between phagocytic events. We have clarified that these events are from movies obtained on at least 3 independent days in the methods.
In other cases, such as Figure 3C and F and Figures 5-6, we are able to take measurements across multiple cells simultaneously at each timepoint. It is therefore appropriate to average over multiple independent experimental repeats rather than individual cells. We have therefore used SEM in our analysis, and both the number of individual cells and independent repeats are stated on the graphs and legend. This was incomplete in a few cases but has now been clarified in all cases.
Regarding statistical tests, which ones were used now been clarified in each figure legend. Note that in Fig 3G, we do not apply any test as both lines essentially overlap and it is clear there would not be any convincing differences. In Figure 4, the graphs all compare co-expression of different reporters rather than different mutants or conditions and are from single events. We therefore feel statistical tests are unnecessary and inappropriate. Comparison of the same reporters between strains averaged across multiple events, with statistical analysis is shown in Fig 2 instead. All these points have now been added to the statistics section of the methods (P9 L1-6)
Minor Comments
It is interesting that 2FYVE-GFP stays on phagosomes for 50 min or more - this is distinct from macrophages. Please comment. Have the authors tried other PI(3)P probes to see if the same (PX-GFP).
We have not used other probes but we have no reason to believe 2xFYVE does not behave as predicted as it is the same probe used for most macrophage studies (FYVE domain from human Hrs), and gets removed from macropinosomes exactly as expected. We did not originally comment in this manuscript but PI3P dynamics are even more interesting as our previous data indicate that latex-bead containing phagosomes lose PI3P after 10 minutes (Buckley et al 2019, Figure 4F-G) This indicates phagosome maturation can be regulated by the cargo (under further investigation). Importantly however, both bead and yeast-containing phagosomes have comparable defects in the absence of PIKfyve. This is more fully discussed in our previous paper (Vines et al. JCB 2023) where we characterise PI(3)P and PI(3,5)P2 dynamics in more detail.
Fig. 7 model: the macropinosome in the diagram seems like a dead end as depicted - is there any arrow or change that could be added to show that it doesn't just sit there in the middle? Also, the light green on yellow hurts the eyes!
We apologise, there was actually supposed to be an arrow there but it was lost somewhere in the drafting process. The whole figure has now been updated to more clearly describe our full and more complex model.
Fig. 3F, could be converted to volume assuming macropinosomes are spheres.
This is true, however as these images are taken from single planes we cannot know where in the sphere the slices are and therefore what the maximum diameter would be. We therefore prefer to keep it as area so as not to confuse and over-interpret the data.
Pg. 10, line 10 - Vps34 is Class III PI3K, not Class II.
Corrected.
4. Description of analyses that authors prefer not to carry out
Please include a point-by-point response explaining why some of the requested data or additional analyses might not be necessary or cannot be provided within the scope of a revision. This can be due to time or resource limitations or in case of disagreement about the necessity of such additional data given the scope of the study. Please leave empty if not applicable.
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Reviewer 2:
(3) ("OPTIONAL") Optionally, the authors could also try to clarify these structures' identity by including further colocalization studies with additional early and late endosomal marker proteins. Are they for example positive for early or late endosomal markers like EEA1, ESCRT or Retromer? How about organelle-specific SNAREs? This would give further insights into the character of the "Rab7-donor" structures and would allow to clarify if multiple subpopulations are contributing to phagosome maturation in a sequential order as stated in the abstract. As I am not an expert on Dictyostellium I can`t estimate the effort that would go into such an experimental setup. However, since the time scale of the events in the cell is nicely worked out in this study, these colocalization studies would not need to be conducted as live-cell microscopy experiments.
This is a sensible suggestion that would in theory help define these populations. However many of these markers are poorly defined with respect to phagosomes and/or Dictyostelium. Dictyostelium does not posses an EEA orthologue, but our data also indicate that these vesicles do not possess PI3P so cannot be canonical early endosomes. We have previously characterised WASH/retromer and whilst it is recruited to phagosomes at around the time of Rab5/7 transition Retromer appears to be recruited from the cytosol and drive recycling rather than being delivered on endosomes that fuse (see King et al. PNAS 2016). We have also previously looked at ESCRT (Lopez-Jimenez et al. PLoS Pathogens 2018) which also does not appear to have any recruitment to early phagosomes that would be consistent with a Rab7-sub-population. The SNAREs are yet to be studied in any detail, as they are often too divergent to assign a direct mammalian orthologue.
Therefore, whilst this is a sensible suggestion, and something we would like to follow up in the future, this is not straight-forward and we feel outside the scope of the current study. We have however included additional discussion of this in the revised manuscript (P20 L21-26).
Reviewer 3:
Major Comments:
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Based on the current data, I am not entirely convinced that Rab7 is delivered mostly by fusion with other compartments. At least the data as provided cannot exclude other models. For example, Rab7-containing organelles that cluster with phagosomes may form contact sites that provide a local environment to load cytosolic Rab7. There's also a possibility that some of their Rab7 clusters are membrane sub-domains and not vesicles. Or perhaps, there is a first wave of cytosolic Rab7 recruitment, which then initiates fusion with Rab7 compartments, i.e., there is a two-phase Rab7 recruitment. While this last possibility is consistent with recruitment of Rab7 by fusion (the second phase), the authors present a model that is too simplistic and conclusive based on the data. The authors may be right, but they need to strengthen their evidence towards their claim. Maybe EM could help determine some of these issues. Perhaps better would be the use of FRAP, photo-activation, or optigenetics of Rab7. For example, if Rab7 is acquired on phagosomes after photobleaching clusters of Rab7, this would suggest a cytosolic Rab7 contribution, and if not, this would support their model. I recognize that these experiments are not necessarily trivial, but either the authors augment their data (as suggested or with other approaches) or significantly pare down their conclusions.
We agree with the Referee that we cannot completely exclude other models, and as we talk about in the discussion, we do not wish to do so. We apologise if the role of fusion was over-stated but the model we propose is as the referee suggests: there is likely an early first wave of canonical Rab7 recruitment from the cytosol that is independent of PIKfyve before the majority of Rab7 is subsequently delivered by fusion in a PIKfyve-dependent manner. Our data indicate that the second wave is both quantitively and functionally more significant (see functional data in Buckley et al. 2019).
We do however agree with the referee that we cannot formally exclude things such as contact-site mediated recruitment from the cytosol or sub-domains but not fusion however there is no data to support these either. In contrast, the hypothetical clustered Rab7 contacts/subdomains often (but not always) contain the transmembrane V-ATPase complex (Figure 2G) which must be delivered by fusion.
However we do not wish to over-simplify our conclusions and as we state in the discussion, we do think there is probably a small amount of Rab7 recruited from the cytosol by the canonical pathway. We accept that our cartoon in Figure 7 is over-focussed on fusion so we have substantially revised this, as well as the discussion to give a more balanced and complex view.
Regarding the proposed experiments, unfortunately, the imaging required to acquire these movies is already at the very limit of what is possible so we do not believe it would be technically feasible to employ methods such as FRAP and optogenetics on these relatively fast-moving phagosomes with the temporal resolution required. Furthermore, to differentiate recruitment from a cytosolic pool, every GFP-Rab7 cluster would need to be photobleached, which could not be reliably achieved.
However, this point will be largely addressed by the suggestion of Reviewer 2 to look at the Mon1/Ccz complex. The presence or absence of this will give strong evidence for canonical Rab5/7 transition and Rab7 recruitment from the cytosol which would significantly clarify our model and define the two different mechanisms of Rab7 recruitment to phagosomes.
Early macropinosomes fuse with early phagosomes more readily than 10-min old macropinosomes. Do 10-min old macropinosomes not fuse with older phagosomes? Is this not an issue of mismatched age?
This is an interesting point that we have clarified in the text. We agree with reviewer that it appears the ages of the macropinosomes and phagosomes must match but our data indicate this only occurs when both parties possess PI(3,5)P2 as macropinosome fusions appears to happen in a single burst at about 240 seconds (Figure 6F) rather than as a continuous process. We also do not start to see any fusion of these older macropinosomes when the phagosomes get past the initial first 10 minutes of maturation (Figure 6G).
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Note: This response was posted by the corresponding author to Review Commons. The content has not been altered except for formatting.
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Reply to the reviewers
Reviewer #1 (Evidence, reproducibility and clarity (Required)):
Summary Maintenance of the histone H3 variant CENP-A at centromeres is necessary for proper kinetochore assembly and correct chromosome segregation. The Mis18 complex recruits the CENP-A chaperone HJURP to centromeres to facilitate CENP-A replenishment. Here the authors characterise the Mis18 complex using hybrid structural biology, and determine complex interface separation-of-function mutants.
Major Comments The SAXS and EM data on the full-length Mis18 components must be included in the main Figures, either as an additional figure or by merging/rearranging the existing figures. The authors discuss these results in three whole paragraphs, which are a very important part of the paper.
We thank the reviewer for this constructive suggestion. We have now included an additional figure (new Fig. 2, attached below), that highlights the fit of the integrative model against the SAXS and EM data.
Could the authors also compare the theoretical SAXS scattering curves generated by their final model(s) with the experimental SAXS curves? This would provide some additional evidence for the overall shape of their complex model beyond the consistency with the Dmax/Rg.
We acknowledge the importance of this suggestion. We have now compared the theoretical SAXS scattering curve of the Mis18a/b core complex (named Mis18a/b DN), which lacks the flexible elements (disordered regions and the helical region flexibility connected to the Yippee domains). The theoretically calculated SAXS scattering curve of the model matches nicely with the experimental data with c2 value of 1.36. This data is now included in new Fig. 2 (Fig. 2f) and is referenced on page 9 line 21.
Minor Comments
While the introduction is clearly written, an additional cartoon schematic, representing the system/question would be helpful to a non-specialist reader to interpret the context of the study.
We have now included a cartoon in the revised Fig. 1 to support the introduction on centromere maintenance and the central role of the Mis18a/b/BP1 complex in this process. Please find the new Fig. 1 below.
No doubt the authors had a reason for choosing their figure allocation, but I wonder if more material couldn't be brought from the supplementary into the main figures?
As addressed in our response to one of the major comments, we have now moved key CLMS, SAXS and EM data from the supplemental figure into the main figure, new Fig. 2.
Page 6 "Mis18-alpha possesses an additional alpha-helical domain" - please make it clear in addition to what (I assume it's in addition to Mis18-beta).
Apologies for the lack of clarity. We have now rephrased this sentence to highlight that this difference is in comparison with Mis18b on page 6 line 15.
Page 7 - Report the RMSD of the Pombe vs. Human Mis18-alpha yipee structures?
The S. pombe Mis18 Yippee structure superposes on to the Human Mis18a Yippee domain with an RMSD of 0.92 angstroms with is now mentioned on page 7 line 9.
Page 7 - "We generated high-confidence structural models...." is there a metric for the confidence as reported by RaptorX? Perhaps includinging the PAE plots in the supplementary for the AlphaFold generated models would be useful?
We thank the reviewer for the valid suggestion. We have now included the PAE plot corresponding to the AlphaFold model in the supplementary Fig. S1d and reference on page 7 line 18. RaptorX ranks models based on estimated error. We have now included this information in the new figure legend for Supplementary Fig. S1.
Figure 1 - Perhaps label figure 1b as being experimentally determined, with the R values (as for Figure 1d), and 1c being a predicted model.
We have included Rfree and Rwork values for the Mis18a Yippee homo dimer structure and labelled Mis18a/b Yippee hetero-dimer as the predicted model in Fig. 1c and 1d.
Page 8 "This observation is consistent with the theoretically calculated pI of the Mis18alpha helix" This is a circular argument, of course this region has a low pI due to the amino acid composition. Please remove this statement.
We have now removed this statement as suggested.
Page 8 "...reveals tight hydrophobic interactions" these are presumably shown in Figure 1d rather than in the referenced 1e.
We apologise for the oversight. We have now referred to the correct figure (Fig. 1f in the revised Fig. 1).
Page 8 - The authors should briefly somewhere discuss why there is a difference between their results and those in Pan et al 2009. As I understand it, the Pan et al paper was based in part on modelling with CLMS data as restraints.
We thank the reviewer for this suggestion. According to Pan et al., 2009, the model shown by them was generated using CCBuilder, and their CLMS data could not differentiate the two models with the 2nd Mis18a C-terminal helix in either parallel or anti-parallel orientation. We now briefly discuss this on page 8 and line 22 as follows: "Although the Pan et al., 2019 model presented the 2nd Mis18a in a parallel orientation, they did not rule out the possibility of this assembling in an anti-parallel orientation within the Mis18a/b C-terminal helical assembly (Pan et al., 2019)."
Figure 1 - The labelling of the residues for Mis18-alpha in Figure 1d is problematic, they are black on dark purple (might be my printer/screen/eyes) suggest amending.
We have now rearranged the label positions to overcome this issue. For clarity, the labels that could not be moved appropriately are shown in white.
Figure S3a - Do the authors have some data to show the mass of the cross-linked complex that was loaded onto grids is consistent with what is expected?
Unfortunately, the amount of material that we recover after performing GraFix is not sufficient enough to determine the molecular weight of the crosslinked sample by techniques such as SEC-MALS. However, GraFix fractions were analysed by SDS PAGE, and fractions that ran around the expected molecular weight were selected for EM analysis. We have now included the corresponding SDS-PAGE showing the migration of the crosslinked sample analysed by EM (Supplementary Fig. S3a).
Figure S3b - scale bar
Revised Fig. 2d now includes the scale bar shown.
Figure S3c - Could the authors show or explain the differences between these different 3D reconstructions?
The models mainly differ in the relative orientations of the bulkier structural features that are referred to as 'ear' and 'mouth' pieces of a telephone handset. This has been mentioned in the text, but we note that the figure is not referenced right next to this statement. We have now amended this (Page 9 line 19), and to make it clear, we have also highlighted the difference using an arrowhead in Fig. 2e and S3b. The different orientations are also stated in the corresponding figure legends.
Page 9 - The use of "AFM" for AlphaFoldMultimer" is a little confusing since AFM is the established acronym for Atomic Force Microscopy. Perhaps AF2M?
We have now replaced AFM with AF2M on page 9 to avoid confusion.
Figure S4a - Control missing for Mis18-alpha wild-type
Apology for the confusion, this control is present in Fig. 4a. We have now stated this in the figure legend of S4a for clarity.
Figure S4 d and e - The contrast between the bands and the background is very bad (at least in my copy).
We have now adjusted the contrast of the blots in Fig. S4d and S4e response to this comment.
Page 13 "Our structural analysis suggests that two Mis18BP1 fragments.....". How did you arrive at this conclusion? Is this based on the AlphaFold/RaptorX model? What additional evidence do you have that the positioning of the Mis18BP1 is correct? Does the CLMS data support this?
We confirm that this statement is based on AlphaFold model. We have now explicitly highlighted this on page 14, line 5. As noted in the same paragraph (page 14, line 19), this model agrees with the contacts suggested by the cross-linking mass spectrometry data presented here.
Figure 4a - Would the authors like to consider using a different colour for Mis18BP1? The contrast is not great, especially in the electrostatic surface inset.
In response to this suggestion, the Mis18BP1 helix is now shown in grey in the inset of Fig. 5a.
Reviewer #1 (Significance (Required)):
General Assessment The paper is extremely clearly written. Likewise the figures are beautifully presented and the data extremely clean and fully supportive of the authors conclusions. Indeed it is seldom that one sees the depth of the structural approaches (X-ray, CLMS, EM, SAXS) in one paper which is a huge strength of the manuscript. In addition the translation of this data into very clean cell biological experiments, makes the paper truly outstanding.
Advance The authors provide the first model of the Mis18 complex, with extensive evidence to back up this model. The authors provide additional evidence as to how the deposition/renewal of CENP-A might be mediated by the Mis18 complex. The advance comes from both the level of clarity, detail, and scope achieved in this paper.
Audience This will likely be of great interest to anyone with an interest in chromosome biology, plus be of interest to structural biologists as an outstanding example of hybrid structural biology.
Expertise I am a biochemist with a background in structural biology with some familiarity with centromere biology
Reviewer #2 (Evidence, reproducibility and clarity (Required)):
Summary: The manuscript "structural basis for Mis18 complex assembly: implications for centromere maintenance" by Thamkachy and colleagues describes a study that uses structural analysis to test essential candidate residues in Mis18 complex components in CENP-A loading. For chromosomes to faithfully segregate during cell division, CENP-A levels must be maintained at the centromere. How CENP-A levels are maintained is therefore important to understand at the mechanistic level. The Mis18 complex has been found to be important, but how exactly the various Mis18 complex components interact and how they regulate new CENP-A loading remains not fully understood. This study set out to characterize the critical residues using X-ray crystallography, negative staining EM, SEC analysis, molecular modeling (Raptorx, AlphaFold2, and AlphaFold-multimer) to identify the residues of Mis18a and Mis18b that are critical for the formation of the Mis18a/b hetero-hexamer and which residues are important for Mis18a and Mis18BP1 interactions. A complex beta-sheet interface dictates the Mis18a and Mis18b interactions. Mutating the Mis18a residues that are important for the Mis18a/b interactions resulted in impaired pull-down of Mis18b and reduced centromeric levels of mutated Mis18a. The functional consequences of mutating residues that impair Mis18a/b interactions is that with reduced centomeric levels of Mis18a, also impaired new CENP-A loading. Interestingly, mutated Mis18b did not impact centromeric Mis18a levels and only modestly impaired new CENP-A loading. These data were interpreted that Mis18a is critical for new CENP-A loading, whereas Mis18b might be involved in finetuning how much new CENP-A is loaded. Overall, it is a very well described and well written study with exciting data.
Major comments:
- Overall, the structural data and the IF data support the importance of Mis18a residues 103-105 are critical for centromeric localization and new CENP-A loading, whereas Mis18b residues L199 and I203 are critical for centromeric localization, but only very modestly impair centromeric Mis18a localization and new CENP-A loading. In the discussion the authors argue that the N-terminal helical region of Mis18a mediate HJURP binding. This latter is postulated based on published work, but not tested in this work. This should be clarified as such.
We thank the reviewer for this comment. Our very recent study aimed at understanding the licencing role of Plk1, independent of the work reported here, serendipitously has now validated this suggestion and demonstrates that a Plk1-mediated phosphorylation cascade activates the Mis18a/b complex via a conformational switch of the N-terminal helical region of Mis18a, which facilitates a robust HJURP-Mis18a/b interaction (Parashara et al. bioRxiv 2024). An independent study from the Musacchio lab (Conti et al. bioRxiv, 2024) also reports similar findings, mutually strengthening our independent conclusions. Overall, these studies highlight the importance of the critical structural insights into the Mis18 complex this study reports. We now explicitly discuss the validation of our original hypothesis by citing our recent work along with that of the Musacchio lab. The corresponding section of the last paragraph now reads as follows (page 17 line 10): "Previously published work identified amino acid sequence similarity between the N-terminal region of Mis18a and R1 and R2 repeats of the HJURP that mediates Mis18a/b interaction (Pan et al., 2019). Deletion of the Mis18a N-terminal region enhanced HJURP interaction with the Mis18 complex (Pan et al., 2019). Here, we show that the N-terminal helical region of Mis18a makes extensive contact with the C-terminal helices of Mis18a and Mis18b, which had previously been shown to mediate HJURP binding by Pan et al., 2019. Collectively these observations suggest that the N-terminal region of Mis18a might directly interfere with HJURP - Mis18 complex interaction. Two independent recent studies (Parashara et al., 2024, Conti et al., 2024) reveal that this is indeed the case and a Plk1-mediated phosphorylation cascade involving several phosphorylation and binding events of the Mis18 complex subunits relieve the intramolecular interactions between the Mis18a N-terminal helical region and the HJURP binding surface of the Mis18a/b C-terminal helical bundle. This facilitates robust HJURP-Mis18a/b interaction in vitroand efficient HJURP centromere recruitment and CENP-A loading in cells. Overall, these studies also highlight the importance of the critical structural insights into the Mis18 complex we report here."
- Overall, the authors clearly describe their data and methodology and use adequate statistical analyses. The structural data of the Mis18a/b complex being a hetero-hexamer is convincing, but the validation in vivo is missing. As structural experiment are not performed under physiological conditions, it is important to establish the stoichiometry in vivo to further support the totality of the findings of the structural experiments and modeling. The data for the hierarchical assembly of Mis18a and Mis18b at the centromere and its importance in new CENP-A loading is convincing. An additional open question is whether "old" centromeric CENP-A or HJURP:new CENP-A complex is needed to recruit Mis18a to the centromere and whether the identified residues have a role in Mis18a centromeric localization. These data would provide a solid link between the Mis18 complex and how it is directly linked to new CENP-A loading.
We agree that establishing the stoichiometry of Mis18 subunits of the Mis18 complex in vivo would be insightful. However, considering that the Mis18 complex assembles in a specific window of the cell cycle (late Mitosis and early G1), we think characterising the stoichiometry in cells is extremely difficult and technically challenging. However, consistent with our structural model, several lines of independent evidence (Pan et al., 2017 and Spiller et al., 2017) using different biophysical methods (Analytical Ultra Centrifugation (Pan et al., 2017), SEC-MALS (Spiller et al., 2017)) showed that recombinantly purified Mis18 complex (irrespective of the expression host, from both E. Coli or insect cells) is a hetero-octamer made of a hetero-hexameric Mis18a/b (4 Mis18a and 2 Mis18 b) complex bound to two copies of Mis18BP1. These observations suggested that hetero-hexamerisation of the Mis18a/b complex may be needed to bind and dimerise Mis18BP1 in cells. Previously published cellular studies support the in vivo requirement of the hetero-octameric Mis18 assembly as: (i) Perturbing the hetero-hexamerisation of the Mis18a/b complex (by introducing mutations at the Mis18a/b Yippee dimerisation interface, which while did not disrupt Mis18a/b complex formation, perturbed its hetero-hexamerisation and resulted in a hetero-trimeric Mis18a/b complex made of 2 Mis18aand 1 Mis18b) abolished Mis18BP1 binding in vitro and in cells, consequently abolished CENP-A deposition (Spiller et al., 2017) and (ii) artificial dimerisation of Mis18BP1, by expressing Mis18BP1 as a GST-tagged protein, enhanced the centromere localisation of Mis18BP1 highlighting the requirement of Mis18a/b hexameric assembly mediated dimerization of Mis18BP1 in cells (Pan et al., 2017). While these studies highlighted the importance of maintaining the right stoichiometry (hetero-octamer of 4 Mis18a, 2 Mis18b and 2 Mis18BP1), lack of structural information on how this essential biological assembly is established remained a major knowledge gap. Our work presented here fills this critical knowledge gap by showing that a segment of Mis18BP1 (aa 20-51) also binds at the Yippee dimerisation interface. To highlight this, we have included the following statements in the introduction on page 5 and 20 "Perturbing the Yippee domain-mediated hexameric assembly of Mis18a/b (that resulted in a Mis18a/b hetero-trimer, 2 Mis18a and 1 Mis18b) abolished its ability to bind Mis18BP1 in vitro and in cells (Spiller et al., 2017), emphasising the requirement of maintaining correct stoichiometry of Mis18a/b subunits. Consistent with this, artificial dimerisation of Mis18BP1, by expressing Mis18BP1 as a GST-tagged protein, enhanced the centromere localisation of Mis18BP1 (Pan et al., 2017)." and in the Results section on page 14 line 12: "Mis18BP120-51 contains two short b strands that interact at Mis18a/b Yippee interface extending the six-stranded-b sheets of both Mis18a and Mis18b Yippee domains. This provides the structural rationale for why Yippee domains-mediated Mis18a/b hetero-hexamerisation is crucial for Mis18BP1 binding (Spiller et al., 2017)."
Regarding the question "whether 'old' centromeric CENP-A or HJURP:new CENP-A complex is needed to recruit Mis18a centromere localisation and whether identified residues have a role in Mis18a centromere localisation": According to the published literature, the Mis18 complex associates with centromeres through interaction with CCAN components CENP-C and CENP-I (Shono et al., 2015, Dambacher et al., 2012, Moree et al., 2011, Hoffmann et al., 2020). Considering CCAN assembles on CENP-A nucleosomes, and HJURP:new CENP-A centromere recruitment depends on the Mis18 complex, it will be reasonable to argue that the 'old' centromeric CENP-A contributes to the centromere localisation of the Mis18 complex. Amongst the components of the Mis18 complex, Mis18BP1 and Mis18bhave previously been suggested to interact with CENP-C. Within the Mis18 complex, we (Spiller et al., 2017) and others (Pan et al., 2017) have shown that Mis18a can directly interact with Mis18BP1, but it does so more efficiently when Mis18a hetero-oligomerises with Mis18b via their Yippee domains. Here, our structural analysis mapped the interaction interfaces and showed that Mis18a residues E103, D104 and T105 contribute to Mis18BP1 binding, as mutating these residues abolishes centromere localisation of Mis18a (Fig. 5c and 5d). To accentuate our findings, we have now included the following paragraph in the discussion section (page 17 line 26): "One of the key outstanding questions in the field is how does the Mis18 complex associate with the centromere. Previous studies identified CCAN subunits CENP-C and CENP-I as major players mediating the centromere localisation of the Mis18 complex mainly via Mis18BP1 (Shono et al., 2015, Dambacher et al., 2012, Moree et al., 2011), although Mis18b subunit has also been suggested to interact with CENP-C (Stellfox et al., 2016). Within the Mis18 complex, we and others have shown that the Mis18a/b Yippee hetero-dimers can directly interact with Mis18BP1. Here our structural analysis allowed us to map the interaction interface mediating Mis18a/b-Mis18BP1 binding. Perturbing this interface on Mis18a completely abolished Mis18a centromere localisation and reduced Mis18BP1 centromere levels. These observations show that Mis18a associates with the centromere mainly via Mis18BP1, and assembly of the Mis18 complex itself is crucial for its efficient centromere association, as previously suggested. Future work aimed at characterising the intermolecular contact points between the subunits of the Mis18 complex, centromeric chromatin and CCAN components and understanding if the Mis18 complex undergoes any conformational and/or compositional variations upon centromere association and/or during CENP-A deposition process, will be crucial to delineate the mechanisms underpinning the centromere maintenance."
Minor comments:
- The bar graphs shown ideally also show the individual data points for the authros to appreciate the spread of the data. These figures can be replicated in the Supplemental to avoid making the main figures look too busy.
We thank the reviewers for this suggestion. Reviewer #3 made a similar comment and suggested we use Superplot, which allows visualisation of individual data points of independent experiments. We have now revised all bar graphs using Superplot to address both reviewers' suggestions.
Reviewer #2 (Significance (Required)):
- This study uses a broad range of structural techniques, including molecular modeling which were subsequently validated by in vitro pull-down assays, co-IP, and IF. This combination of these techniques is important because many structural techniques cannot be performed under physiological conditions. Validating the main findings of the structural results by IF and co-IP is therefore critical.
- This work greatly advances our structural understanding how Mis18a, Mis18b, and Mis18BP1 form the Mis18 complex and how the critical residues in especially Mis18a help the Mis18 complex localize to the centromere and influence new CENP-A loading. This study also provides the first strong evidence in hierarchical assembly of the Mis18 complex.
- How centromere identity is maintained is a critical question in chromosome biology and genome integrity. The Mis18 complex has been identified as an important complex in the process. Several structural and mutational studies (all adequately cited in this manuscript) have tried to address which residues guide the assembly and functional regions of the Mis18 complex. This work builds and expands our understanding how especially Mis18a holds a pivotal role in both Mis18 complex formation and its impact on maintaining centromeric CENP-A levels.
- This work will be of interest to the chromosome field in general and anyone studying the mechanism of cell division.
- Chromatin, centromere, CENP-A, cell division. This reviewer has limited expertise in structural biology.
Reviewer #3 (Evidence, reproducibility and clarity (Required)):
Centromere identity is defined by CENP-A loading to specific sites on genomic DNA. CENP-A loading is known to rely on the Mis18 complex, and several regulators are known; yet how the Mis18 complex achieves this complex process has remained puzzle. By elucidating the structural basis of Mis18 complex assembly using integrative structural approaches the authors show that multiple homo and heterodimeric interfaces of Mis18alpha, beta and Mis18BP1 are involved in centromere maintenance. The authors show that Mis18alpha can associate with centromeres and deposit CENP-A independent of Mis18 β. Mis18α functions in CENP-A deposition at centromeres independent of Mis18β. Mis18β is required for maintaining a specific level of CENP-A occupancy at centromeres. Thus, using structure-guided and separation-of-function mutants the study reveals how Mis18 complex ensures centromere maintenance. Major comments: This is an excellent study on centromere inheritance, combining structural and cell biology techniques. The comments here primarily refer to Cell biology aspect of the work.
Figures show that new CENP-A deposits in Mis18βL199D/I203D mutants, but the level was reduced moderately. Based on this observation, the authors make a strong conclusion that Mis18β licenses the optimal levels of CENP-A at centromeres. Mis18α may be essential for both CENP-A incorporation and depositing a specific amount of CENP-A, as Mis18α and CENP-A levels are both reduced in Mis18βL199D/I203D mutants which failed to form the triple helical assembly with Mis18α as shown in Figure 3B and 3C. The authors may want to qualify some of these claims as preliminary or speculative.
We thank the reviewer for this suggestion. We agree that although the reduction in CENP-A levels upon replacing WT Mis18b with Mis18b L199D/I203D is more prominent than the reduction in centromere localised Mis18a, one cannot completely rule out the contribution of reduced Mis18a on CENP-A loading. This also raises an interesting possibility where Mis18b ensures the correct amount of CENP-A deposition by facilitating the optimal level of Mis18a at centromeres. We now explicitly discuss this in the discussion as follows (page 16 line 26): "Whilst proteins involved in CENP-A loading have been well established, the mechanism by which the correct levels of CENP-A are controlled is yet to be thoroughly explored and characterised. The data presented here suggest that Mis18b mainly contributes to the quantitative control of centromere maintenance - by ensuring the right amounts of CENP-A deposition at centromeres - and maybe one of several proteins that control CENP-A levels. We also note that the Mis18b mutant, which cannot interact with Mis18a, moderately reduced Mis18a levels at centromeres, and hence, it is possible that Mis18b ensures the correct level of CENP-A deposition by facilitating optimal Mis18a centromere recruitment. Future studies will focus on dissecting the mechanisms underlying the Mis18b-mediated control of CENP-A loading amounts along with any other mechanisms involved."
This work and others show that phosphorylation of Mis18BP1 by CDK1 can interfere with complex function (Spiller et al., 2017, Pan et al., 2017). Does the structure provide any insight into PLK1-mediated phosphorylation surfaces for activation of the complex? If yes, a brief discussion would help to link CDK1 and PLK1 mediated opposing actions will strengthen the work.
As described in our response to the first major comment of Reviewer 2, our very recent study aimed at understanding the licencing role of Plk1, independent of the work reported here, identified and evaluated the functional contribution of Plk1 phosphorylation on the subunits of the Mis18 complex (Parashara et al., bioRxiv 2024). Serendipitously, this recent work has now validated our hypothesis proposed based on the structural characterisation reported here and demonstrates that a Plk1-mediated phosphorylation cascade activates the Mis18a/b complex via a conformational switch of the N-terminal helical region of Mis18a which facilitates a robust HJURP-Mis18a/b interaction (Parashara et al. bioRxiv 2024). An independent study from the Musacchio lab (Conti et al., bioRxiv 2024) also reports similar findings, mutually strengthening our independent conclusions. Overall, these studies highlight the importance of the critical structural insights into the Mis18 complex this study reports. We now explicitly discuss the validation of our original hypothesis by citing our recent work along with that of the Musacchio lab. The corresponding section of the last paragraph now reads as follows (page 17 line 10): "Previously published work identified amino acid sequence similarity between the N-terminal region of Mis18a and R1 and R2 repeats of the HJURP that mediates Mis18a/binteraction (Pan et al., 2019). Deletion of the Mis18a N-terminal region enhanced HJURP interaction with the Mis18 complex (Pan et al., 2019). Here, we show that the N-terminal helical region of Mis18a makes extensive contact with the C-terminal helices of Mis18a and Mis18b, which had previously been shown to mediate HJURP binding by Pan et al., 2019. Collectively these observations suggest that the N-terminal region of Mis18a might directly interfere with HJURP - Mis18 complex interaction. Two independent recent studies (Parashara et al., 2024, Conti et al., 2024) reveal that this is indeed the case and a Plk1-mediated phosphorylation cascade involving several phosphorylation and binding events of the Mis18 complex subunits relieve the intramolecular interactions between the Mis18a N-terminal helical region and the HJURP binding surface of the Mis18a/b C-terminal helical bundle. This facilitates robust HJURP-Mis18a/b interaction in vitro and efficient HJURP centromere recruitment and CENP-A loading in cells. Overall, these studies also highlight the importance of the critical structural insights into the Mis18 complex we report here."
I am happy with the way cell biology data and the methods are presented so that they can be reproduced. The experiments are adequately replicated and the statistical analysis adequate. It will help to include sample size of cells or centromeres used for building the graphs.
We have now included this information in figure legends of Fig. 3a, 3c, 4b, 4c, 5b, 5c and 5d.
This is a strong interdisciplinary study using a variety of in vitro and in vivo techniques. Can the authors discuss if they expect chromatin associated Mis18 complex to host a similar structure as the soluble one? In other words, are they able to comment on any key differences between chromatin and non-chromatin associated Mis18 complexes.
We thank the reviewer for the suggestion. We agree that one cannot rule out the possibility of the Mis18 complex undergoing compositional and/or conformational variations during the processes of CENP-A loading at centromeres. We now explicitly discuss this possibility in the last paragraph of the discussion section (page 18 line 10): "Future work aimed at characterising the intermolecular contact points between the subunits of the Mis18 complex, centromeric chromatin and CCAN components and understanding if the Mis18 complex undergoes any conformational and/or compositional variations upon centromere association and/or during CENP-A deposition process, will be crucial to delineate the mechanisms underpinning the centromere maintenance."
Minor comments: -
In cell biology experiments, fluorescence intensities could be presented as a superplot for added value across cells and repeats (instead of bar graphs). More on superplot:https://doi.org/10.1083/jcb.202001064.
We thank the reviewers for this kind suggestion. We have now included graphs made using 'superplot' as suggested.
In general, ACA levels do not appear to change significantly between WT and mutant expressing cells although new CENP-A loading is significantly absent in the presence of a few mutants - please comment if ACA used here can recognise CENP-A. Would this mean that old CENP-A remains normally?
We thank the reviewer for this comment. While new CENP-A incorporated at centromeres is selectively labelled using the SNAP-tag, the ACA antibody used in these experiments can recognise CENP-A, CENP-B and CENP-C, with CENP-B being the primary target (Kallenberg, Clinical Rheumatology,1990). We would also like to note that ACA has commonly been used to locate the centromere in CENP-A loading assays where new CENP-A levels are assessed via selective labelling (e.g. McKinley 2014).
It is unclear whether any of the mutant acted in a dominant negative fashion in the presence of endogenous Mis18 proteins. It would have been useful to test this particularly in the context of mis18alpha mutants that seem to fully abolish new CENP-A recruitment.
As Mis18 subunits oligomerise (homo and hetero), we thought expressing these mutants in the presence of endogenous proteins might interfere with endogenous protein in a heterogenous manner and might make the interpretation difficult. Hence, we did not test this. Instead, as described in the manuscript we have tested these mutants in siRNA rescue experiments (Fig. 3, 4 and 5).
In figure 3a, GFP panel (input lane, 1) is shown to mark a band corresponding to GFP. Is this expected? Please comment.
Yes, as a control, an empty vector was transfected to express just GFP along with Mis18a-mCherry. These were used to show that there was no unspecific interaction between the beads used for IP or Mis18a-mCherry and GFP tag, and that any interaction seen was due to Mis18b. A similar control was used in S4b, where mCherry was expressed along with Mis18b-GFP. We have now clarified this in the corresponding legends of Fig. 4a and S4b.
Would be useful to have the scale for the cropped images presented as insets. Figure 4B should read YFP and not YPF.
We apologise for this typographical error. We have now corrected this.
The authors may want to explain whether the tag differences matter for their study (Case in point: His-SUMO-Mis18a191-233 WT and mutant His-MBP-Mis18b188-229 proteins).
The MBP tag was chosen to perform amylose pull-down assays, whereas the SUMO tag was chosen to increase the protein size. This is crucial as the C-terminal fragments of Mis18a and Mis18b are less than 50 amino acids long and are not easy to visualise by the band intensity in the Coomassie-stained SDS PAGE gels.
Reviewer #3 (Significance (Required)):
This work elucidates the structural basis of Mis18 complex assembly and the intermolecular interfaces essential for Mis18 functions. This is a significant advance in the field as it helps researchers in the field better understand CENP-A deposition and mechanism underpinning the maintenance of centromere identity. This is a broad area of research benefitting those studying cell division, genome stability, centromere identity and epigenetics might all be interested in and influenced by these findings. Novelty and strength lies in combining structural and cell biology work. Strengths of the work are structural details of the Mis18 complex. Minor weakness is the link between Mis18 structure and Centromere inheritance is limited to one immunostaining assay (I have mentioned this as a minor comment because addressing this may not be within the scope of this manuscript and is likely to require a repeat of a vast majority of the work with additional reagents which may not directly add value to the current manuscript).
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- Feb 2024
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Reply to the reviewers
Manuscript number: RC-2023-02270
Corresponding author(s): Usha Vijayraghavan
General Statements
We thank all three Reviewers for their thorough assessment of our manuscript and their constructive feedback and comments.
Point-by-point description of the revisions
This section is mandatory. *Please insert a point-by-point reply describing the revisions that were already carried out and included in the transferred manuscript. *
Reviewer #1
We are encouraged by the very positive comments made on the significance of our study that it provides convincing insights on alternative modes of nuclear positioning and division which is an important question in cell biology. We also took all possible suggestions to improve the interpretation of our results, have also added some newer data to address the constructive points raised by the reviewer.
Major comments:
- A) I am concerned about the lethal phenotype caused by slu7 deprivation. Slu7 deficiency causes defective nuclear positioning at the bud in late G2. This phenotype per se should not cause defective mitosis, so slu7 deficiency may also be interfering with other aspects of mitosis which might indeed impinge on cell viability.
Response: Our data indeed show Slu7 knockdown has severe growth defect when grown on non-permissive media (YPD) where a two-fold difference in O.D. was seen by 12 hours (Supplementary figure 2.B).
We agree with the reviewer that defective mitosis, arises from several aspects of cell cycle including those in mitosis. The data we present show G2 arrest, small-budded cells with unsegregated nuclei and large-budded cells with segregated nuclei, all which do not progress through cell cycle phases and contribute to the severe growth defect. Further, GO enrichment analysis of deregulated pathways on knockdown of Slu7 support the above findings as various cell cycle related pathways are abnormal in their expression levels. In this study, we have focused on an in depth analysis of the role of Slu7 in a particular window and uncover how it controls nuclear position for progress G2-M phase cell cycle progression. The likely targets and mechanisms by which Slu7 regulates other phases of the cell cycle which needs similar other deeper investigations in future. Our detailed analysis of nuclear movement in Slu7 knockdown cells grown in YPD for 12 hours showed no nuclear movement (Supplementary figure 3B) which is the terminal phenotype. To examine events that lead to nuclear mispositioning phenotype we investigated the dividing slu7kd cells grown in non-permissive media for only 6 hours; under these conditions Slu7 protein is still detected at lower amount (Supplementary figure 1D). From the studies of nuclear position, mitotic spindle position and dynein distribution in mother and daughter cell, we propose that in the dividing cells, the nucleus does not experience enough force to move inside the daughter bud during mitosis. Further, we delineate the role of Slu7 in the splicing of transcripts for PAC1 encoding a protein whose homolog in S. cerevisiae has a proven role in nuclear migration. In live imaging of slu7kd cells that show nuclear segregation at the start of live imaging, new bud was not formed till the end of 60 minutes, implying that are arrested after transition to mitosis. We could speculate a role for Slu7 through regulation of genes involved in mitotic exit or cytokinesis.
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B) Supp. Fig4 shows defective mitosis in TBZ, so TBZ may be exacerbating defective mitosis of slu7-deficient cells.
__Response: __Studies with yeast and mammalian model systems have revealed that the mobility and repair of damaged DNA are compromised upon disruption of microtubules (Wu et al, 2008; Chung et al, 2015; Lottersberger et al, 2015; Lawrimore et al, 2017; Oshidari et al, 2018; Laflamme et al, 2019). These data point to reasons why the mutants in DNA damage checkpoint genes are sensitive to TBZ. In this context, we observed that CnSlu7 knockdown is also sensitive to MMS stress (shown below). In addition, recent work on human Slu7 in Hela cell lines has elucidated the its role in the maintenance of genome integrity by preventing the formation of R-loops (Jiménez et al, 2019). We suggest that TBZ may exacerbate the defective mitosis of Slu7 depleted cells, however, whether it is particular only to mitosis or to the other cellular processes where the microtubules are involved needs further investigation.
Throughout the figures it can be observed uneven chromosome/nuclear segregation in cells deprived of slu7, however, these mitotic defects have not been mentioned or explored in depth. From Supp Figure 3C it can be inferred that CENP-A segregation is uneven. Is this correct? Is CENP-A-GFP segregation normal?
__Response: __ It should be noted that in Cryptococcus, the kinetochore remains unclustered during the early phase of cell cycle, cluster to a single punctum at the end of G2 phase and then de-cluster at the end of mitosis. Since this is a highly dynamic process, its technically challenging to measure the intensity CENP-A in mother and daughter cell. In the fixed cell imaging or live imaging data, there are no appreciable differences in intensity of the GFP signal of the tagged proteins (H4 and CENPA). The uneven chromosome/nuclear segregation observed in certain panels images presented are due to technical issues in that particular stack while generating the montage. This has been re-examined and we infer that there are no major differences in the signals from GFP-H4 and GFP - CENPA through mitosis.
Additionally, taking the cue from the reviewer’s comment, we examined the likelihood of improper chromosome segregation by evaluating if there are any appreciable cell populations that are aneuploid. We revisited our flow cytometry data, we found no significant difference in the population of aneuploid cells between the knockdown strain and wildtype strain grown in non-permissive condition for 12 hours. This data was assessed again in new experiments where we also analyzed by flow cytometry the ipl1 mutant where aneuploidy is reported (Varshney et al, 2019). It has been reported in Cryptococcus neoformans that aneuploid cells are resistance to anti-fungal drug fluconazole. Preliminary experiments showed that slu7kd cells were sensitive to fluconazole and in this assay were similar to wildtype cells. Hence, we speculate that chromosome segregation is normal in Slu7 depleted cells.
If chromosome segregation is altered upon slu7 deprivation, this might also explain the drop in cell viability and slow growth rates of this condition.
__Response: __ From live microscopy imaging and flow cytometry data, we believe that the chromosome segregation is normal in Slu7 depleted cells. Dilution spotting in permissive media after growth in non-permissive media revealed that slu7kd cells resumed growth without losing viability, indicating the arrest phenotype associated with the depletion of Slu7 is largely reversible and does not cause chromosome mis-segregation (figure is now added to manuscript as supplementary figure 2D). Prolonged arrest at various cell cycle phase might lead to cell death and hence drop in cell viability.
The manuscript will improve if authors analyse chromosome segregation for example, by showing time-lapse images of chromosome dynamics during mitosis.
__Response: __Chromosome dynamics during the mitotic phase is given below. We observe that the chromosome segregation is equal in both mother and daughter bud. The uneven chromosome/nuclear segregation observed in certain panels images presented in original manuscript were due to technical issues while generating the montage.
The authors perform an RNA seq comparing wild-type cells with slu7 deficiency and detect changes in gene expression, however, they do not explore from this data the percentage of un-spliced introns genome-wide which might be very informative, even more than changes in gene expression, which many of them, might be an indirect consequence of Slu7 deficiency. Authors should re-analyze the RNA seq data looking for unprocessed mRNAs and provide information about the overall impact of slu7 in intron processing.
__Response: __ A very detailed bioinformatic analysis of the impact on slu7 on global transcriptome and splice pattern, is an ongoing study in the laboratory. The findings are indeed giving good leads which are being validated by further experiments using mini-gene exon-intron constructs. These studies are extensive and form a future manuscript identifying and characterizing intronic features which predispose an intron towards Slu7 dependency. Therefore, it falls outside the scope for this study on the cell biological role of Slu7 on mitosis, specifically nuclear position to ensure faithful mitotic segregation.
Minor comments:
__ __1. "Previous studies of slu7 mutants in S. cerevisiae and the conditional knockdown of its S. pombe homolog". Consider replacing homolog with Ortholog.
Response: The suggestion is well taken, and the word “homolog” has been replaced with word “ortholog”.
- A) Taking these results together, we conclude that the inability of the conditional mutant to grow in the non-permissive media is due to impaired progression through the G2-M phase of the cell cycle. Is the G2/M delay the cause of the slow growth phenotype of the Slu7 deficiency?
Response: From the live microscopy, we note that even when the budding index for mitosis has been reached the nucleus in slu7kd cells is still in the mother cell and spends more time here rather than reaching the bud or bud neck. We present G2/M delay as ONE of the reasons for the slow growth of Slu7 depleted cells. Although we have showed that Slu7 depletion does not activate MAD2 dependent Spindle Assembly Checkpoint, we have not investigated the activation of other cell cycle checkpoints such as G2 DNA damage checkpoint. These are potential new leads as we infer from our RNA seq datasets that CHK1, TEL1, BDR1 and RAD51 show increased expression in Slu7 knockdown condition when compared to wildtype. It is therefore reasonable to conclude that Slu7 might play a role at various cell cycle phases through direct or indirect effect on genes involved in these phases. Delayed positioning of the nucleus during G2/M is one of the major effects that is investigated in depth in this study.
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B) If so, growth defects of slu7 deficiency could be suppressed by ectopic expression of G2/M activators.
Response: We have not tested this possibility, but we predict that expression of G2/M activators would at best offer only partial rescue the growth defect of Slu7 depleted cells since multiple pathways are adversely affected in cells depleted of Slu7.
In this line of investigation, we have tested the consequences of PAC1 overexpression, as PAC1 expression levels and splicing are affected by loss of Slu7. We report a partial rescue of nuclear position defect during mitosis, yet these cells were arrested at cytokinesis. Further, the unavailability of an array of suitable auxotrophic (or other) markers in this model system makes it technically challenging to do rescue experiments by overexpression of multiple candidate downstream genes.
Supp Figure 3C, remove the drawing on the right. Adjust times relative to panels.
Response: The drawing has been removed and the time points have been adjusted.
- Tracking the nucleus in wild-type cells with a small bud showed that the nucleus moved into the daughter bud, divided into two, and one-half migrated to the mother bud (Supplementary Figure 3B, top row).
Please replace the sentence: "one-half" with "one of the daughter nuclei". Additionally, as this nuclear positioning occurring during late mitosis is due to spindle elongation, I would not use the term migrated but "positioned" or "moved". Nuclear movement into the bud, which is referred to as "moved", can indeed be named "migrated".
Response: The word “migrated” in the above sentence has been replaced with the word “moved”.
- Indicates in Figure 2B the marker used (GFP-H4), as in Fig Supp 3B.
Response: The marker has been indicated in the figure.
- Nuclear division initiates in the bud, and one of the divided nuclei with segregated chromosomes migrates back to the mother cell (Figure 2B, top panel, wildtype, quantified in Figure 2C grey bar).
As mentioned before, I would not name this, nuclear migration as it is the result of spindle elongation, and it can be confusing or misleading for non-expert readers.
Response: The word “migrate” in the above sentence has been replaced with the word “move”.
- These two conclusions should be revised and described in temporal/sequential order.
- Thus, we identify that the depletion of CnSlu7 severely affects the temporal and spatial sequence of events during mitosis, particularly nuclear migration and division.
- Together, these results confirmed that without affecting the kinetochore clustering, depletion of Slu7 affects nuclear migration during the G2 to mitotic transition in Cryptococcus neoformans.
Response: We thank the reviewer for bringing out the clarity in the concluding statements. These has now been revised to read as follows:
“Together, these results confirm that without affecting the kinetochore clustering, depletion of Slu7 affects nuclear movement during the G2 to mitotic transition in Cryptococcus neoformans. Thus, we identify that the depletion of CnSlu7 severely affects the temporal and spatial sequence of events during mitosis, particularly nuclear migration, and division.”
- In slu7d cells, in cells with small buds, numerous cMTs were nucleated from the MTOCs, and as the cell cycle progressed, they organized to form the unipolar mitotic spindle (Figure 3A, slu7kd GFP-TUB1 panel, time point 55 mins).
Please, revise whether the term unipolar mitotic spindle is correct here.
Response: The word unipolar has been removed.
- I suggest including page and line numbers in the manuscript to facilitate revision.
Response: We regret missing out this formatting guideline. The Page and line numbers have provided.
Reviewer #2
We are thankful by the very positive comments on the significance of our work, its novelty and findings being of broad interest to microbiology; splicing; cell cycle and cell division communities. We respond to all comments raised below.
- The authors test the Mad2-dependent spindle assembly checkpoint and show that it is not relevant for slu7-depletion. This is as expected if the defect is in nuclear positioning. They could test other checkpoint pathways that would monitor nuclear positioning in budding yeasts. Perhaps they have considered this: Bub2, Bfa1, Tem1, Lte1 mutants? I don't think this experiment is essential for publication, but it could strongly support their model.
Response: We appreciate the comment on other checkpoints operating during mitosis. However, we have not done these experiments to examine role of components that arrest mitosis (Bub2, Tem1 etc.) in response to spindle or kinetochore damage. We hope the reviewer appreciates that this line of work would require the generation of bub2Δ strain and extensive characterization for their role in checkpoint in Cryptococcus before it can be brought into strains compromised for Slu7.
__ Minor comments:__ 1. in Figure 3, Dyn1-GFP is imaged and in many of the cells in which Slu7 is depleted, nothing (or very little) can be seen. It is later argued that this is an indirect effect, due to defects in Pac1 and associated functions. Have the authors attempted a Dynein western blot (the 3xGFP tag should be quite sensitive)? It would be good to demonstrate that the Dynein motor complex hasn't simply fallen apart and Dynein been degraded in the slu7-depletion.
Response: A study in S. cerevisiae has reported the dynein expression does not change in pac1Δ cells (Lee et al., 2003). Since the molecular weight of CnnDYN1 along with the tag is 630kDa, we did attempt the very challenging experiment of western blot to check for the expression levels this very large protein in wildtype and slu7kd cells. Based on the reviewer’s suggestion, we have attempted dot blot of protein lysates from wild type and from slu7kd cells probed with anti GFP antibody for estimating DYN-GFP levels. Untagged WT H99 strain was used as negative control. The same blot was stripped and re-probed for PSTAIRE which served as a loading control. This experiment revealed that dynein levels are same in both wildtype and slu7kd cells.
in Figure 7: have any intronless genes been tested for rescue of the post-mitotic delay/arrest? This is not necessary for publication, but if any have been tested already, they could be listed here.
Response: We have not tested intronless genes for their role in the rescue of post mitotic delay/arrest. From the RNA seq data, we observed that most of the genes involved in mitotic exit network (MEN) and cytokinesis were highly expressed in slu7kd cells as compared to the wildtype indicating and indirect role for Slu7 in their expression level. So, we had validated three candidates MOB2, CDC12 and DBF2 by qRT PCR (Supplementary 7.D) and found they were upregulated in slu7kd cells and hence speculate that deregulation of these transcript could contribute to the post mitotic arrest in slu7kd.
In SFig2C legend make it clear that these cells are HU arrested at time zero. Are the cells in glucose or galactose during HU treatment.?
Response: We regret the lack of clarity in the legend and the required details have been added. The cells were initially grown in non-permissive media for 2 hours to deplete Slu7 and then HU was added to the non-permissive media and the cell were allowed to grow for 4 hours.
in SFig4, the TBZ sensitivity isn't very convincing as the slu7kd strain is struggling to grow at all on YPD.
Response: We agree with the reviewer comment on the growth of slu7kd cells on media YPD containing TBZ. TBZ may exacerbate the defective mitosis of Slu7 depleted cells, however whether it pertains only to mitosis or any cellular processes where microtubules are involved requires further investigation.
In SFig5 legend the volcano plot needs to be better explained. What are the dashed lines etc. ?
Response: We regret missing these details on the volcano plot which has now been added to the legend.
__Reviewer #3 __
We appreciate the views that our work provides strong evidence to support out conclusions that Cryptococcus neoformans Slu7 controls mitotic progression by efficient splicing of cell cycle regulators and cytoskeletal elements. We have taken all comments of the reviewer into account to revise our manuscript with additional data, and by improving the presentation. The key additional data are summarized below.
Major comments:
1) The authors claimed that CnSlu7 is the most divergent among the fungal homologs and closer to its human counterpart (Fig. 1A, Supplementary Fig 1A). -Just based on the phylogenetic tree including limited members, as in Supplementary Fig. 1, it cannot be concluded that CnSlu7 is closer to its human counterpart since the basidiomycete yeast such as C. neoformans itself is more closely positions to humans compared to the ascomycete yeasts S. cerevisiae and Sch. pombe in phylogenetic tree analysis. It is strongly recommended to include other fungal species from the Basidiomycota, such as Ustilago maydis, in phylogenetic analysis in Supplementary Fig. 1. - Conservation analysis among diverse eukaryotes is more meaningful data that the conservation withing the fungi group, so that it is recommended that the data of Fig. 1 A would be replaced with the revised Supplementary Fig 1. -The analysis data on amino acid identities among Slu7 homologues should be presented to support the claim.
Response: We agree with the reviewer that our data would be better served by an improved analysis of the phylogenetic relationship between various Slu7 homologs. We have therefore reconstructed the phylogenetic tree by including other fungal groups. This is presented here and also in the revised manuscript Supplementary Figure 1A. These data too, show that Cryptococcus (deneoformans and neoformans) Slu7 is the most diverged among its homologs from various fungal species with its closest homologs being other pathogens Puccinia graminis and Ustilago maydis.
2) Despite that CnSlu7 is the main key subject, the comparative analysis of CnSlu7 to the previously reported Slu7 homologues, in the aspect of functional domain organization, is not provided in the present manuscript. - It was reported that Slu7 contains the four motifs that control its cellular localization and canonical function as a splicing factor, such as a nuclear location signal, a zinc knuckle motif, four stretches of leucine repeats and a lysine-rich domain. Notably, human Slu7 protein is 204 amino acids longer than S. cerevisiae homolog with only 24% identity in the zinc knuckle motif (Molecular Biology of the Cell Vol. 15, 3782-3795). Thus, it is strongly recommended to provide additional information on the conserved and diverged features of CnSlu7 compared to other Slu7 homologs as a part of revised Figure.
Response: The multiple sequence alignment of Cryptococcus neoformans Slu7 with its fungal and higher eukaryote homologs such as human Slu7 and plant Slu7 proteins revealed that only the CCHC zinc finger motif is highly conserved. We do not detect conservation in the nuclear localization signal, stretch of leucine repeats and lysine rich domain except for leucine 3 stretch near the C terminal. This additional information is presented in revised Figure 1A.
3) The manuscript clearly demonstrated that one of key targets of Slu7-mediated splicing is PAC1 in C. neoformans. Considering, Pac1 is also conserved from S. cerevisiae to human, it could be speculated that the defect of Slu7 can affect nuclear migration in other fungal species and human cells by inefficient splicing of PAC1, despite striking differences in their nuclear position during cell division. Please discuss this possibility or provide the qRT-PCR analysis data of PAC1 homologs in the available fungal Slu7 mutant strains.
Response: Cell cycle arrest phenotypes of splicing factor mutants (studied largely in budding and fission yeast) results from inefficient pre-mRNA splicing of cell cycle-related genes. Slu7 is a well characterized second step splicing factor in S. cerevisiae where in vitro splicing assays with ACT1 minigene transcripts with a modified single intron showed ScSlu7 is dispensable for splicing when the branchpoint to 3'SS distance is less than seven nucleotides in the mini transcript (Brys and Schwer, 1996). In fission yeast we reported the effects of metabolic depletion of Slu7, which is an essential gene (Banerjee et al., 2013) and showed unexpectedly that in addition to BrP to 3'SS distance new intronic features contributors of dependency of fission yeast intron containing transcripts on Slu7 functions. The work also showed in multi-intronic transcripts its role is intron-specific and thus the candidate gene/ transcript is likely to be to dependent on Slu7 by virtue of the intronic features and not its biological function. In this study a splicing dependent role of CnSlu7 in cell cycle progression is investigated where based on a strong nuclear mis-positioning phenotype we narrowed on PAC1 transcripts as one of targets. We show PAC1, encoding a cytoskeletal factor, has introns dependent on CnSlu7 for efficient splicing and show partial rescue of nuclear position in strain complemented with expression of an intronless PAC1 gene. In this scenario, while it is likely that in other species where PAC1 exon-introns nucleotide sequences are similar to that in Cryptococcus a role for Slu7 may be predicted, for validation by other experimentalists.
Interestingly, PAC1 in S. cerevisiae is an intronless gene and its homolog is not annotated in S. pombe. In human cell lines, knockdown of Slu7 by siRNA resulted in metaphase arrest by inefficient splicing of soronin – which is crucial in sister chromatid cohesion and correct spindle assembly, according to recent research in human cell lines (Jiménez et al., 2019).
Hence the roles of splicing factor in cell cycle is through splicing of targets involved in cell cycle wherein the targets regulated by splicing factor may or may not be conserved in other species.
Minor comments:
General points 1) Provide information on the marker sizes in the data of qRT-PCR analysis presented in Figures 5 and 6, and Supplementary Fig 2A.
Response: We regret the omission of this technical data and have corrected the same by providing the marker sizes in all the figures.
2) Please unify the format of gene names. Some genes were written with superscript of "+", such as CLN1+ and PAC1+ in Fig. 4. What does "+" mean in the gene names?
Response: We have taken the suggestion to carefully review the nomenclature of genes and their expressed transcripts as is typical for Cryptococcus neoformans. To depict the wildtype form of transcript we had used +. Thus CLN1+ was used to denote Cyclin 1 cellular transcript from expressed from its own locus without any modification of promoter or the intronic features.
3) Supplementary Figure 1 C: Please correct "Slu7KD" 6 hrs YPD to "slu7kd" 6 hrs YPD.
Response: This error has been corrected.
4) Supplementary Figure 2A: What do "mRNA" and "No RT29X/", respectively, indicate?
Response: The mRNA indicates the spliced form across any intron after intron is spliced out, so denotes exon-exon sequences in the mRNA. The reactions marked as “No RT 29 X” denote semi- quantitative PCR performed on DNase treated RNA sample, without reverse transcription to generate the cDNA. These reactions were done to confirm that there is no genomic DNA present in the RNA sample used for reverse transcription reaction of the cellular transcripts. Some of these details are now included in the Supp Fig 2A legend.
5) Supplementary Figure 4C: Please provide brief explanation in the text on why the authors employed mad2Δ slu7kd cells.
Response: In Page 8, line 6, we had provided the rationale for generating and studying mad2Δ slu7kd strain. This is recapitulated below:
“To investigate whether Slu7 knockdown triggers the activation of spindle assembly checkpoint (SAC), we generated a strain with conditional slu7kd in cells with mad2Δ allele and the GFP-H4 nuclear marker.”
6) Supplementary Figure 6D legend: Please correct the description of "slu7kd SH:Slu7 FL" from "expressing intronless PAC1" to "expressing full length of SLU7".
Response: The error in the legend is regretted and this has been corrected.
7) Supplementary Figure 7D: The authors confirmed that MOB2, CDC12, and DFB1 were expressed at higher levels in slu7kd when compared to wildtype. Please briefly explain in the text why the expression level of these genes in slu7kd was mentioned.
Response: slu7kd cells expressing intronless Pac1 arrest post nuclear division. Revisiting our transcriptomic data, we found that genes involved in mitosis exit network and cytokinesis, such as DFB1, MOB2, CDC12, BUD4, and CHS2, were deregulated in slu7kd when compared to wildtype. We confirmed the same by performing qRT PCRs for three candidates, MOB2, DBF1 and CDC12 and that these transcript were expressed at high levels in knockdown when compared to wildtype.
8) The species name should be written as abbreviation after the first mention. For example, please correct Cryptococcus neoformans to C. neoformans throughout manuscript.
Response: The suggestion is well taken, and the required edits have been made throughout the text.
9) Please unify the format of paper titles listed in References.
Response: This formatting error is regretted and corrected to have all references in a single format.
10) No page information for Hoffmann et al (2010) in References.
Response: This omission is corrected.
11) Update the information on the published journal of Chatterjee et al. (2021) in References.
Response: This omission is regretted and is now corrected.
12) Information on the authors, title, published journal and pages should be provided for the papers (Yadav and Sanyal, 2018; Sridhar et al., 2021) in Supplementary Table 1, which were not included in the main Reference list.
Response: The references are now added to the main list.
References used for addressing the reviewer’s comments:
- Chung DKC, Chan JNY, Strecker J, Zhang W, Ebrahimi-Ardebili S, Lu T, Abraham KJ, Durocher D, Mekhail K (2015) Perinuclear tethers license telomeric DSBs for a broad kinesin- and NPC-dependent DNA repair process. Nat Commun doi:10.1038/NCOMMS8742.
- Jiménez M, Urtasun R, Elizalde M, Azkona M, Latasa MU, Uriarte I, Arechederra M, Alignani D, Bárcena-Varela M, Alvarez-Sola G et al (2019) Splicing events in the control of genome integrity: Role of SLU7 and truncated SRSF3 proteins. Nucleic Acids Res 47: 3450–3466. doi:10.1093/nar/gkz014.
- Laflamme G, Sim S, Leary A, Pascariu M, Vogel J, D’Amours D (2019) Interphase Microtubules Safeguard Mitotic Progression by Suppressing an Aurora B-Dependent Arrest Induced by DNA Replication Stress. Cell Rep 26: 2875-2889.e3. doi:10.1016/J.CELREP.2019.02.051.
- Lawrimore J, Barry TM, Barry RM, York AC, Friedman B, Cook DM, Akialis K, Tyler J, Vasquez P, Yeh E et al (2017) Microtubule dynamics drive enhanced chromatin motion and mobilize telomeres in response to DNA damage. Mol Biol Cell 28: 1701–1711. doi:10.1091/MBC.E16-12-0846.
- Lee WL, Oberle JR, Cooper JA (2003) The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J Cell Biol. doi:10.1083/jcb.200209022.
- Lottersberger F, Karssemeijer RA, Dimitrova N, De Lange T (2015) 53BP1 and the LINC Complex Promote Microtubule-Dependent DSB Mobility and DNA Repair. Cell 163: 880–893. doi:10.1016/J.CELL.2015.09.057.
- Oshidari R, Strecker J, Chung DKC, Abraham KJ, Chan JNY, Damaren CJ, Mekhail K (2018) Nuclear microtubule filaments mediate non-linear directional motion of chromatin and promote DNA repair. Nat Commun doi:10.1038/S41467-018-05009-7.
- Varshney N, Som S, Chatterjee S, Sridhar S, Bhattacharyya D, Paul R, Sanyal K (2019) Spatio-temporal regulation of nuclear division by Aurora B kinase Ipl1 in Cryptococcus neoformans. PLoS Genet doi:10.1371/journal.pgen.1007959.
- Wu G, Zhou L, Khidr L, Guo XE, Kim W, Lee YM, Krasieva T, Chen PL (2008) A novel role of the chromokinesin Kif4A in DNA damage response. Cell Cycle 7: 2013–2020. doi:10.4161/CC.7.13.6130.
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Author Response
The following is the authors’ response to the original reviews.
eLife assessment:
This important study represents a comprehensive computational analysis of Plasmodium falciparum gene expression, with a focus on var gene expression, in parasites isolated from patients; it assesses changes that occur as the parasites adapt to short-term in vitro culture conditions. The work provides technical advances to update a previously developed computational pipeline. Although the findings of the shifts in the expression of particular var genes have theoretical or practical implications beyond a single subfield, the results are incomplete and the main claims are only partially supported.
The authors would like to thank the reviewers and editors for their insightful and constructive assessment. We particularly appreciate the statement that our work provides a technical advance of our computational pipeline given that this was one of our main aims. To address the editorial criticisms, we have rephrased and restructured the manuscript to ensure clarity of results and to support our main claims. For the same reason, we removed the var transcript differential expression analysis, as this led to confusion.
Public Reviews:
Reviewer #1:
The authors took advantage of a large dataset of transcriptomic information obtained from parasites recovered from 35 patients. In addition, parasites from 13 of these patients were reared for 1 generation in vivo, 10 for 2 generations, and 1 for a third generation. This provided the authors with a remarkable resource for monitoring how parasites initially adapt to the environmental change of being grown in culture. They focused initially on var gene expression due to the importance of this gene family for parasite virulence, then subsequently assessed changes in the entire transcriptome. Their goal was to develop a more accurate and informative computational pipeline for assessing var gene expression and secondly, to document the adaptation process at the whole transcriptome level.
Overall, the authors were largely successful in their aims. They provide convincing evidence that their new computational pipeline is better able to assemble var transcripts and assess the structure of the encoded PfEMP1s. They can also assess var gene switching as a tool for examining antigenic variation. They also documented potentially important changes in the overall transcriptome that will be important for researchers who employ ex vivo samples for assessing things like drug sensitivity profiles or metabolic states. These are likely to be important tools and insights for researchers working on field samples.
One concern is that the abstract highlights "Unpredictable var gene switching..." and states that "Our results cast doubt on the validity of the common practice of using short-term cultured parasites...". This seems somewhat overly pessimistic with regard to var gene expression profiling and does not reflect the data described in the paper. In contrast, the main text of the paper repeatedly refers to "modest changes in var gene expression repertoire upon culture" or "relatively small changes in var expression from ex vivo to culture", and many additional similar assessments. On balance, it seems that transition to culture conditions causes relatively minor changes in var gene expression, at least in the initial generations. The authors do highlight that a few individuals in their analysis showed more pronounced and unpredictable changes, which certainly warrants caution for future studies but should not obscure the interesting observation that var gene expression remained relatively stable during transition to culture.
Thank you for this comment. We were happy to modify the wording in the abstract to have consistency with the results presented by highlighting that modest but unpredictable var gene switching was observed while substantial changes were found in the core transcriptome. Moreover, any differences observed in core transcriptome between ex vivo samples from naïve and pre-exposed patients are diminished after one cycle of cultivation making inferences about parasite biology in vivo impossible.
Therefore, – to our opinion – the statement in the last sentence is well supported by the data presented.
Line 43–47: “Modest but unpredictable var gene switching and convergence towards var2csa were observed in culture, along with differential expression of 19% of the core transcriptome between paired ex vivo and generation 1 samples. Our results cast doubt on the validity of the common practice of using short-term cultured parasites to make inferences about in vivo phenotype and behaviour.” Nevertheless, we would like to note that this study was in a unique position to assess changes at the individual patient level as we had successive parasite generations. This comparison is not done in most cross-sectional studies and therefore these small, unpredictable changes in the var transcriptome are missed.
Reviewer #2:
In this study, the authors describe a pipeline to sequence expressed var genes from RNA sequencing that improves on a previous one that they had developed. Importantly, they use this approach to determine how var gene expression changes with short-term culture. Their finding of shifts in the expression of particular var genes is compelling and casts some doubt on the comparability of gene expression in short-term culture versus var expression at the time of participant sampling. The authors appear to overstate the novelty of their pipeline, which should be better situated within the context of existing pipelines described in the literature.
Other studies have relied on short-term culture to understand var gene expression in clinical malaria studies. This study indicates the need for caution in over-interpreting findings from these studies.
The novel method of var gene assembly described by the authors needs to be appropriately situated within the context of previous studies. They neglect to mention several recent studies that present transcript-level novel assembly of var genes from clinical samples. It is important for them to situate their work within this context and compare and contrast it accordingly. A table comparing all existing methods in terms of pros and cons would be helpful to evaluate their method.
We are grateful for this suggestion and agree that a table comparing the pros and cons of all existing methods would be helpful for the general reader and also highlight the key advantages of our new approach. A table comparing previous methods for var gene and transcript characterisation has been added to the manuscript and is referenced in the introduction (line 107).
Author response table 1.
Comparison of previous var assembly approaches based on DNA- and RNA-sequencing.
Reviewer #3:
This work focuses on the important problem of how to access the highly polymorphic var gene family using short-read sequence data. The approach that was most successful, and utilized for all subsequent analyses, employed a different assembler from their prior pipeline, and impressively, more than doubles the N50 metric.
The authors then endeavor to utilize these improved assemblies to assess differential RNA expression of ex vivo and short-term cultured samples, and conclude that their results "cast doubt on the validity" of using short-term cultured parasites to infer in vivo characteristics. Readers should be aware that the various approaches to assess differential expression lack statistical clarity and appear to be contradictory. Unfortunately, there is no attempt to describe the rationale for the different approaches and how they might inform one another.
It is unclear whether adjusting for life-cycle stage as reported is appropriate for the var-only expression models. The methods do not appear to describe what type of correction variable (continuous/categorical) was used in each model, and there is no discussion of the impact on var vs. core transcriptome results.
We agree with the reviewer that the different methods and results of the var transcriptome analysis can be difficult to reconcile. To address this, we have included a summary table with a brief description of the rationale and results of each approach in our analysis pipeline.
Author response table 2.
Summary of the different levels of analysis performed to assess the effect of short-term parasite culturing on var and core gene expression, their rational, method, results, and interpretation.
Additionally, the var transcript differential expression analysis was removed from the manuscript, because this study was in a unique position to perform a more focused analysis of var transcriptional changes across paired samples, meaning the per-patient approach was more suitable. This allowed for changes in the var transcriptome to be identified that would have gone unnoticed in the traditional differential expression analysis.
We thank the reviewer for his highly important comment about adjusting for life cycle stage. Var gene expression is highly stage-dependent, so any quantitative comparison between samples does need adjustment for developmental stage. All life cycle stage adjustments were done using the mixture model proportions to be consistent with the original paper, described in the results and methods sections:
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Line 219–221: “Due to the potential confounding effect of differences in stage distribution on gene expression, we adjusted for developmental stage determined by the mixture model in all subsequent analyses.”
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Line 722–725: “Var gene expression is highly stage dependent, so any quantitative comparison between samples needs adjustment for developmental stage. The life cycle stage proportions determined from the mixture model approach were used for adjustment.“
The rank-expression analysis did not have adjustment for life cycle stage as the values were determined as a percentage contribution to the total var transcriptome. The var group level and the global var gene expression analyses were adjusted for life cycle stages, by including them as an independent variable, as described in the results and methods sections.
Var group expression:
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Line 321–326: “Due to these results, the expression of group A var genes vs. group B and C var genes was investigated using a paired analysis on all the DBLα (DBLα1 vs DBLα0 and DBLα2) and NTS (NTSA vs NTSB) sequences assembled from ex vivo samples and across multiple generations in culture. A linear model was created with group A expression as the response variable, the generation and life cycle stage as independent variables and the patient information included as a random effect. The same was performed using group B and C expression levels.“
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Line 784–787: “DESeq2 normalisation was performed, with patient identity and life cycle stage proportions included as covariates and differences in the amounts of var transcripts of group A compared with groups B and C assessed (Love et al., 2014). A similar approach was repeated for NTS domains.”
Gobal var gene expression:
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Line 342–347: “A linear model was created (using only paired samples from ex vivo and generation 1) (Supplementary file 1) with proportion of total gene expression dedicated to var gene expression as the response variable, the generation and life cycle stage as independent variables and the patient information included as a random effect. This model showed no significant differences between generations, suggesting that differences observed in the raw data may be a consequence of small changes in developmental stage distribution in culture.”
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Line 804–806: “Significant differences in total var gene expression were tested by constructing a linear model with the proportion of gene expression dedicated to var gene expression as the response variable, the generation and life cycle stage as an independent variables and the patient identity included as a random effect.“
The analysis of the conserved var gene expression was adjusted for life cycle stage:
- Line 766–768: “For each conserved gene, Salmon normalised read counts (adjusted for life cycle stage) were summed and expression compared across the generations using a pairwise Wilcoxon rank test.”
And life cycle stage estimates were included as covariates in the design matrix for the domain differential expression analysis:
- Line 771–773: “DESeq2 was used to test for differential domain expression, with five expected read counts in at least three patient isolates required, with life cycle stage and patient identity used as covariates.”
Reviewer #1:
- In the legend to Figure 1, the authors cite "Deitsch and Hviid, 2004" for the classification of different var gene types. This is not the best reference for this work. Better citations would be Kraemer and Smith, Mol Micro, 2003 and Lavstsen et al, Malaria J, 2003.
We agree and have updated the legend in Figure 1 with these references, consistent with the references cited in the introduction.
- In Figures 2 and 3, each of the boxes in the flow charts are largely filled with empty space while the text is nearly too small to read. Adjusting the size of the text would improve legibility.
We have increased the size of the text in these figures.
- My understanding of the computational method for assessing global var gene expression indicates an initial step of identifying reads containing the amino acid sequence LARSFADIG. It is worth noting that VAR2CSA does not contain this motif. Will the pipeline therefore miss expression of this gene, and if so, how does this affect the assessment of global var gene assessment? This seems relevant given that the authors detect increased expression of var2csa during adaptation to culture.
To address this question, we have added an explanation in the methods section to better explain our analysis. Var2csa was not captured in the global var gene expression analysis, but was analyzed separately because of its unique properties (conservation, proposed role in regulating var gene switching, slightly divergent timing of expression, translational repression).
- Line 802/3: “Var2csa does not contain the LARSFADIG motif, hence this quantitative analysis of global var gene expression excluded var2csa (which was analysed separately).”
- In Figures 4 and 7, panels a and b display virtually identical PCA plots, with the exception that panel A displays more generations. Why are both panels included? There doesn't appear to be any additional information provided by panel B.
We agree and have removed Figure 7b for the core transcriptome PCA as it did not provide any new information. The var transcript differential analysis (displayed in Figure 4) has been removed from the manuscript.
- On line 560-567, the authors state "However, the impact of short-term culture was the most apparent at the var transcript level and became less clear at higher levels." What are the high levels being referred to here?
We have replaced this sentence to make it clearer what the different levels are (global var gene expression, var domain and var type).
- Line 526/7: “However, the impact of short-term culture was the most apparent at the var transcript level and became less clear at the var domain, var type and global var gene expression level.”
Reviewer #2:
The authors make no mention or assessment of previously published var gene assembly methods from clinical samples that focus on genomic or transcriptomic approaches. These include:
https://pubmed.ncbi.nlm.nih.gov/28351419/
https://pubmed.ncbi.nlm.nih.gov/34846163/
These methods should be compared to the method for var gene assembly outlined by the co-authors, especially as the authors say that their method "overcomes previous limitations and outperforms current methods" (128-129). The second reference above appears to be a method to measure var expression in clinical samples and so should be particularly compared to the approach outlined by the authors.
Thank you for pointing this out. We have included the second reference in the introduction of our revised manuscript, where we refer to var assembly and quantification from RNA-sequencing data. We abstained from including the first paper in this paragraph (Dara et al., 2017) as it describes a var gene assembly pipeline and not a var transcript assembly pipeline.
- Line 101–105: “While approaches for var assembly and quantification based on RNA-sequencing have recently been proposed (Wichers et al., 2021; Stucke et al., 2021; Andrade et al., 2020; TonkinHill et al., 2018, Duffy et al., 2016), these still produce inadequate assembly of the biologically important N-terminal domain region, have a relatively high number of misassemblies and do not provide an adequate solution for handling the conserved var variants (Table S1).”
Additionally, we have updated the manuscript with a table (Table S1) comparing these two methods plus other previously used var transcript/gene assembly approaches (see comment to the public reviews).
But to address this particular comment in more detail, the first paper (Dara et al., 2017) is a var gene assembly pipeline and not a var transcript assembly pipeline. It is based on assembling var exon 1 from unfished whole genome assemblies of clinical samples and requires a prior step for filtering out human DNA. The authors used two different assemblers, Celera for short reads (which is no longer maintained) and Sprai for long reads (>2000bp), but found that Celera performed worse than Sprai, and subsequently used Sprai assemblies. Therefore, this method does not appear to be suitable for assembling short reads from RNA-seq.
The second paper (Stucke et al. 2021) focusses more on enriching for parasite RNA, which precedes assembly. The capture method they describe would complement downstream analysis of var transcript assembly with our pipeline. Their assembly pipeline is similar to our pipeline as they also performed de novo assembly on all P. falciparum mapping and non-human mapping reads and used the same assembler (but with different parameters). They clustered sequences using the same approach but at 90% sequence identity as opposed to 99% sequence identity using our approach. Then, Stucke et al. use 500nt as a cut-off as opposed to the more stringent filtering approach used in our approach. They annotated their de novo assembled transcripts with the known amino acid sequences used in their design of the capture array; our approach does not assume prior information on the var transcripts. Finally, their approach was validated only for its ability to recover the most highly expressed var transcript in 6 uncomplicated malaria samples, and they did not assess mis-assemblies in their approach.
For the methods (619–621), were erythrocytes isolated by Ficoll gradient centrifugation at the time of collection or later?
We have updated the methods section to clarify this.
- Line 586–588: “Blood was drawn and either immediately processed (#1, #2, #3, #4, #11, #12, #14, #17, #21, #23, #28, #29, #30, #31, #32) or stored overnight at 4oC until processing (#5, #6, #7, #9, #10, #13, #15, #16, #18, #19, #20, #22, #24, #25, #26, #27, #33).”
Was the current pipeline and assembly method assessed for var chimeras? This should be described.
Yes, this was quantified in the Pf 3D7 dataset and also assessed in the German traveler dataset. For the 3D7 dataset it is described in the result section and Figure S1.
- Line 168–174: “However, we found high accuracies (> 0.95) across all approaches, meaning the sequences we assembled were correct (Figure 2 – Figure supplement 1b). The whole transcript approach also performed the best when assembling the lower expressed var genes (Figure 2 – Figure supplement 1e) and produced the fewest var chimeras compared to the original approach on P. falciparum 3D7. Fourteen misassemblies were observed with the whole transcript approach compared to 19 with the original approach (Table S2). This reduction in misassemblies was particularly apparent in the ring-stage samples.” - Figure S1:
Author response image 1.
Performance of novel computational pipelines for var assembly on Plasmodium falciparum 3D7: The three approaches (whole transcript: blue, domain approach: orange, original approach: green) were applied to a public RNA-seq dataset (ENA: PRJEB31535) of the intra-erythrocytic life cycle stages of 3 biological replicates of cultured P. falciparum 3D7, sampled at 8-hour intervals up until 40hrs post infection (bpi) and then at 4-hour intervals up until 48 (Wichers al., 2019). Boxplots show the data from the 3 biological replicates for each time point in the intra-erythrocytic life cycle: a) alignment scores for the dominantly expressed var gene (PF3D7_07126m), b) accuracy scores for the dominantly var gene (PF3D7_0712600), c) number of contigs to assemble the dominant var gene (PF3D7_0712600), d) alignment scores for a middle ranking expressed vargene (PF3D7_0937800), e) alignment scores for the lowest expressed var gene (PF3D7_0200100). The first best blast hit (significance threshold = le-10) was chosen for each contig. The alignment score was used to evaluate the each method. The alignment score represents √accuracy* recovery. The accuracy is the proportion of bases that are correct in the assembled transcript and the recovery reflects what proportion of the true transcript was assembled. Assembly completeness of the dominant vargene (PF3D7 071200, length = 6648nt) for the three approaches was assessed for each biological f) biological replicate 1, g) biological replicate 2, h) biological replicate 3. Dotted lines represent the start and end of the contigs required to assemble the vargene. Red bars represent assembled sequences relative to the dominantly whole vargene sequence, where we know the true sequence (termed “reference transcript”).
For the ex vivo samples, this has been discussed in the result section and now we also added this information to Table 1.
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Line 182/3: “Remarkably, with the new whole transcript method, we observed a significant decrease (2 vs 336) in clearly misassembled transcripts with, for example, an N-terminal domain at an internal position.”
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Table 1:
Author response table 3.
Statistics for the different approaches used to assemble the var transcripts. Var assembly approaches were applied to malaria patient ex vivo samples (n=32) from (Wichers et al., 2021) and statistics determined. Given are the total number of assembled var transcripts longer than 500 nt containing at least one significantly annotated var domain, the maximum length of the longest assembled var transcript in nucleotides and the N50 value, respectively. The N50 is defined as the sequence length of the shortest var contig, with all var contigs greater than or equal to this length together accounting for 50% of the total length of concatenated var transcript assemblies. Misassemblies represents the number of misassemblies for each approach. **Number of misassemblies were not determined for the domain approach due to its poor performance in other metrics.
Line 432: "the core gene transcriptome underwent a greater change relative to the var transcriptome upon transition to culture." Can this be shown statistically? It's unclear whether the difference in the sizes of the respective pools of the core genome and the var genes may account for this observation.
We found 19% of the core transcriptome to be differentially expressed. The per patient var transcript analysis revealed individually highly variable but generally rather subtle changes in the var transcriptome. The different methods for assessing this make it difficult to statistically compare these two different results.
The feasibility of this approach for field samples should be discussed in the Discussion.
In the original manuscript we reflected on this already several times in the discussion (e.g., line 465/6; line 471–475; line 555–568). We now have added another two sentences at the end of the paragraph starting in line 449 to address this point. It reads now:
- Line 442–451: “Our new approach used the most geographically diverse reference of var gene sequences to date, which improved the identification of reads derived from var transcripts. This is crucial when analysing patient samples with low parasitaemia where var transcripts are hard to assemble due to their low abundancy (Guillochon et al., 2022). Our approach has wide utility due to stable performance on both laboratory-adapted and clinical samples. Concordance in the different var expression profiling approaches (RNA-sequencing and DBLα-tag) on ex vivo samples increased using the new approach by 13%, when compared to the original approach (96% in the whole transcript approach compared to 83% in Wichers et al., 2021. This suggests the new approach provides a more accurate method for characterising var genes, especially in samples collected directly from patients. Ultimately, this will allow a deeper understanding of relationships between var gene expression and clinical manifestations of malaria.”
MINOR
The plural form of PfEMP1 (PfEMP1s) is inconsistently used throughout the text.
Corrected.
404-405: statistical test for significance?
Thank you for this suggestion. We have done two comparisons between the original analysis from Wichers et al., 2021 and our new whole transcript approach to test concordance of the RNAseq approaches with the DBLα-tag approach using paired Wilcoxon tests. These comparisons suggest that our new approach has significantly increased concordance with DBLα-tag data and might be better at capturing all expressed DBLα domains than the original analysis (and the DBLα-approach), although not statistically significant. We describe this now in the result section.
- Line 352–361: “Overall, we found a high agreement between the detected DBLα-tag sequences and the de novo assembled var transcripts. A median of 96% (IQR: 93–100%) of all unique DBLα-tag sequences detected with >10 reads were found in the RNA-sequencing approach. This is a significant improvement on the original approach (p= 0.0077, paired Wilcoxon test), in which a median of 83% (IQR: 79–96%) was found (Wichers et al., 2021). To allow for a fair comparison of the >10 reads threshold used in the DBLα-tag approach, the upper 75th percentile of the RNA-sequencingassembled DBLα domains were analysed. A median of 77.4% (IQR: 61–88%) of the upper 75th percentile of the assembled DBLα domains were found in the DBLα-tag approach. This is a lower median percentage than the median of 81.3% (IQR: 73–98%) found in the original analysis (p= 0.28, paired Wilcoxon test) and suggests the new assembly approach is better at capturing all expressed DBLα domains.”
Figure 4: The letters for the figure panels need to be added.
The figure has been removed from the manuscript.
Reviewer #3:
It is difficult from Table S2 to determine how many unique var transcripts would have enough coverage to be potentially assembled from each sample. It seems unlikely that 455 distinct vars (~14 per sample) would be expressed at a detectable level for assembly. Why not DNA-sequence these samples to get the full repertoire for comparison to RNA? Why would so many distinct transcripts be yielded from fairly synchronous samples?
We know from controlled human malaria infections of malaria-naive volunteers, that most var genes present in the genomic repertoire of the parasite strain are expressed at the onset of the human blood phase (heterogenous var gene expression) (Wang et al., 2009; Bachmann et al, 2016; Wichers-Misterek et al., 2023). This pattern shifts to a more restricted, homogeneous var expression pattern in semi-immune individuals (expression of few variants) depending on the degree of immunity (Bachmann et al., 2019).
Author response image 2.
In this cohort, 15 first-time infections are included, which should also possess a more heterogenous var gene expression in comparison to the pre-exposed individuals, and indeed such a trend is already seen in the number of different DBLa-tag clusters found in both patient groups (see figure panel from Wichers et al. 2021: blue-first-time infections; grey–pre-exposed). Moreover, Warimwe et al. 2013 have shown that asymptomatic infections have a more homogeneous var expression in comparison to symptomatic infections. Therefore, we expect that parasites from symptomatic infections have a heterogenous var expression pattern with multiple var gene variants expressed, which we could assemble due to our high read depth and our improved var assembly pipeline for even low expressed variants.
Moreover, the distinct transcripts found in the RNA-seq approach were confirmed with the DBLα tag data. To our opinion, previous approaches may have underestimated the complexity of the var transcriptome in less immune individuals.
Mapping reads to these 455 putative transcripts and using this count matrix for differential expression analysis seems very unlikely to produce reliable results. As acknowledged on line 327, many reads will be mis-mapped, and perhaps most challenging is that most vars will not be represented in most samples. In other words, even if mapping were somehow perfect, one would expect a sparse matrix that would not be suitable for statistical comparisons between groups. This is likely why the per-patient transcript analysis doesn't appear to be consistent. I would recommend the authors remove the DE sections utilizing this approach, or add convincing evidence that the count matrix is useable.
We agree that this is a general issue of var differential expression analysis. Therefore, we have removed the var differential expression analysis from this manuscript as the per patient approach was more appropriate for the paired samples. We validated different mapping strategies (new Figure S6) and included a paragraph discussing the problem in the result section:
- Line 237–255: “In the original approach of Wichers et al., 2021, the non-core reads of each sample used for var assembly were mapped against a pooled reference of assembled var transcripts from all samples, as a preliminary step towards differential var transcript expression analysis. This approach returned a small number of var transcripts which were expressed across multiple patient samples (Figure 3 – Figure supplement 2a). As genome sequencing was not available, it was not possible to know whether there was truly overlap in var genomic repertoires of the different patient samples, but substantial overlap was not expected. Stricter mapping approaches (for example, excluding transcripts shorter than 1500nt) changed the resulting var expression profiles and produced more realistic scenarios where similar var expression profiles were generated across paired samples, whilst there was decreasing overlap across different patient samples (Figure 3 – Figure supplement 2b,c). Given this limitation, we used the paired samples to analyse var gene expression at an individual subject level, where we confirmed the MSP1 genotypes and alleles were still present after short-term in vitro cultivation. The per patient approach showed consistent expression of var transcripts within samples from each patient but no overlap of var expression profiles across different patients (Figure 3 – Figure supplement 2d). Taken together, the per patient approach was better suited for assessing var transcriptional changes in longitudinal samples. It has been hypothesised that more conserved var genes in field isolates increase parasite fitness during chronic infections, necessitating the need to correctly identify them (Dimonte et al., 2020, Otto et al., 2019). Accordingly, further work is needed to optimise the pooled sample approach to identify truly conserved var transcripts across different parasite isolates in cross-sectional studies.” - Figure S6:
Author response image 3.
Var expression profiles across different mapping. Different mapping approaches Were used to quantify the Var expression profiles of each sample (ex Vivo (n=13), generation I (n=13), generation 2 (n=10) and generation 3 (n=l). The pooled sample approach in Which all significantly assembled van transcripts (1500nt and containing3 significantly annotated var domains) across samples were combined into a reference and redundancy was removed using cd-hit (at sequence identity = 99%) (a—c). The non-core reads of each sample were mapped to this pooled reference using a) Salmon, b) bowtie2 filtering for uniquely mapping paired reads with MAPQ and c) bowtie2 filtering for uniquely mapping paired reads with a MAPQ > 20. d) The per patient approach was applied. For each patient, the paired ex vivo and in vitro samples were analysed. The assembled var transcripts (at least 1500nt and containing3 significantly annotated var domains) across all the generations for a patient were combined into a reference, redundancy was removed using cd-hit (at sequence identity: 99%), and expression was quantified using Salmon. Pie charts show the var expression profile With the relative size of each slice representing the relative percentage of total var gene expression of each var transcript. Different colours represent different assembled var transcripts with the same colour code used across a-d.
For future cross-sectional studies a per patient analysis that attempts to group per patient assemblies on some unifying structure (e.g., domain, homology blocks, domain cassettes etc) should be performed.
Line 304. I don't understand the rationale for comparing naïve vs. prior-exposed individuals at ex-vivo and gen 1 timepoints to provide insights into how reliable cultured parasites are as a surrogate for var expression in vivo. Further, the next section (per patient) appears to confirm the significant limitation of the 'all sample analysis' approach. The conclusion on line 319 is not supported by the results reported in figures S9a and S9b, nor is the bold conclusion in the abstract about "casting doubt" on experiments utilizing culture adapted
We have removed this comparison from the manuscript due to the inconsistencies with the var per patient approach. However, the conclusion in the abstract has been rephrased to reflect the fact we observed 19% of the core transcript differentially expressed within one cycle of cultivation.
Line 372/391 (and for the other LMM descriptions). I believe you mean to say response variable, rather than explanatory variable. Explanatory variables are on the right hand side of the equation.
Thank you for spotting this inaccuracy, we changed it to “response variable” (line 324, line 343, line 805).
Line 467. Similar to line 304, why would comparisons of naïve vs. prior-exposed be informative about surrogates for in vivo studies? Without a gold-standard for what should be differentially expressed between naïve and prior-exposed in vivo, it doesn't seem prudent to interpret a drop in the number of DE genes for this comparison in generation 1 as evidence that biological signal for this comparison is lost. What if the generation 1 result is actually more reflective of the true difference in vivo, but the ex vivo samples are just noisy? How do we know? Why not just compare ex vivo vs generation 1/2 directly (as done in the first DE analysis), and then you can comment on the large number of changes as samples are less and less proximal to in vivo?
In the original paper (Wichers et al., 2021), there were differences between the core transcriptome of naïve vs previously exposed patients. However, these differences appeared to diminish in vitro, suggesting the in vivo core transcriptome is not fully maintained in vitro.
We have added a sentence explaining the reasoning behind this analysis in the results section:
- Lines 414–423: “In the original analysis of ex vivo samples, hundreds of core genes were identified as significantly differentially expressed between pre-exposed and naïve malaria patients. We investigated whether these differences persisted after in vitro cultivation. We performed differential expression analysis comparing parasite isolates from naïve (n=6) vs pre-exposed (n=7) patients, first between their ex vivo samples, and then between the corresponding generation 1 samples. Interestingly, when using the ex vivo samples, we observed 206 core genes significantly upregulated in naïve patients compared to pre-exposed patients (Figure 7 – Figure supplement 3a). Conversely, we observed no differentially expressed genes in the naïve vs pre-exposed analysis of the paired generation 1 samples (Figure 7 – Figure supplement 3b). Taken together with the preceding findings, this suggests one cycle of cultivation shifts the core transcriptomes of parasites to be more alike each other, diminishing inferences about parasite biology in vivo.”
Overall, I found the many DE approaches very frustrating to interpret coherently. If not dropped in revision, the reader would benefit from a substantial effort to clarify the rationale for each approach, and how each result fits together with the other approaches and builds to a concise conclusion.
We agree that the manuscript contains many different complex layers of analysis and that it is therefore important to explain the rationale for each approach. Therefore, we now included the summary Table 3 (see comment to public review). Additionally, we have removed the var transcript differential expression due to its limitations, which we hope has already streamlined our manuscript.
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Author Response
The following is the authors’ response to the original reviews.
Reviewer #1 (Public Review):
"MAGIC" was introduced by the Rong Li lab in a Nature letters article in 2017. This manuscript is an extension of this original work and uses a genome wide screen the Baker's yeast to decipher which cellular pathways influence MAGIC. Overall, this manuscript is a logical extension of the 2017 study, however the manuscript is challenging to follow, complicated by the data often being discussed out of sequence. Although the manuscripts make claims of a mechanism being pinpointed, there are many gaps and the true mechanisms of how the factors identified in the screen influence MAGIC is not clear. A key issue is that there are many assumptions drawn on previous literature, but central aspects of the mechanisms being proposed are not adequately shown.
Key comments:
- Reasoning and pipelines presented in the first two sections of the results are disordered and do not follow figure order. In some instances, the background to experimental analyses such as detailing the generation of spGFP constructs in the YKO mutant library, or validation of Snf1 activation are mentioned after respective results are discussed. This needs to be fixed.
We thank the reviewer for pointing out potential confusion to readers. We have revised the first two sections according to reviewer’s suggestion. (Page 4-6)
- In general there is a lack of data to support microscopy data and supporting quantification analysis. The validity of this data could be significantly strengthened with accompanying western blots showing accumulation of a given constructs in mitochondrial sub compartments (as was the case in the lab’s original paper in 2017).
We appreciate the reviewer’s suggestion on biochemical validations. However, the validity of this imaging-based assay for detecting import of cytosolic misfolded proteins into mitochondria, including the use of FlucSM as a model misfolding-prone protein, was carefully established in our previous study by using appropriate controls, super resolution imaging, APEX-based proximity labeling, and classical biochemical fractionation and protease protection assay (Ruan et al., 2017 Nature, ref. 10). We have reminded readers of these validation experiments in the previous study on Page 4, line 14-17.
In recent years, advancements in imaging-based tools have allowed many protein interactions and dynamic processes, which were previously examined by using biochemical assays in lysates of populations of cells, to be observed with various level of quantitation in live cells with intact cellular compartments. Many of these assays, e.g., the RUSH assay for ER to Golgi transport, FRAP-based analysis for nuclear/cytoplasmic shuttling of proteins, or FRET-based assays for protein-protein interactions, have been well accepted and even embraced by the respective fields of study once validated with genetic and biochemical approaches. The advantages for live-cell imaging-based assays are often their unique ability to report dynamic processes or unstable molecular species with spatiotemporal sensitivity. Respectfully, it is our view, based on our own experience, that the traditional protease protection assay is not adequate or sufficiently quantitative for examining the presence of unstable misfolded proteins in mitochondrial sub-compartments, given the obligatorily lengthy in vitro cell lysis and mitochondrial isolation process, during which the unstable proteins are continuously being degraded. This likely explains our previous biochemical fractionation result that only weak protein signals were detected in the matrix fraction (Ruan et al., 2017 Nature, ref. 10). In addition, unlike stably folded, native mitochondrial matrix proteins, misfolded/unfolded proteins such as Lsg1 or FlucSM are highly susceptible to protease treatment. This sensitivity makes the assay unreliable for detecting such proteins if trace amount of the protease penetrates mitochondrial membranes during cell lysis even without detergent treatment.
While we agree that protease protection assay is highly valuable for qualitative detection of the presence of a protein in certain mitochondrial compartments or determining its topology on membranes, this assay (regrettably in our hands) does not allow quantitative comparisons that were necessary for this study, because of inherent sample to sample variation, yet the laborious and low throughput nature of this assay makes it difficult for adequate statistical analysis. Furthermore, the level of protein detection in various fractions is highly sensitive to how the sample is treated with protease and detergent. Our imaging-based quantification, on the other hand, allows us to compare increased or decreased presence of GFP11-tagged proteins in mitochondria under different metabolic conditions or in different mutant or wild-type strains. Data from hundreds of cells and at least three independent biological replicates allowed us to apply adequate statistical analysis to aid our conclusion.
- Much of the mechanisms proposed relies on the Snf1 activation. This is however not shown but assumed to be taking place. Given that this activation is central to the mechanism proposed, this should be explicitly shown here - for example survey the phosphorylation status of the protein.
Both REG1 deletion and low glucose conditions have been demonstrated extensively for Snf1 phosphorylation and activation in yeast (e.g., many seminal papers from Marian Carlson’s and other lab, such as ref. 24-28). In our study, we have indeed corroborated this by showing that Mig1 was exported from the nucleus in Δreg1 mutant and in low glucose conditions (Figure 1—figure supplement 2H and I. The mechanism of Snf1-mediated nuclear export of Mig1 has been characterized in detail as well (e.g., ref. 29-31).
Recommendations for the authors: please note that you control which, if any, revisions, to undertake
Reviewer #1 (Recommendations For The Authors):
SPECIFIC COMMENTS
Genetic Screen o Line 20 - the narrative moves to SNF1, but the reasoning for the selection of this Class I substrate is not defined. What was the basis for this selection - what happened to the other Class I substrates. It is stated in the text that the other Class I proteins show the same increase in spGFP signal. The data showing this should be included in the Supp Figure 1 for transparency.
We have moved the narratives of Snf1 function to the second section and clarified that we were interested in this gene due to its central role in metabolism and mitochondrial functions that may influence MAGIC (Page 5: line 16-20). Other genes in class 1 were shown in Table S1. Detailed discussion of other genes in this category is beyond the scope of this study.
Snf1/AMPK prevents MP accumulation in mitochondria:
The FlucDM data in human RPE-1 mitochondria seems to be added to only increase the significance of the work. The mechanisms suggested here with Hap4 would not be possible in human cells as there is no homologue of this protein in human cells. Making generalisations that these pathways are conserved based on this one experiment is not appropriate.
We appreciate this feedback. Although the focus of this study is the regulation of MAGIC by the yeast AMPK Snf1, we would like to share our initial observation that suggests a similar role of AMPK in human RPE-1 cells. We acknowledge that the underlying mechanisms regarding the downstream transcription factors and pathway for misfolded protein import could be different in mammalian cells, but the overall effect of AMPK in mitochondrial biogenesis is well known to resemble that of Snf1. To avoid making over-generalization, we changed our statement of conclusion to: ‘These results suggest that AMPK in human cells regulates MP accumulation in mitochondria following a similar trend as in yeast, although the underlying mechanisms might differ between these organisms.’ (Page 7: line 2-4)
Mechanisms of MAGIC regulation by Snf1:
While the lysosome is ruled out here the authors have not considered the proteasomes. Is there a reason for this? Given accumulation of aggregates outside of mitochondria, and previous connections of the proteasome to mitochondrial quality control this would be an obvious thing to check. We examined the role of lysosomal degradation here because it is known to be activated under Snf1active condition (ref. 37). We appreciate this feedback and have included a new analysis on MG132treated FlucSM spGFP strains in which PDR5 gene was deleted to avoid drug efflux.
This result suggests that the proteosome inhibitor did not ablate the difference in FlucSM accumulation between these conditions. That MG132 promoted mitochondrial accumulation of FlucSM in both high glucose and low glucose conditions was not surprising, as FlucSM is also degraded by proteasome in the cytosol (Ruan et al., 2017 Nature, ref. 10), and preventing this pathway could divert more of such protein molecules toward MAGIC. (Page 7: line 26-29).
Line 13 "we hypothesized that elevated expression of mitochondrial preproteins induced by the activation of Snf1-Hap4 axis (REF) may outcompete MPs for import channels". This statement has some assumptions. The authors have not shown that Snf1 is activated in thier models and more importantly that they have an accumulation of mitochondrial preproteins. The data that follows using the cytosolic domains of the receptors is hard to rationalise without seeing evidence that there is in fact pre-protein accumulation or impacts on the mitochondrial proteome in this system.
As stated in our response to main point [3], Snf1 activation in reg1 mutant or in low glucose is evidenced by our data showing Mig1 export from nucleus to cytoplasm and had also been shown in many previous publications. A recent study (Tsuboi et al., 2020 eLife) also showed a dramatic increase in mitochondrial volume fraction in Δreg1 cells and wild-type cells in respiratory conditions, further supporting the role of Snf1 in mitochondrial biogenesis. We have provided relevant references in the manuscript (ref. 24-28).
The ability of Tom70 cytosolic domain (Tom70cd), which can bind mitochondrial preproteins but not localize to mitochondria due to lack of N-terminal targeting sequence, to compete with endogenous Tom70 for mitochondrial preproteins has been well documented (ref. 47-49). However, we agree with the reviewer that a future quantitative proteomics study to measure changes in mitochondrial proteome under Tom70cd over-expression could allow more accurate interpretation of our experimental result.
AMPK protects cellular fitness during proteotoxic stress:
The inhibition of preprotein import by overexpressing the cytosolic domains of receptors is not supported with some proof of principle data. If this was working as the authors assume, it is not clear why only an effect with Tom70 is observed. The majority of the mitochondrial proteome is imported via Tom20/Tom22 so this does not align with what the authors are suggesting. Is the Tom70CD and any associated Hsp proteins facilitating the observed changes to the MPs?
We thank the reviewer for raising this point. We expressed different TOM receptor cytosolic domains but found that Tom70cd had the strongest rescue on MAGIC under AMPK activation conditions. It is possible that certain Tom70 substrates or Tom70-assoicated heat shock proteins inhibit the import of MAGIC substrates. We admit that a clear explanation of this unexpected observation necessitates a better understanding of how native and MAGIC substrates are selected and imported by the outer-membrane channel. We can only offer our best interpretation based on the current state of the understanding, and we feel that we have been careful to acknowledge such in the manuscript.
While the effect of AMPK inactivation reducing FUS accumulation was striking, this was all in the context of overexpression and may not be physiologically relevant - or may occur very transiently under basal conditions. Is GST an appropriate control here, why not use WT FUS? Likewise, one representative image is shown in Figure 5 - can the authors show western blotting that mitochondrial accumulation of FUS can be reduced with AMPK activation?
We thank the reviewer for this suggestion, however, overexpressed FUS WT is also aggregation prone (Zhihui Sun et al., 2011, PloS Biology; Shulin Ju, 2011, PloS Biology; Jacqueline C. Mitchell et., 2013, Acta Neuro). We believe that GST, as a well-folded protein, is an appropriate control (Ruan et al., 2017 Nature, ref. 10). As we discussed in response to main point [1], the in vitro assay involving protease protection and western blots do not allow reliable quantitative comparison in our hands.
In text changes.
The analysis pipeline of the YKO mutant library should be introduced at the very start of the first paragraph, not the end.
Addressed on Page 4, second paragraph
"Fluc" should be introduced as "Firefly luciferase" within the first paragraph of the first section, also need to define SM and DM in FlucSM/FlucDM - these appear to be missing.
Addressed in both Introduction (Page 2: line 29; Page 3: line 8-9) and re-clarified in Result (Page 5: line 27-29)
The role of Reg1 should be explicitly stated in the text, not just in the figure.
Addressed on Page 6: line 3-6
Figure 1H legend states Reg1 (WT) is Snf1-inactive and Reg1 KO is Snf1-active. This wording is confusing and is not supported by data, but by assumption. If the authors want to use this wording then evidence needs to be provided - as suggested above.
We have changed this and other legends to only show genotypes and medium conditions.
"Tom70cd overexpression also exacerbated growth rate reduction due to FlucSM expression in HG medium (Figure 4A; Figure 4 - figure supplement 1A)" should be figure supplement 1B.
Fixed on Page 10: line 10
"These results suggest that glucose limitation protects mitochondria and cellular fitness during FlucSM induced proteotoxic stress through Snf1-dependent inhibition of MP import into mitochondria". The phrase "Snf1-dependent inhibition of MP import into mitochondria" may be misleading, as Snf1 isn't modulating import directly but is acting on transcriptional regulators to modulate mitochondrial import under stress.
We restated the conclusion as follows: ‘These results suggest that Snf1 activation under glucose limitation protects mitochondrial and cellular fitness under FlucSM-associated proteotoxic stress.’ (Page 10: line 20- 21)
"... Significantly increased the fraction of spGFP-positive and MMP-low cells in both HG and LG medium (Figure 4G-K)" should be (Figure 4J-K).
Fixed on Page 11: line 3
Reviewer #2 (Public Review):
Work of Rong Li´s lab, published in Nature 2017 (Ruan et al, 2017), led the authors to suggest that the mitochondrial protein import machinery removes misfolded/aggregated proteins from the cytosol and transports them to the mitochondrial matrix, where they are degraded by Pim1, the yeast Lon protease. The process was named mitochondria as guardian in cytosol (MAGIC).
The mechanism by which MAGIC selects proteins lacking mitochondrial targeting information, and the mechanism which allows misfolded proteins to cross the mitochondrial membranes remained, however, enigmatic. Up to my knowledge, additional support of MAGIC has not been published. Due to that, MAGIC is briefly mentioned in relevant reviews (it is a very interesting possibility!), however, the process is mentioned as a "proposal" (Andreasson et al, 2019) or is referred to require "further investigation to define its relevance for cellular protein homeostasis (proteostasis)" (Pfanner et al, 2019).
Rong Li´s lab now presents a follow-up story. As in the original Nature paper, the major findings are based on in vivo localization studies in yeast. The authors employ an aggregation prone, artificial luciferase construct (FlucSM), in a classical split-GFP assay: GFP1-10 is targeted to the matrix of mitochondria by fusion with the mitochondrial protein Grx5, while GFP11 is fused to FlucSM, lacking mitochondrial targeting information. In addition the authors perform a genetic screen, based on a similar assay, however, using the cytosolic misfolding-prone protein Lsg1 as a read-out.
My major concern about the manuscript is that it does not provide additional information which helps to understand how specifically aggregated cytosolic proteins, lacking a mitochondrial targeting signal could be imported into mitochondria. As it stands, I am not convinced that the observed FlucSM-/Lsg1-GFP signals presented in this study originate from FlucSM-/Lsg1-GFP localized inside of the mitochondrial matrix. The conclusions drawn by the authors in the current manuscript, however, rely on this single approach.
In the 2017 paper the authors state: "... we speculate that protein aggregates engaged with mitochondria via interaction with import receptors such as Tom70, leading to import of aggregate proteins followed by degradation by mitochondrial proteases such as Pim1." Based on the new data shown in this manuscript the authors now conclude "that MP (misfolded protein) import does not use Tom70/Tom71 as obligatory receptors." The new data presented do not provide a conclusive alternative. More experiments are required to draw a conclusion.
In my view: to confirm that MAGIC does indeed result in import of aggregated cytosolic proteins into the mitochondrial matrix, a second, independent approach is needed. My suggestion is to isolate mitochondria from a strain expressing FlucSM-GFP and perform protease protection assays, which are well established to demonstrate matrix localization of mitochondrial proteins. In case the authors are not equipped to do these experiments I feel that a collaboration with one of the excellent mitochondrial labs in the US might help the MAGIC pathway to become established.
We thank Reviewer 2 for these suggestions, but we would like to respectfully offer our difference in opinion:
a. Regarding the suggestion “to isolate mitochondria from a strain expressing FlucSM-GFP and perform protease protection assays”, in our previous study (Ruan et al., 2017 Nature, ref. 10), we have indeed applied two independent biochemical approaches: APEX-mitochondrial matrix proximity labeling and classic protease protection assay using non-spGFP strains, both consistently confirmed the entry of misfolded proteins into mitochondria under proteotoxic stress. Our super-resolution imaging further confirmed the import of the split GFP-labeled proteins to be inside mitochondria. Moreover, as we discussed in response to Reviewer 1’s main point [2], while the suggested biochemical assay is useful for validating topology within mitochondria, it is not quantitative and may not reliably report the in vivo accumulation of misfolded proteins in mitochondria due to the isolation process that takes hours, during which the unstable proteins could be continuously degraded within mitochondria.
While we agree with the reviewer that we do not yet understand how misfolded proteins are imported into mitochondria, it would be unfair to state “as it stands, I am not convinced..” simply because the underlying mechanism remains to be elucidated. We would like to point out that targeting sequences for many well-established mitochondrial proteins are still not well defined. It is well known that mitochondrial targeting sequences are not as uniformly predictable as, for example, nuclear targeting sequences. Our finding that deletion of TOM6 enhances the import of misfolded proteins suggest that their import may involve the TOM channel in a more promiscuous conformation, which may reduce the requirement for a specific sequence-based targeting signal associated with the substrate.
b. Regarding the role of Tom70, in our 2017 study, using proteomics and subsequently immunoprecipitation we validated the binding, albeit not necessarily direct, between misfolded protein FlucSM and Tom70. Therefore, “we speculate that protein aggregates engaged with mitochondria via interaction with import receptors such as Tom70”. Recent studies from different labs confirmed the interactions between Tom70 and aggregation prone proteins (Backes et al., 2021, Cell Reports; Liu et al., 2023, PNAS). In the current study, surprisingly, knockout of TOM70 did not block MAGIC, suggesting redundant components of mitochondria import system may facilitate the recruitment of misfolded proteins in the absence of Tom70, and this does not contradict the notion that Tom70 helps tether protein aggregates to mitochondria.
c. Regarding other studies also showing the import of misfolding or aggregation-prone cytosolic proteins into mitochondria, there have been at least several recent studies in the literature for mammalian cells involving either model substrates or disease proteins (e.g., ref. 12-15; 56-58; Vicario, M. et al. 2019 Cell Death Dis.). The studies are briefly mentioned in Introduction (Page 3, paragraph 2). The present manuscript documents a major effort from our group using whole genome screen in yeast to understand the mechanism and regulation of MAGIC. Many of the screen hits have yet to be studied in detail. We full agree that much remains to be understood about whether and how this pathway affects proteostasis and what might be the evolutionary origin for such a mechanism.
Additional comments:
The genetic screen:
The genetic screen identified five class 1 deletion strains, which lead to enhanced accumulation of Lsg1GFP and a larger set of class 2 mutants, which lead to reduced accumulation. Please note, in my opinion it is not clear that accumulation of the reporters occurs inside the mitochondria. In any case, the authors selected one single protein for further analysis: Snf1, the catalytic subunit of the yeast SNF complex, which is required for respiratory growth of yeast.
The results of the screen are not discussed in any detail. The authors mention that ribosome biogenesis factors are abundant among class 2 mutants. Noteworthy, Lsg1 is involved in 60S ribosomal subunit biogenesis. As Lsg1-GFP11 is overexpressed in the screen this should be discussed. Class 2 mutants also .include several 40S ribosomal subunit proteins (only one of the 60S subunit). What does this imply for the MAGIC model? Also, it should be discussed that the screen did not identify reg1 and hap4, which I had expected as hits based on the data shown in later parts of the manuscript.
We apologize for the confusion, but the GFP11 tag was in fact knocked into the C-terminus of Lsg1 in the endogenous LSG1 locus, and so Lsg1 was not overexpressed in the screen. We have made sure that this information is clearly conveyed in the revised manuscript (Page 4: line 20-22). How the ribosome small subunit affects MAGIC is beyond the focus of the current study and will be pursued in the future.
Regarding why certain mutants did not come out of our initial screen, this is not unexpected as the YKO collection, although extremely valuable to the community, is known to be potentially affected by false knockouts, suppressor accumulation and cross contamination (for references, e.g., Puddu et al., 2019 Nature). Additionally, high-through screens can also miss real hits. In our experience using this collection in several studies, we often found additional hits from analysis of genes implicated by known genetic or biochemical interactions.
Mutant yeast strains and growth assays:
The Δreg1 strain grows poorly in all growth conditions and frequently accumulates extragenic suppressor mutations (Barrett et al, 2012). It would be good to make sure that this is not the case in the strains employed in this study. My suggestion is to do (and show) standard yeast plating assays with the relevant mutant strains including Δreg1, snf1, hap4, Δreg1Δhap4 without the split GFP constructs and also with them (i.e. the strains that were used in the assays).
We thank the reviewer for the suggestion. We were indeed aware of potential accumulation of suppressor mutations from the YKO library. Therefore, deletion mutants like Δreg1 and loss of TFs downstream of Snf1 that we used in the study after the initial screen were all freshly made and validated. At least 3 independent colonies were analyzed for each mutant (mentioned in Methods & Materials; Page 33, line 57). Moreover, the plating assay suggested here may not reveal additional information other than growth, which was taken into consideration during our experiments.
Activation of Snf1 in the relevant strains should be tested with the commercially available antibody recognizing active Snf1, which is phosphorylated at Snf1-T210.
Snf1 activation was validated by the Mig1 exporting from the nucleus. We also noted above that many studies have clearly demonstrated Snf1 activation in reg1 mutant and under low glucose growth (e.g., ref. 24-28).
Effects of Snf1, Reg1, Hap4 and respiratory growth conditions:
The authors show that split GFP reporters show enhanced accumulation during fermentative growth, in Δsnf1, and Δreg1Δhap4 and fail to accumulate during respiratory growth, in Δreg1 and upon overexpression of HAP4. Analysis of Δhap4 should be included in Fig. 2. The suggestion that upon activation of Snf1 enhanced Hap4-dependent expression "outcompetes" misfolded protein import seems unlikely as only a fraction of mitochondrial genes is under control of Hap4. Without further experimental evidence I do not find that a valid assumption. More likely, the membrane potential plays a role: it is low during fermentative growth, in Δsnf1 and Δreg1Δhap4, and high during respiratory growth and in Δreg1 (Hübscher et al, 2016). Such an effect of the membrane potential seems to contradict the findings in the 2017 paper and the issue should be clarified and discussed. In any case, these data do not reveal that GFP reporters accumulate inside of the mitochondria. Based on the currently available evidence they may accumulate in close proximity/attached to the mitochondria. This has to be tested directly (see above).
We have included our analysis of Δhap4 in Page 8: line 14-15 and Figure 2—figure supplement 1H. Consistent with our result for Δreg1Δhap4 in glucose-rich medium, HAP4 deletion also resulted in a significant increase in mitochondrial accumulation of FlucSM in low glucose medium compared to WT. It did not have effect in high glucose condition in which Snf1 is largely inactive.
It is our view that the importance of Hap4 should not be judged by the number of nuclear encoded mitochondrial proteins they regulate. Still, this sub-group comprises a considerable number of proteins (at least 55 genes upregulated by Hap4 overexpression, ref. 43), and certain substrates may be more competitive with misfolded cytosolic proteins for import. Our genetic data strongly suggest that the inhibitory effect of active Snf1 on MAGIC is through Hap4, although we agree with the reviewer that detailed mechanism on how Hap4 substrates may compete with misfolded proteins need to be addressed in future studies.
Membrane potential is important for mitochondrial import. During respiratory growth and in Δreg1, membrane potential is well known to be elevated comparing to fermentative condition (e.g., Figure 4C). Our observation that the import of misfolded proteins into mitochondria is reduced under these conditions simply suggests that this reduction is not due to a lack of membrane potential. This is not in any way contradictory to our 2017 finding that misfolded protein import requires membrane potential (ref. 10).
Again, the accumulation of misfolded proteins in mitochondria, especially the model protein FlucSM, has been validated by using super resolution imaging (Figure 1—figure supplement 1A) in addition to the protease protection assay in our 2017 study.
Introduction and Discussion:
Both are really short, too short in my view. Please provide some background of the general principals of mitochondrial protein import and information of how exactly translocation of cytosolic, aggregated proteins (lacking targeting information) is supposed to work. I do not understand exactly how the authors actually envisage the process.
We thank the reviewer for the suggestion. In the revised manuscript, we have extended both Introduction (Page 2-3) and Discussion section (Page 11-13)
The results from the 2022 eLife paper (Liu et al, 2022), which suggests that Tom70 may "regulate both the transcription/biogenesis and import of mitochondrial proteins so the nascent mitochondrial proteins do not compromise cytosolic proteostasis or cause cytosolic protein aggregation" should be discussed with regard to the data obtained with overexpression of the Tom70 soluble domain.
We thank the reviewer for pointing out that study and we have included a brief comment in Discussion section (Page 12: line 13-16). As the function of Tom70 appears to be complex, we cannot exclude the possibility that overexpression of the cytosolic domain has additional or indirect effects in addition to that due to preprotein binding.
Andreasson, C., Ott, M., and Buttner, S. (2019). Mitochondria orchestrate proteostatic and metabolic stress responses. EMBO Rep 20, e47865.
Barrett, L., Orlova, M., Maziarz, M., and Kuchin, S. (2012). Protein kinase A contributes to the negative control of Snf1 protein kinase in Saccharomyces cerevisiae. Eukaryot Cell 11, 119-128.
Hubscher, V., Mudholkar, K., Chiabudini, M., Fitzke, E., Wolfle, T., Pfeifer, D., Drepper, F., Warscheid, B., and Rospert, S. (2016). The Hsp70 homolog Ssb and the 14-3-3 protein Bmh1 jointly regulate transcription of glucose repressed genes in Saccharomyces cerevisiae. Nucleic Acids Res. 44, 5629-5645.
Liu, Q., Chang, C.E., Wooldredge, A.C., Fong, B., Kennedy, B.K., and Zhou, C. (2022). Tom70-based transcriptional regulation of mitochondrial biogenesis and aging. Elife 11
Pfanner, N., Warscheid, B., and Wiedemann, N. (2019). Mitochondrial proteins: from biogenesis to functional networks. Nat Rev Mol Cell Biol 20, 267-284.
Ruan, L., Zhou, C., Jin, E., Kucharavy, A., Zhang, Y., Wen, Z., Florens, L., and Li, R. (2017). Cytosolic proteostasis through importing of misfolded proteins into mitochondria. Nature 543, 443-446.
I prefer to have "all in one", also due to time limitation.
It would be great to be able to upload the review file as otherwise formatting and symbols get lost.
Reviewer #3 (Public Review):
In this study, Wang et al extend on their previous finding of a novel quality control pathway, the MAGIC pathway. This pathway allows misfolded cytosolic proteins to become imported into mitochondria and there they are degraded by the LON protease. Using a screen, they identify Snf1 as a player that regulates MAGIC. Snf1 inhibits mitochondrial protein import via the transcription factor Hap4 via an unknown pathway. This allows cells to adapt to metabolic changes, upon high glucose levels, misfolded proteins an become imported and degraded, while during low glucose growth conditions, import of these proteins is prevented, and instead import of mitochondrial proteins is preferred.
This is a nice and well-structured manuscript reporting on important findings about a regulatory mechanism of a quality control pathway. The findings are obtained by a combination of mostly fluorescent protein-based assays. Findings from these assays support the claims well.
While this study convincingly describes the mechanisms of a mitochondria-associated import pathway using mainly model substrates, my major concern is that the physiological relevance of this pathway remains unclear: what are endogenous substrates of the pathway, to which extend are they imported and degraded, i.e. how much does MAGIC contribute to overall misfolded protein removal (none of the experiments reports quantitative "flux" information). Lastly, it remains unclear by which mechanism Snf1 impacts on MAGIC or whether it is "only" about being outcompeted by mitochondrial precursors.
We thank Reviewer 3 for the positive and encouraging comments on our manuscript. We agree with the reviewer that identifying MAGIC endogenous substrates and understanding what percentage of them are degraded in mitochondria are very important issues to be addressed. We are indeed carrying out projects to address these questions. We also agree with Reviewer 3 that the effect of Snf1 on MAGIC may have additional mechanisms in addition to precursors competition, such as Tom6 mediated conformational changes of TOM pores. In the revised manuscript, we had added a discussion to address these comments (Page 12: line 21-28).
Reviewer #3 (Recommendations For The Authors):
- In their screen, the authors utilize differences in GFP intensity as a measure for import efficiency. However, reconstitution of the GFP from GFP1-10 and GFP11 in the matrix might also be affected (folding factors, differential degradation).
Upon Snf1 activation, the protein abundance of mitochondrial chaperones such as Hsp10, Hsp60, and Mdj1, and mitochondrial proteases such as Pim1 are not significantly changed (ref. 35). Therefore, it is unlikely that the folding and degradation capacity of mitochondrial matrix is drastically affected by Snf1 activation.
To examine the effect of Snf1 activation on spGFP reconstitution, Grx5 spGFP strain was constructed in which the endogenous mitochondrial matrix protein Grx5 was C-terminally tagged with GFP11 at its genomic locus, and GFP1-10 was targeted to mitochondria through cleavable Su9 MTS (MTS-mCherryGFP1-10) (ref. 10). Only modest reduction in Grx5 spGFP intensity was observed in LG compared to HG, and no significant difference after adjusting the GFP1-10 abundance (spGFP/mCherry ratio) (Figure 1— figure supplement 3A-D). These data suggest that any effect on spGFP reconstitution is insufficient to explain the drastic reduction of MP accumulation in mitochondria under Snf1 activation. Overall, our results demonstrate that Snf1 activation primarily prevents mitochondrial accumulation of MPs, but not that of normal mitochondrial proteins. (Page 6: line 17-25).
We admit, however, that to fully rule out these factors, specific intra-mitochondrial folding or degradation reporter assays would be needed.
- Scoring of protein import always takes place using fluorescence-based assays. These always require folding of the "sensors" in the matrix. An additional convincing approach that would not rely on matrix folding could be pulse chase approaches coupled to fractionation assays and immunoprecipitation.
We thank reviewer 3 for this suggestion. In our previous study, we applied two different biochemical assays: APEX proximity labeling, and mitochondrial fractionation followed by protease protection. Both confirmed the entry of misfolded proteins into mitochondria as observed by using split GFP. As we discussed in response to Reviewer 1’s main point [3], the fractionation assays are not quantitative enough for the comparisons made in our study. In particular, during the over 2-hour assay, misfolded proteins continue to be degraded within mitochondria. By using proper controls, our spGFP system provides quantitative comparisons for mitochondrial accumulation of misfolded proteins in non-disturbed physiological conditions.
- Could the pathway be reconstituted in vitro with isolated mitochondria to test for the "competition hypothesis"
This is an excellent suggestion, but setting up such a reconstituted system is a project on its own. The study documented in this manuscript already encompasses a large amount of work that we feel should be published timely.
- Fluorescence figures are not colour blind friendly (red-green). This should be improved by changing the color scheme.
We thank reviewer 3 for pointing this out and sincerely apologize for any inconvenience. However, we are unfortunately unable to change all images within a limited time. We will adopt another color scheme in future work.
- spGFP in human cells appears to form "spot-like" structures. What are these granules?
We indeed observed granule-like structures by spGFP labeled FUS in mitochondria, which is interesting, but we did not investigate this further because it is a not a focus of this study.
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Note: This rebuttal was posted by the corresponding author to Review Commons. Content has not been altered except for formatting.
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Reply to the reviewers
Please find our point-to-point response to the reviewer’s comments below, where we marked all changes implemented in the manuscript in italics.
Reviewer #1 (Evidence, reproducibility and clarity (Required)):
With the emergence and spread of resistance to Artemisinin (ART), a key component of current frontline malaria combination therapies, there is a growing effort to understand the mechanisms that lead to ART resistance. Previous work has shown that ART resistant parasites harbour mutations in the Kelch13 protein, which in turn leads to reduced endocytosis of host haemoglobin. The digestion of haemoglobin is thought to be critical for the activation of the artemisinin endoperoxide bridge, leading to the production of free radicals and parasite death. However, the mechanisms by which the parasites endocytose host cell haemoglobin remain poorly understood.
Previous work by the authors identified several proteins in the proximity of K13 using proximity-based labelling (BioID) (Birnbaum et al. 2020). The authors then went on to characterise several of these proteins, showing that when proteins including EPS15, AP2mu, UBP1 and KIC7 are disrupted, this leads to ART resistance and defects in endocytosis leading to the hypothesis that these two processes are inextricably linked.
In this manuscript, Schmidt et al. set themselves the task of characterising more K13 component candidates identified in their previous work (Birnbaum et al. 2020) that were not previously validated or characterised. They chose 10 candidates and investigated their localisations, and colocalisation with K13, and their involvement in endocytosis and in vitro ART resistance, 2 processes mediated by K13 and some members of the K13 compartments
The authors show that of their 10 candidates, only 4 can be co-localised with K13. Then, using a combination of targeted gene disruption (TGD) as well as knock sideways (KS), they characterised these 4 proteins found in the K13 compartment. They show that MyoF and KIC12 are involved in endocytosis and are important for parasite growth, however their disruption does not lead to a change in ART sensitivity. The authors also confirm the findings of their previous publication (Birnbaum et al. 2020), using a slightly different TGD
(note from the authors: we apologise if this has not properly transpired from the manuscript but the difference between the TGDs is substantial and relevant: one has less than 3% of the protein left and hence can be considered to fully inactivate MCA2 and has a growth defect whereas the other contains about two thirds of the protein (1344 amino acids/~66% are left), has no growth defect, although it lacks the MCA2 domain (hence that domain can not be critical for the growth defect)),
that MCA2 is involved in ART resistance, however they did not check whether its disruption impacts haemoglobin uptake. They also show that KIC11 is not involved in mediating haemoglobin uptake or ART resistance. To finish, the authors used AlphaFold to identify new domains in the proteins of the K13 compartment. This led them to the conclusion that vesicle trafficking domains are enriched in proteins of the K13 compartment involved in endocytosis and in vitro ART resistance.
The majority of the experiments conducted by the authors are performed to a good standard in biological and technical replicates, with the correct controls. Their findings provide confirmation that their 4 candidate genes seem to be important for parasite growth, and show that some of their candidates are involved in endocytosis. While the KD and KS approaches employed by the authors to study their candidate genes each have their own advantages and can be excellent tools for studying a large sets or genes, this manuscript highlights the many limitations of these approaches. For example, the large tag used for the KS approach can mislocalise proteins or disrupt their function (as is the case for MyoF), resulting in spurious results, or indeed the inability to generate the tagged line (as is the case for MCA2). The KS approach also makes the results of a protein with a dual localisation, like KIC12, extremely difficult to interpret.
We thank the reviewer for this thorough and insightful review.
The limitations mentioned above were addressed in the response to the main points and a general detailed response in regards to the systems used for this research are added at the end of this rebuttal. Briefly summarised here: while we agree that there are limitations of the system used, we are convinced that
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the advantages of using a large tag in most cases outweighs the drawbacks as it permits to track the inactivation of the target, if need be on the individual cell level
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while not optimal for MyoF, the partial inactivation actually helps in its functional study as detailed in major point 23&28 or reviewer#3 major point 11: it shows a consistent correlation of the phenotype with different causes and degrees of inactivation (this is now better illustrated in Figure 1L1M). Further, regarding the concern of the large tag: the effect of the tag based on localisation was overestimated in the review by what seems to have been a mix up comparing numbers from MyoF with a number from MCA2 (there is a difference, but it is only small) (see reviewer#1 major point #23).
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KS is the optimal method for most of the assays in this work (e.g. bloated food vacuole assays and RSAs); these assays would be impossible or difficult to use with other inactivation systems currently used in P. falciparum research (see details in the response to the specific points and after the rebuttal)
In regards to the difficulty to interpret KIC12 data: this is only true for measuring absolute essentiality, everything else we believe we actually have the optimal method. If not KS, which method targets a specific pool of a protein with a dual localisastion? Again, our assays targeting the K13 pool and revealing the specific function would have been difficult or impossible with any other system.
Ultimately the question is whether any other system would have resulted in a different conclusion on the function of the proteins studied. At present we are confident this would not be the case and other systems probably would not have delivered the specific functional data shown in this work. Clearly, more in depth work will provide more nuanced and detailed insights into the proteins analysed in this work and this likely will also include the use of other systems for specific aspects they are most suitable for. However, this (e.g. different complementations in a diCre cKO) is complex and therefore beyond what fits into this work which had the goal to assess which proteins are true positives for the K13 compartment and to place them into functional groups in regards to endocytosis.
Moreover, the manuscript is disjointed at times, with the authors choosing to conduct certain experiments for only a subset of genes, but not for others. For example, considering that the aim of this paper was to identify more proteins involved in ART resistance and endocytosis, it is confusing why the authors do not perform the endocytosis assays for all their selected proteins, and why they do not do this for the proteins they identify in their domain search. There is significant room for improvement for this manuscript, and a generally interesting question.
The reviewer remarks that not every experiment was done for every target. Based on the rebuttal we tried to amend this but also note that there was some sentiment by the reviewers to better stick to the point and not make the manuscript more disjointed. We attempted to balance that as much as possible and hope we were able to honour both aspects (amendments were done as detailed in the point by point response below).
In regards to endocytosis and choice of targets: We did do endocytosis assays for all proteins that showed a growth phenotype upon inactivation in this work. We therefore assume the reviewer here refers to major point #40 asking for endocytosis assays with KIC4 and KIC5 (which were not studied in this manuscript) as well as MCA2 (point 17). We fully agree with the reviewer that this would fill a gap in the work on K13 compartment proteins but such assays are difficult with TGDs (there are issues with non-comparable samples and compensatory effects) and proteins that are not essential (and hence likely have a smaller impact on endocytosis when truncated). We nevertheless now carried them out, but due to the limitations to do this with these lines would be hesitant to draw definite conclusions (see major point 17 and 40 for details and outcomes).
But in it's current format, other than confirming that MCA2 is involved in ART resistance (which was already known from the Birnbaum paper), the authors do not further expand our understanding of the link between ART resistance and endocytosis in this manuscript.
We would like to point out that the importance of the K13 compartment and endocytosis goes beyond ART resistance (see e.g. also newly published papers on the K13 compartment in Toxoplasma, (Wan et al., 2023; Koreny et al., 2023)). Endocytosis is an essential and prominent process in blood stages. However, in contrast to processes such as invasion, our understanding about endocytosis is only rudimentary. Hence, this manuscript provides important insights on an emerging topic that in our opinion deserves more attention:
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it identifies novel proteins at the K13 compartment and provides 2 new proteins in endocytosis (MyoF and KIC12); getting an as complete as possible list of proteins involved in the process will be critical to study and understand it
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it leads to the realisation that not all growth-relevant proteins detected at the K13 compartment are needed for endocytosis
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it provides domains and stage specificity of function for several K13 compartment proteins, overall bolstering the model of endocytosis in ART resistance and providing a framework critical to direct future studies on endocytosis and their detailed mechanistic function at the cytostome
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the identified vesicle trafficking domains (for instance now also found in UBP1) are expected to strengthen the support for the role of endocytosis of the K13 compartment; this and also the above points are important as (based on the current literature) there still seems to be prominent sentiment in the field that (in part due to the involvement of UBP1 and K13) the cause of ART resistance is due to various unclearly defined stress response pathways
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with MyoF it also shows the first protein in connection with the K13 compartment that acts downstream of the generation of hemoglobin-filled containers in the parasite and provides the first protein that explains the suspected involvement of actin in endocytosis (so far this was only based on CytD studies)
Overall we therefore believe this manuscript contains critical information and a framework for future studies on endocytosis and the K13 compartment. We hope the relevance of endocytosis as one of the most prominent and essential processes in the parasites and the connection to various aspects linked with many commercial drugs (in addition to the role of endocytosis in ART resistance), is adequately explained in the introduction. We also would like to mention that the main focus of the work is reflected in the title of the manuscript which does not mention ART susceptibility.
Major Comments
1) line 31: please change defined to characterised - defined suggests that novel proteins were identified in this study, which is not the case.
We apologise, but we do not fully understand this comment. We did identify novel proteins not before known to be at the K13 compartment (MCA2 (admittedly this one was likely but had not previously been verified), MyoF, KIC11 and KIC12). In our view "further defining the composition of the K13 compartment" therefore is an accurate statement. Additionally, the identification of previously not-discovered domains, the stage-specificity and function of these proteins helped to further define the K13 compartment.
If the reviewer is referring to the fact that the proteins analysed in this study were taken from a previously generated list of hits, we would like to stress that the presence in such a list (obtained from a BioID, but also if from an IP etc) can not be equalled for them to be true positives, they are merely candidates that still need to be experimentally validated. This is what we did in this work to find out which further proteins from the list can be classified as K13 compartment proteins (for hits with lower FDRs this is even more relevant as illustrated by the fact that 6 of the here analysed hits were not at the K13 compartment). In an attempt to address this comment in the manuscript, we changed the wording of this sentence to (line 31): "Here we further defined the composition of the K13 compartment by analysing more hits from a previous BioID, showing that MyoF and MCA2 as well as Kelch13 interaction candidate (KIC) 11 and 12 are found at this site."
2) line 37: please change 'second' to "another". As explained further below, the authors identified 3 classes of proteins (confer ART resistance + involved in HCCU, involved in HCCU only, or involved in neither).
We realized that the groups description wasn’t clear in the abstract. Please see response to major comment #41 for a detailed answer to this (endocytosis is an overarching criterion, ART resistance is a subgroup and applies only to those proteins with a function in endocytosis in ring stages). To clarify this (see also major point #8) we added an explanation on the influence of stage-specificity of endocytosis on ART susceptibility to the introduction (line 76): “In contrast to K13 which is only needed for endocytosis in ring stages (the stage relevant for in vitro ART resistance), some of these proteins (AP2µ and UBP1) are also needed for endocytosis in later stage parasites (Birnbaum et al., 2020). At least in the case of UBP1, this is associated with a higher fitness cost but lower resistance compared to K13 mutations (Behrens et al., 2021; Behrens et al., 2023). Hence, the stage-specificity of endocytosis functions is relevant for in vitro ART resistance: proteins influencing endocytosis in trophozoites are expected to have a high fitness cost whereas proteins not needed for endocytosis in rings would not be expected to influence resistance.” The abstract was changed in response to this and other comments and hope it is now clearer in regards to the groups.
3) Line 40: You define KIC11 as essential but according to your data some parasites are still alive and replicating 2 cycles after induction of the knock sideways. Please consider changing "essential" to "important for asexual parasite growth".
We fully agree with the reviewer, we reworded the sentence as suggested.
4) Line 40: please change 'second group' to 'this group'
We reworded this part of the abstract and it know reads: (line 38): “While this strengthened the link of the K13 compartment to endocytosis, many proteins of this group showed unusual domain combinations and large parasite-specific regions, indicating a high level of taxon-specific adaptation of this process.”
5) line 41: state here that despite it being essential, it is unknown what it is involved in.
With the newly added data we show that this protein either has a function in invasion or very early ring development although we did not see any evidence for the latter. We therefore changed the sentence to (line 43): “We here identified the first protein of this group that is important for asexual blood stage development and showed that it likely is involved in invasion*..” *
6) Line 50: the authors should state here that there is actually a reversal in this trend over the last few years.
Done as suggested.
7) Line 54: please separate out the references for each of the two statements made in this line (a: that ART resistance is widespread in SEA, and b: that ART resistance is now in Africa) Reference 14 also seems to reference ART resistance in Amazonia - which is not covered by the statement made by the authors (in which case the authors should state ART is now present in Africa and South America). The authors should also reference PMID: 34279219 for their statement that ART resistance is now found in Africa (albeit a different mutation to the one found in SEA).
Done as suggested.
8) Line 65: it is also worth mentioning here that there are other mutations in proteins other than K13, such as AP2mu and UBP1 (PMID: 24994911;24270944) that can lead to ART resistance.
As suggested by the reviewer, we included a sentence about non-K13 mutations linked with reduced ART susceptibility in the introduction (line 74): “Beside K13 mutations in other genes, such as Coronin (Demas et al., 2018) UBP1 (Borrmann et al., 2013; Henrici et al., 2020b; Birnbaum et al., 2020; Simwela et al., 2020) or AP2µ (Henriques et al., 2014; Henrici et al., 2020b)* have also been linked with reduced ART susceptibility." *
We here also added data on fitness cost that is related to this and is also relevant for the issue of proteins with a stage-specific function in endocytosis, making a transition for this statement which might help clarifying the grouping of K13 compartment proteins (see also major point #2).
9) Line 80, 86: ref 43 is misused. Reference 43 refers to Maurer's clefts trafficking which takes place in the erythrocyte cytosol and is not involved in haemoglobin uptake as far as I know. Please replace ref 43 with one showing the role of actin in haemoglobin uptake.
We thank the reviewer for pointing this out, Ref 43 was removed from the manuscript.
10) Line 98: the authors state here that they 'identified' further candidates from the K13 proxiome. This suggests that they identified new proteins in this paper, when in fact the list was already generated in ref 26. All they did was characterise proteins from that list that were not previously characterised. The authors should therefore remove identified from this statement.
We agree with the reviewer that we did not identify further candidates, we identified new K13 compartment proteins from the list of potential K13 compartment proteins. We therefore changed “identified further candidates” into “identified further K13 compartment proteins” (line 116). Please see also response to major comment #1.
11) Line 107-108: it is not clear from this sentence why these proteins were left out of the initial analysis in Ref 26. A sentence here explaining this would be valuable for the reader.
This is a good point. One reason why we did not analyse more in our previous publication was that we had to stop somewhere and adding more would have been very difficult to fit into what was already a packed paper. However, as shown in this work, the list does contain further interesting candidates (e.g. K13 compartment proteins that are involved in endocytosis).
We altered the relevant part of the introduction to highlight that we previously analysed the top hits, clarifying that the 'remaining' hits analysed in this work were further down in the list. This now reads: (line 113)“We reasoned that due to the high number of proteins that turned out to belong to the K13 compartment when validating the top hits of the K13 BioID (Birnbaum et al., 2020), the remaining hits of these experiments might contain further proteins belonging to the K13 compartment.” We hope this clarifies that we simply moved further down in the candidate list.
12) Line 117-123: The authors say that PF3D7_0204300, PF3D7_1117900 and PF3D7_1016200 were not studied because they were not in the top 10 hits. However, the current organisation of Supplementary Table 1 shows all 3 proteins among the top 10 hits (MyoF, KIC12, UIS14 and 0907200 being after them). I think the authors should reorganise their table. It is also unclear according to what the proteins in the table are ranked. Could the authors indicate the metric used for the ranking?
We thank the reviewer for alerting us to this. The issue here is that the 3 non-analysed proteins belong to a 'lower stringency' group comprising hits significant with FDRThe information about ranking is now also included as “Table legend” in the revised manuscript and the Table heading has been changed to: “List of putative K13 compartment proteins, proteins selected for further characterization in this manuscript are highlighted.”
13) Line 129-141: Can the authors be clearer with their explanations of the identification of mutation Y1344Stop? One dataset (ref 61) shows that 52% of African parasites have a mutation in MCA2 in position 1344 leading to a STOP codon. But another dataset (ref 62) shows that the next base is also mutated, reverting the stop codon. That should have been seen in the first dataset as well. Could the authors please clarify.
This mutation was first spotted in the MalariaGEN database (https://www.malariagen.net) (MalariaGEN et al., 2021), which allows online accessing of the data by using the “variant catalogue” tool, which is in a table format of frequency rather than in a sequence context. Hence, only after further research later on it became evident to us, that this mutation does not occur alone when looking at individual MCA2 sequences from patient samples in (Wichers et al., 2021b). We hope this is accurately reflected in our results section.
14) Line 147: the authors say that MCA2 is expressed throughout the intraerythrocytic cycle as shown by live cell imaging. In Birnbaum et al 2020 fig 4I, the authors show that MCA2 is mainly expressed between 4 and 16hpi. But in Figure 1B of this manuscript there is a clear multiplication of MCA2 signal between trophozoite and schizont. How do the authors explain this discrepancy? Could expression of the truncated MCA2 be different than the full length? This cannot be assessed as expression and localisation of the full-length HA tag MCA2 is not shown in Schizonts.
The key difference lies in transcription vs protein expression (usually protein levels peak after mRNA levels peak and - depending on turnover - protein levels can stay high even after mRNA levels have declined). Figure 4 of the Birnbaum et al paper presents transcriptomic data, but with a peak in trophozoites (The axis label in Fig. 4l of that publication is a bit confusing, as hour 0 is at the top, 48 h at the bottom; it is clearer in Fig. S13 of that paper) which would fit very well with the multiplication of the signal between trophozoites and schizonts mentioned by the reviewer. So, overall, the temporal peaks of transcripts and protein of that protein fit well.
For the signal in rings: Likely the protein has a turnover rate that is sufficiently low for some protein to be taken into the new cycle after re-invasion. Also different transcriptomic datasets e.g. (Otto et al., 2010; Wichers et al., 2019; Subudhi et al., 2020) available on plasmoDB show some mRNA present across the complete asexual development cycle, with each dataset showing maximum peak at a slightly different stage.
Even when located in foci and hence aiding detection of small amounts of protein (as is the case for MCA2-Y1344-GFP), the MCA2 signal in rings is not strong. For MCA2-TGD, the GFP signal is dispersed and therefore likely below our detection limit, while the same amount of protein concentrated at the K13 compartment is visible as foci in the MCA2-Y1344 cell line. Please note that MCA2-TGD has only 2.8% of the protein left whereas MCA2-Y1344 has 66.5% left and based on our manuscript is almost fully functional, hence fitting the different locations between the two versions.
Overall we believe this shows that there are actually no significant discrepancies of the expression of the different MCA2 versions.
15) Line 158: would it not have been more useful for the authors to have episomally expressed MCA2-3xHA in their MCA2Y1344STOP-GFPENDO line to make sure that the truncated protein is indeed going to the correct compartment? The experiments done by the authors suggests that the MCA2Y1344STOP goes to the right location but does not really confirm it.
We appreciate the reviewers caution here. However, considering that MCA2Y1344STOP-GFPendo co-locates with mCherryK13 and endogenously HA-tagged full length MCA2 does the same to a similar extent, there is in our opinion little doubt that MCA2 is found at the K13 compartment and that this is similar with both constructs. If there are minor differences, these might as well occur if MCA2 is episomally (as suggested in the comment) instead of endogenously expressed. Given the limited insight, we therefore decided against the episomal overexpression (which due to its size of > 6000bp may also be somewhat less straight forward than it may sound).
16) Line 191: it is stated that MCA2 confers resistance independently of the MCA domain, however in both the MCA2-TGD and MCA2Y1344STOP-GFPENDO parasites, the MCA domain is deleted, and for both parasites, there is resistance (albeit to a lower level in the MCA2Y1344STOP-GFPENDO line). Therefore, how can the authors state that the ART resistance is independent of the MCA domain? This statement should be that resistance is dependent on the loss of the MCA domain.
We agree that this can’t be categorically excluded. However, a ~5 fold difference in ART sensitivity was observed between the parasites with MCA2 truncated at amino acid 57 compared to those with MCA at amino acid 1344 even though both do not contain the MCA2 domain. Hence, at least this difference is not dependent on the MCA2 domain. The larger construct missing the MCA domain shows only a very moderate reduction in RSA survival, again suggesting the MCA domain is not the main factor. We amended our statement in an attempt to more accurately reflect the data (line 487): “This considerable reduction in ART susceptibility in the parasites with the truncation at MCA2 position 57 compared to the parasites still expressing 1344 amino acids of MCA2, despite both versions of the protein lacking the MCA domain, indicates that the influence on ART resistance is not, or only partially due to the MCA domain.” We would be hesitant to state the reviewer's conclusion that “resistance is dependent on the loss of the MCA domain”, as the larger construct missing the MCA2 domain has a milder RSA effect compared to MCA2-TGD, which suggests the reduction in ART susceptibility is independent of the MCA domain. These considerations also agree with the fact that the parasites with the longer MCA2 version (in contrast to the MCA2-TGD) do not have any detectable growth defect which indicates that the protein can fulfil its function without the MCA2 domain.
17) Line 192: Why did the authors not check if MCA2 is involved in endocytosis? They state later on in the manuscript that they did not do endocytosis assays with TGD lines, however if the authors include the correct controls, this could be easily done. It would also be really interesting to see whether endocytosis gets progressively worse going from WT to MCA2Y1344STOP to MAC2TGD. This experiment (as well as doing endocytosis assays for KIC4 and KIC5 TGD lines) would drastically increase the impact of this study. These experiments would not take more than 3 weeks to perform, and would not require the generation of new lines.
So far were very hesitant to do bloated FV assays with TGDs (even though TGDs were available for the genes encoding MCA2 and KIC4 and KIC5). The reason for this was:
- the fact that these proteins could be disrupted indicated either redundancy or only a partial effect on endocytosis which might lead to only small effects that likely are difficult to pick up in an assay scoring for the rather absolute phenotype of bloated vs non-bloated. Using the refined assay measuring FV size could partly amend this but we note that also FV without hemoglobin have a certain size, reducing the relative effect if there are smaller differences.
- a TGD line does not permit tightly controlled inactivation of the target which makes comparing the outcome of bloated food vacuole assays difficult if there are smaller growth and stage differences to the 3D7 control.
- in contrast to conditional inactivation parasites, the TGD lines had ample times to adapt to loss of the target protein (compensatory mechanisms are well known for endocytosis, for instance in clathrin mediated endocytosis loss of individual components can be compensated (Chen and Schmid, 2020)). We nevertheless see the reviewer's point that this should at least be attempted and now conducted these assays (see also major point 40). For MCA2 (as requested in this point), the data is shown in Figure S5C-E. This assay showed that in MCA2-TGD, MCA2Y1344STOP-GFPendo (similar to the 3D7 control) >95% of parasites developed bloated food vacuoles. Additionally, we also measured the parasite and food vacuole size of individual cells in an attempt to solve some of the problems with TGDs with such assays. In order to specifically solve problem 2 mentioned above, we analysed the food vacuoles of similarly sized parasites, however, they were non-distinguishable between the three lines. Of note, in agreement with the reduced parasite proliferation rate (Birnbaum et al., 2020) a general effect on parasite and food vacuole size was observed for MCA2-TGD parasites, indicating reduced development speed in these parasites. Hence, it is possible that a potential endocytosis reduction was accompanied by a slowed growth, and the comparison of similarly sized parasites may have obscured the effect. It is therefore not sure if there indeed is no endocytosis phenotype, although we can exclude a strong effect in trophozoites.
Based on the RSA results at least rings can be expected to have a reduced endocytosis in the MCA2-TGD. Apart from options 1-3 mentioned above, it is therefore possible there is an effect restricted to rings, although in that case the reduced growth in trophozoites would be due to other functions of MCA2. Overall, we can conclude that the MCA2-TGD parasites do not have a strongly reduced endocytosis, but given the fact that the parasites are viable, this is not surprising. Whether the MCA2-TGD has no effect at all on endocytosis we would be very hesitant to postulate based on these results.
18) The authors should consider re-organising the MCA2 section, first showing that the 3xHA tagged line colocalises with K13, then performing the new truncation.
We attempted to re-organise as suggested but because we now included additional fluorescence microscopy images of schizont and merozoites (in response to reviewer 2 major comment 3) the main figure would become even larger. To prevent this, we kept the 3xHA data in the supplement.
19) Line 197: Once again ref 43 is not correct to illustrate that actin/myosin is involved in endocytosis
We thank the reviewer for pointing this out – we removed Ref 43.
20) Line 202: the authors state that MyoF localises near the food vacuole from ring stage/trophs onwards. However, how can this statement be made in schizonts based on these images (Fig. 2A), where it doesn't look like MyoF is anywhere near the FV? This statement can only be made for schizonts if co-localised with a FV marker (which is done in Fig. 2B), however, based on the number of MyoF foci, it appears that this was not done for schizonts. Please either remove the statement that MyoF is near the food vacuole from trophs onwards (because it is only seen near the FV up until trophs) or show the data in Fig. 2B of schizonts to substantiate these claims.
This is a valid point. We originally did not focus on schizonts because most markers end up in some focal area in the forming merozoite but other proteins (such as e.g. K13) also have one or more additional foci at the FV, making interpretation unclear, particularly if the schizont is still organizing to become fully segmented. This is why we generally focused the K13 co-localisations on the trophozoite stage to obtain the clearest information on endocytosis. However, given the fact that this manuscript gives the first localization of MyoF in P. falciparum parasites, we now provide a comprehensive time course (Figure 1C, S1A) including schizonts, which show quite a complex pattern: while the MyoF-GFP localization in trophozoites appeared as multiple foci close to K13 and also the FV, the MyoF-GFP pattern changes in late schizonts (fully segmented) and merozoites, appearing as elongated foci no longer close to K13 or the FV. Of note, this pattern has been previously reported for MyoE in P. berghei (Wall et al., 2019).
We therefore revised the statement about MyoF localization in schizont to better reflect the observed localization: (line 175): “In late schizonts and merozoite the MyoF-GFP signal was not associated with K13, but showed elongated GFP foci (Figure 1C, S2A) reminiscent of the MyoE signal previously reported in P. berghei schizonts (Wall et al., 2019).”
21) Line 204-206: what does this statement bring to the paper? Is it to show that it is the real localisation of MyoF because 2 tag cell line show the same localisation? I don't think this is needed, especially as later in the manuscript an HA-tag MyoF line is used and show similar localisation.
We see the reviewers point, but prefer to keep this data included in the supplement, particularly because potential differences in the location of tagged MyoF were a major concern.
Related to the tag issue: in order to get a better understanding of the effect of C-terminally tagging with different sized tags we now performed a more detailed analysis of the MyoF-3xHA cell line (Figure S2F-G), showing that this cell line shows a growth rate similar to the 3D7 wild type parasites, and has less vesicles than the 2x-FKBP-GFP-2xFKBP cell line, but still slightly, but significantly more than 3D7 parasites. Overall, this indicates that the smaller 3xHA tag has less effect on the parasite, than the larger 2x-FKBP-GFP-2xFKBP tag (see also new Figure 1L, showing a correlation of level of inactivation and the endocytosis phenotype for MyoF).
22) Line 212: The overlap of K13 with MyoF in Figure 2C 3rd panel (1st trophozoite panel) is not obvious, especially as the MyoF signal seems inexistant. I would advise the authors to replace with a better image. Also, why are there no images of schizonts shown in Figure 2C?
As suggested we exchanged the trophozoite image of panel Figure 2 C (now Figure 1C) and expanded this panel with images covering the complete asexual development cycle including schizonts in response to this and the previous points. As indicated above (point 20), schizont stages are complex to interpret. While late schizonts likely are not very relevant for endocytosis this is the first description of the location of the protein in this parasite and we therefore now provide a more thorough representation of the MyoF location across asexual stages in Figure1C and S2A.
23) Line 217: the spatial association of MyoF with K13 is very different when it is tagged with GFP and when it is tagged with 3xHA. The way the authors word it here, it seems that there is agreement with the two datasets, when this is not in fact the case (59% overlap for MyoF-GFP and only 16% overlap with MyoF-3xHA). These data suggest that the GFP and the multiple FKBP tags are doing something to the protein and therefore maybe the ensuing results using this line should not be trusted or be taken with a pinch of salt.
We agree with the reviewer that the location of this MyoF-GFP in the cell might differ due to the partial inactivation but in contrast to this comment, the data does not indicate any large differences. It seems the reviewer mixed something up (the 59% mentioned might come from the MCA2 figure?). The data with the two lines with differently tagged MyoF co-localised with K13 are actually quite comparable: GFP-tagged vs HA-tagged MyoF overlapping with K13 was 8% vs 16% full overlap, 12% vs 19% partially overlapping foci, 36% vs 63% foci that were touching but not overlapping (compare what now is Figure 1D and Figure S2C). Only in the 'no overlap' there is a much smaller proportion in the HA-tagged line. However, given that these are IFAs which on the one hand are more sensitive to see small protein pools but on the other hand also have pitfalls due to fixing of the cells (e.g. tiny increase in focus size due to fixing could increase the number of touching foci that in live cells might be close but did not touch), some variation can be expected to the live cells. We agree though that the partly reduced functionality of MyoF might be the reason for the consistent tendency of a lower overlap even though the difference is much less than indicated in the comment. We added "with a tendency for higher overlap with K13 which might be due to the partial inactivation of the GFP-tagged MyoF" to the sentence "IFA confirmed the focal localisation of MyoF and its spatial association with mCherry-K13 foci"
While we expect the fact that the difference between these parasites is only small somewhat reduces the "pinch of salt" with the MyoF line, we do agree that the partial functional inactivation of the GFP-tagged MyoF line may have some impact. However, we do not think that this means the results with the MyoF-GFP line are untrustworthy. On the contrary, it provides insights into its function that in some ways is equivalent to a knock down or TGD. Overall all the MyoF lines show: few vesicles occur in the MyoF-HA-line, more in the MyoF-GFP line and even more after knock sideways of MyoF-GFP. Importantly the severity of this phenotype correlates with the growth rates in these lines. Hence, together with the bloated food vacuole assays, this provides consistent data indicating that MyoF has a role in the transport of HCC to the FV and its level of activity correlates with the number of vesicles and growth. To better highlight this, it is now summarised in Figure 1M.
24) Line 219: the authors state here that they could not detect MyoF-GFP in rings, when in Figure 2C they show MyoF-GFP in rings, and also show that they could detect MyoF in Sup Fig. 3B with the 3xHA tagged line. Is this a labelling mistake in Figure 2C? If the authors could indeed not see MoyF-GFP in rings, this statement should have been made when Figure 2A was presented, and not so late in the manuscript, which causes confusion.
We thank the reviewer for pointing this out. We now provide a detailed time course (see also previous points) which shows that there is no detectable MyoF-GFP signal during ring stage development until the stage where the parasites starts the transition to trophozoites (i.e. MyoF-GFP signal could only be observed in parasites already containing hemozoin). In addition to the extended time course in Figure 1C (previously 2C) we included a panel of example ring stage images below to further highlight this. We also changed the labelling of the parasite with MyoF-GFP signal the reviewer mentions in Figure 1C to “late ring stage” (it already contains hemozoin) to clarify this.
The description of Figure 1A is now changed to: (line 153) *“The tagged MyoF was detectable as foci close to the food vacuole from the stage parasites turned from late rings to young trophozoite stage onwards, while in schizonts multiple MyoF foci were visible (Figure 1A, S2A).” *
Please see our answer to major comment #45 where we provide an explanation for the difference between MyoF-3xHA and MyoF-GFP signal in ring stage parasites.
[Figure MyoF]
25) Line 237: Showing a DNA marker (DAPI, Hoecht) for Figure 2E, and subsequent figures using mislocalisation to the nucleus, would help the reader assess efficiency of the mislocalisation.
Please see response to major comment #64 for a detailed answer on why we did not include DNA staining in the imaging used to assess mislocalization upon knock-sideways.
26) Line 254-256: authors should show the results of the bloating assay for parental 3D7 parasites (+ and - rapalog) to see whether the MyoF line - rapalog has increased baseline bloating. This applies to all subsequent FV bloating assays.
We did do several controls for bloated assays (including +/- rapalog of an irrelevant knock sideways line as well as using a chemical insult for which the control was 3D7 without treatment) in previous work (Birnbaum et al., 2020), which indicated that there is no effect of rapalog to reduce bloating. Although these controls are more stringent, we nevertheless did a 3D7 +/- rapalog control and added this to the manuscript (Figure S2I). As it is not possible to do this side by side with the assays that are already in the manuscript and the +/- rapalog 3D7 cells consistently showed no or very low numbers of cells without bloating (and stringent controls in the past equally did not show an effect), we believe adding this control once suffices.
27) Line 254-257: The authors say that because fewer parasites show a bloated food vacuole upon inactivation of MyoF it means that less hemoglobin reached the food vacuole. I understand the authors statement, however, shouldn't they look at the size of the food vacuole, instead of the number of parasites with bloated FV, to make such a statement? This has been done for KIC12 so why not doing it for MyoF?
This was now done and is provided as Figure 1J-K, S2J. The results confirm the assessment scoring bloated vs non-boated food vacuoles.
28) Line 259-261: these results would be difficult to interpret namely because the authors have dying parasites, which is exacerbated with the protein being knocked sideways. The authors should mention the pitfalls their knock sideways and tagging design here. Line 260-261: RSA is an assay relying on measuring parasite growth 1 cycle after a challenge with ART for 6 hours.
Fortunately, this concern is unfounded, as the survival (measured by parasitemia after one cycle) of the same sample + and - DHA is assessed, isolating the DHA effect independent of potential growth defects which are cancelled out. Hence, if there were parasites dying in the MyoF line (please note that they might not actually die, but simply grow more slowly), this factor applies for both the + and - ART condition. As we are testing for a decreased susceptibility to ART which would manifest as an increased survival in RSA surfacing above 1%, antagonistic effects of reduced MyoF function and ART treatment would not result in detectable differences as without effect, the RSA survival is always close to zero.
The same applies for the knock sideways where we assess the survival of +rapalog between +ART and -ART. If the reduced MyoF activity of the knock sideways leads to a decreased survival, this applies to both +ART and -ART. Please also note that rapalog was lifted after the DHA pulse (see e.g. Figure S2K).
That effects on growth are cancelled out is nicely illustrated for proteins where there is a stronger and more rapid effect on growth upon their conditional inactivation. For instance when KIC7 is knocked aside, there is a considerable increased of RSA survival, even though continued inactivation of KIC7 would have a severe growth defect (Birnbaum et al., 2020). Vice versa, a growth defect alone does not result in reduced RSA susceptibility as evident from knock sideways of an unrelated protein or using a chemical insult (Figure 4H in (Birnbaum et al., 2020) or simply slowing the ring stage by e.g. reducing EXP1 levels (Mesén-Ramírez et al., 2019). Hence, a growth reduction is not expected to alter the RSA outcome. And even if it did, it would only lead to an underestimation of the readout if growth is too severely affected (which would be obvious in the + rapalog without DHA sample, which was not the case).
In that respect it is valuable to have the rapid kinetics of knock sideways which permit inactivation of a protein before severe growth defects occur (although the only partial responsiveness of MyoF clearly is not the most optimal). In contrast, the absolute loss of a gene (as is the case if diCre is used) prevents (or at least makes it extremely difficult as the timing would need to exactly hit sufficient protein reduction without killing the parasite until the end of the RSA) using this system in these experiments (again see (Mesén-Ramírez et al., 2021) where in a EXP1 diCre based knock out RSA was only possible because we complemented with a lowly, episomally expressed EXP1 copy to have parasites with only a partial phenotype to do this assay).
29) Line 261-263: the authors sate that MyoF has a function in endocytosis but at a different step compared to K13 compartment proteins. I am not sure what they mean here. Can this be clarified?
The different steps in endocytosis are explained in the introduction and we now tried to further clarify this (line 98). “So far VPS45 (Jonscher et al., 2019), Rbsn5 (Sabitzki et al., 2023), Rab5b (Sabitzki et al., 2023), the phosphoinositide-binding protein PX1 (Mukherjee et al., 2022), the host enzyme peroxiredoxin 6 (Wagner et al., 2022) and K13 and some of its compartment proteins (Eps15, AP2µ, KIC7, UBP1) (Birnbaum et al., 2020) have been reported to act at different steps in the endocytic uptake pathway of hemoglobin. While inactivation of VPS45, Rbsn5, Rab5b, PX1 or actin resulted in an accumulation of hemoglobin filled vesicles (Lazarus et al., 2008; Jonscher et al., 2019; Mukherjee et al., 2022; Sabitzki et al., 2023), indicative of a block during endosomal transport (late steps in endocytosis), no such vesicles were observed upon inactivation of K13 and its compartment proteins (Birnbaum et al., 2020), suggesting a role of these proteins during initiation of endocytosis (early steps in endocytosis).“
VPS45 has not apparent spatial connection to the K13 compartment but the fact that MyoF does - and its inactivation also results in vesicle accumulation - indicates that it is downstream of vesicle initiation, providing the first connection from the initiation phase to the transport phase. More evidence for these different steps of endocytosis has been published in a recent preprint from our lab, where we simultaneously inactivated a protein of both “endocytosis steps” (Sabitzki et al., 2023).
To clarify this in the results as requested, we changed the statement to: (line 256) “Overall, our results indicate a close association of MyoF foci with the K13 compartment and a role of MyoF in endocytosis albeit not in rings and at a step in the endocytosis pathway when hemoglobin-filled vesicles had already formed and hence is subsequent to the function of the other so far known K13 compartment proteins.”
30) Do the authors mean that it is involved in endocytosis but not in ART resistance? If so, this is a very difficult statement to make since the parasites are dying. Is there any evidence of point mutations in MyoF in the field?
We split this point to address all issues raised here. Please see response to point 29 which clarifies that this was meant in a different way and our response to point 28 which explains why the dying parasite issue is not expected to affect the RSA (please also note that we do not have evidence of actually dying parasites in the MyoF-2xFKBP-GFP-2xFKBP line, most likely the growth is slowed).
The mutation issue is interesting. In fact evidence exists that MyoF mutations may be associated with resistance (Cerqueira et al., 2017) (please note that there it is still called MyoC) but in a recent preprint from our lab we did not find any evidence for a significantly changed RSA survival in 12 tested mutations in the corresponding gene (Behrens et al., 2023).
To clarify this we added the following statement to the discussion (line 709): "Of note, mutations in myoF have previously been found to be associated with reduced ART susceptibility (Cerqueira et al., 2017), but 12 mutations tested in the laboratory strain 3D7 did not result in increased RSA survival (Behrens et al., 2023)*. *
31) Line 298: the authors state that there is no growth defect in the first cycle when rapalog is added to the KIC11 line, however based on Figure 3D, there is evidently a 25% reduction in growth compared to - rapalog at day 1 post treatment, and a 60% reduction by day 2, which is still within the 1st growth cycle. The authors should either revise their statement or provide an explanation for these findings. The authors should also explain why their Giemsa data in Fig. 3E is not in accordance with their FACS data.
We think there is a misunderstanding here, as our figure legend was not detailed enough and we apologise if this had been misleading. The growth effect is restricted to invasion or possibly the first hours of ring stage development (see point 4&5, reviewer 2), which in asynchronous cultures more rapidly takes effect as the culture also contains schizonts that immediately generate cells that re-invade but can't due to inactivation of KIC11 (due to the rapid action of the knock sideways, KIC11 is already inactivated). In contrast, in highly synchronous cultures, this effect can only be evident once the parasites reached the schizont stage (starting with rings this takes close to 2 days). We now clarify that Figure 2E (previously Figure 3D) shows growth data obtained with an asynchronous parasite culture, while in Figure 2F the growth assay is performed with tightly synchronized (4h window) parasites as stated in the Figure legend.
We now explicitly state in each Figure legend and for each growth experiment throughout the manuscript whether we used asynchronous or synchronized parasites for growth assays.
Related to this, the incorrect y-axis label of what is now Figure 2E mentioned in major comment #58 is now corrected.
32) Line 301: KIC11 could also be important very early for establishment of the ring stage for example for establishment of the PV. Also, was mislocalisation assessed in rapalog-treated parasites at 72 hours or in cycle 3?
This is a valid point and this has now been addressed. We performed an invasion/egress assay revealing similar schizont rupture rates, but significantly reduced numbers of newly formed ring stage parasites (Figure 2H, S3G), indicating an effect of KIC11 inactivation either on invasion or possibly the first hours of ring stage development. A very similar point was raised by Reviewer 2, please see reviewer 2; major comment #4. This is now also reflected in line 302, which now reads: ”… indicating an invasion defect or an effect on parasite viability in merozoites or early rings but no effect on other parasite stages (Figure 2F-H, Figure S3F-G).”
We further included an assessment of mislocalization 80 hours after the induction of knock-sideways by addition of rapalog in Figure S3E which showed mislocalization of KIC11 to the nucleus.
33) Line 311: the authors should change the sentence from 'not related to endocytosis' to 'not related to endocytosis or ART resistance'.
Done as suggested.
34) Line 323-325: Authors say that a nuclear GFP signal can be observed in early schizonts for KIC12. According to the pictures provided in Figure 4A and Figure S5A it is not very obvious. Also faint cytoplasmic GFP signal could only be background as we can see that exposure is higher for schizont pictures
We changed the sentence (line 339) to: “…nuclear signal and a faint uniform cytoplasmic GFP signal was detected in late trophozoites and early schizonts and these signals were absent in later schizonts and merozoites (Figure 3A, Figure S4A,B).” in order to emphasize that the nuclear signal disappears early during schizont development.
35) Line 326-328: The authors say that kic12 transcriptional profile indicate mRNA levels peak (no s at peak) in merozoites. Should they show live cell imaging of merozoites then? Because from the Figure 4A schizont pictures where schizonts are almost fully segmented no signal can be observed.
The observation that mRNA levels of early ring stage expressed proteins tend to increase already in mature schizonts and merozoites is well established (e.g. (Bozdech et al., 2003)). A very good example for this are exported proteins of which most show a transcription peak in schizonts but the proteins are only detected in rings see e.g. (Marti et al., 2004). Hence, our observation for KIC12 is quite typical.
We originally did not include merozoites, as in the last row of Figure 3B fully developed merozoites within a schizont with already ruptured PVM are shown and no GFP signal can be detected in these parasites. We now provide images of free merozoites in Figure S4A-B showing again no detectable GFP signal.
We thank the reviewer for pointing out the typo, "peak" has been corrected.
36) Line 347: The authors state that using the Lyn mislocaliser the nuclear pool of KIC12 is inactivated by mislocalisation to the PPM. This tends to suggest that only the nuclear pool of KIC12 is mislocalised. How is it possible that only the nuclear pool is mislocalised?
The Lyn mislocaliser is at the PPM which is continuous with the cytostomal neck where the K13 compartment likely is found. The effect of the Lyn mislocalizer on the KIC12 protein pool localizing at the K13 compartment is therefore somewhat unclear. For this reason we already had the following statement in the original submission (line 400): “Foci were still detected in the parasite periphery and it is unclear whether these remained with the K13 compartment or were also in some way affected by the Lyn-mislocaliser.” We would like to stress here that the same does not apply to the nuclear mislocaliser, which is only a trafficking signal delivering KIC12 to the nucleus and hence likely does not affect the nuclear pool of KIC12, only the K13 compartment pool (the main interest of this manuscript).
We realised that the statement towards the end of this paragraph was unnecessarily ambiguous in regards to the K13 compartment pool of KIC12 which might have caused some confusion about the function of this pool of KIC12 and therefore modified it to (line 374): "Due to the possible influence on the K13 compartment located foci of KIC12 with the Lyn mislocaliser, a clear interpretation in regard to the functional importance of the nuclear pool of KIC12 other than that it confirms the importance of this protein for asexual blood stages is not possible. In contrast, the results with the nuclear mislocaliser indicate that the K13 located pool of KIC12 is important for efficient parasite growth.". It is also important to note that this limitation does not apply to the NLS knock sideways in regard to the K13 compartment and that the endocytosis function of this pool of KIC12 seems solid which with this statement is enforced.
37) Line 368-369: Effect was also only partial for MyoF. Why didn't you measure the same metrics for MyoF?
This was now done and is provided as Figure 1J-K, S2J, confirming our previous interpretation, see also point #27 which raises the same point.
38) Line 379: you don't know if all proteins acting later in endocytosis will have an increased number of vesicles as a phenotype
This is based on our current definition as stated in the introduction. It assumes a directional vesicular transport of hemoglobin to the food vacuole where inhibition of early stages will prevent transport before HCC-filled autonomous vesicular containers have formed and entered the cell. In contrast later inhibition stops such containers from further transport, leading to their accumulation. Such an accumulation is visible after VPS45-inactivation and other proteins (Jonscher et al., 2019; Mukherjee et al., 2022; Sabitzki et al., 2023) or treatment with cytochalasin D (Lazarus et al., 2008). While it is possible that there may be smaller intermediates formed at the K13 compartment that later on unite or fuse with the compartment evident after VPS45 inactivation and these might be missed due to small size (i.e. inhibition of a step between K13 compartment and an early endosome or equivalent), this would still be upstream of the VPS45 induced containers and hence would be earlier. We therefore believe that based on the framework given in the introduction (see also (Spielmann et al., 2020)) to assume that a phenotype manifesting as reduced food vacuole bloating without formation of detectable vesicles likely signifies inhibition of the process early whereas reduced bloating but with vesicles signifies inhibition later in the process.
39) Line 413-414: The authors state that no growth defect was observed upon KS of 1365800. Is growth alone enough to say that there is no impact on endocytosis?
This is an interesting point. The endocytosis proteins we studied so far indicate that efficient impairment of endocytosis manifests as a severe growth defect. Hence, lack of a growth defect can be assumed to be an indicator for absence of an important role for endocytosis (or any other growth relevant process). Clearly there is a gradual response, such as seen in the different MyoF versions resulting in proportional growth and vesicle appearance phenotypes. Hence, a protein with a minor role might have slipped our attention but then it probably is also not a very important protein in endocytosis.
To further strengthen our assessment of PF3D7_1365800 importance for asexual blood stage development, we now also generated a cell line expressing the PPM Mislocalizer, enabling knock sideways to the PPM. This was done because this protein consistently has a focus at the nucleus that may be within the nucleus. Again this revealed no growth defect upon inactivation (Figure S7D).
40) Line 432: in this section, the authors state that KIC4 and KIC5 seem to have domains that may suggest these proteins are involved in endocytosis, based on the alpha fold data that is publicly available. Considering the authors have TGD-SLI versions of these lines (Birnbaum et al. 2020) and have already confirmed in this previous publication that they confer resistance to ART; it would make sense to look at endocytosis for these genes. This would be a relatively simple and straightforward experiment, taking no longer than two to three weeks, and would require no additional reagents or line generation. Doing these experiments would add a lot more weight to this final section. The authors later state that KIC4 and 5 are TGD lines, so not the best for endocytosis assays. It is unclear why this would be difficult to do if an adequate control is contained in the experiment (such as parental 3D7). It explains why they did not perform the MCA2 endocytosis assays further up, but in my opinion, an attempt at doing these assays is important and would significantly increase the impact of this paper. Identical as major comment #17.
As stated in the manuscript and above, we were originally hesitant to do these assays due to the fact that we can't induce inactivation which is less ideal than comparing the identical parasite population split into plus and minus and is further complicated by the likely smaller effect as the TGDs still permitted growth. However, we see the point of the reviewer and now performed these assays using 3D7 as controls and taking extra care to account for stage differences between the TGD lines and 3D7. However, there was no significant difference in the bloated food vacuole assays with these cell lines. Due to the reasons mentioned in major point 17, we are not sure this indeed means these proteins have no role in endocytosis. One possible reason why we were able to obtain these TGDs may have been because the effect on endocytosis is less than in the essential proteins (or is ring stage specific) and in a TGD an endocytosis defect may therefore not be detectable with our assays (see details and further possible explanations in response to point 17).
In an attempt to address the TGD issue, we generated knock sideways cell lines for KIC4 and KIC5. Unfortunately, the mislocalization of KIC5 to the nucleus was inefficient (see figure below). As this did not result in a growth defect (in contrast to the clear KIC5-TGD growth defect (Birnbaum et al., 2020)), this line is not suitable to study a potential role of this protein in endocytosis. Therefore, we performed the bloated food vacuole assay only with KIC4-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser parasites. However, this revealed no effect on HHC uptake, which is in line with the normal growth of KIC4-TGD parasites (Birnbaum et al., 2020) and suggests that this protein could only have a minor or redundant role in endocytosis (it is the line that shows the smallest effect in RSA). As the KIC4 and KIC5 knock sideway lines did not permit any conclusions, we did not include them into the revised manuscript but they can be found here:
[Figure KIC4 knock sideways & KIC5 knocksideways]
Figure legend: (A) Live-cell microscopy of knock sideways (+ rapalog) and control (without rapalog) KIC4-2xFKBP-GFP-2xFKBPendo+ 1xNLS mislocaliser parasites 4 and 20 hours after the induction of knock-sideways by addition of rapalog. Scale bar, 5 µm. Relative growth of asynchronous KIC4-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser plus rapalog compared with control parasites over five days. Three independent experiments were performed. Growth of knock sideways (+ rapalog) compared to control (without rapalog) KIC4-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser (blue) or KIC5-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser (red) parasites over five days. Mean relative parasitemia ± SD is shown. (B) Live-cell microscopy of knock sideways (+ rapalog) and control (without rapalog) KIC5-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser parasites 4 and 20 hours after the induction of knock-sideways by addition of rapalog. Scale bar, 5 µm. Growth of asynchronous KIC5-2xFKBP-GFP-2xFKBPendo+ 1xNLSmislocaliser plus rapalog compared with control parasites over five days. Four independent experiments were performed. __(C) __Bloated food vacuole assay with KIC4-2xFKBP-GFP-2xFKBPendo+1xNLSmislocaliser parasites 8 hours after inactivation of KIC4 (+rapalog). Cells were categorized as with ‘bloated FV’ or ‘non-bloated FV’ and percentage of cells with bloated FV is displayed; n = 3 independent experiments with each n=19-30 (mean 21.4) parasites analysed per condition. Representative DIC are displayed. Area of the FV, area of the parasite and area of FV divided by area of the corresponding parasites were determined. Mean of each independent experiment indicated by coloured symbols, individual datapoints by grey dots. Data presented according to SuperPlot guidelines (Lord et al., 2020); Error bars represent mean ± SD. P-value determined by paired t-test. Area of FV of individual cells plotted versus the area of the corresponding parasite. Line represents linear regression with error indicated by dashed line.
41) Line 490-493: the authors state that the K13 compartment proteins fall in two groups, some that are involved in ART resistance AND endocytosis, and some that have different functions. However, in this manuscript the authors have demonstrated 3 flavours that K13 compartment proteins can come in: • Some that confer ART resistance and are involved in HCCU (MCA2) • Some that are involved in HCCU but not ART resistance (MyoF & KIC12) • Some that are involved in neither (KIC11) The authors should therefore revise this statement.
We agree that this was not well phrased. To account for the fact that not all endocytosis proteins confer increased RSA survival to the parasites when inactivated we changed this statement (line 604): "This analysis suggests that proteins detected at the K13 compartment can be classified into at least two groups of which one comprises proteins involved in endocytosis or in vitro ART resistance whereas the other group might have different functions yet to be discovered.“
Generally, we believe that endocytosis is the overarching criterion and we therefore would like to keep the definitions of the main groups (endocytosis or not). As indicated by the title, the focus of the manuscript is on the K13 compartment for which so far endocytosis is the only experimentally associated function. That this group contains proteins that do not confer reduced ART susceptibility when conditionally inactivated (KIC12 and MyoF) is explained by their stage-specificity, making this a subgroup of the overarching endocytosis group.
We realise that with the endocytosis data on the KIC4, KIC5 and MCA2 TGD there is now also a subgroup we were unable to demonstrate an endocytosis effect in trophozoites although they show changes in RSA survival. However, as indicated above, we would be hesitant to fully exclude some role of these proteins in endocytosis in rings. Particularly as a comparably small reduction in endocytosis protein activity or abundance is sufficient to increase RSA survival (Behrens et al., 2023). A principal classification of "endocytosis or ART resistance" or "neither endocytosis nor ART resistance" still accounts for this and therefore seems to us to be the most useful, particularly also in light of our domain identification that then can be linked with one or the other group.
42) Line 508: the authors state that they expanded the repertoire of K13 compartments, when in fact they functionally analysed them - they did not do another BioID to identify more candidates.
We respectfully disagree with the reviewer in this point, we did expand the repertoire of known K13 compartment proteins. Only independently experimentally validated proteins from proximity biotinylation experiments can be considered part of the K13 compartment (or any other cellular site or complex). Without validation of the location, the identified proteins can only be considered candidates. This is highlighted in this manuscript by the finding that several proteins of the list did not localize at the K13 compartment.
43) Line 570-572: has anyone ever tested whether CytoD or JAS treatment in rings, is sufficient to mediate ART resistance? Something similar to what was done in PMID 21709259 with protease inhibitors. If not this would be a pretty interesting experiment for the authors to do that could shed more light on the MyoF data. It would take maybe 2 weeks to do and not require the generation of any new lines. This would clarify whether other Myosins other than MyoF are involved in endocytosis, as is suggested by previous publications (PMID: 17944961).
We now included this experiment. In agreement with a lacking need of MyoF in rings and no effect on RSA survival, there was no increased survival of the parasites in RSA (neither on 3D7 nor on K13 C580Y parasites) after cytD treatment (new part in Figure 1M). We thank the reviewer for pointing out that this experiment might also inform on whether other myosins influence endocytosis in ring stages. We added (line 250): “Similarly, also incubation with the actin destabilising agent Cytochalasin D (Casella et al., 1981), had no effect on RSA survival in 3D7 or K13C580Y (Birnbaum et al., 2020) parasites, indicating an actin/myosin independent endocytosis pathway in ring stage parasites (Figure 1M) and speaking against other myosins taking over the MyoF endocytosis function in rings.”
44) Line 608: inhibitors targeting the metacaspase domain of MCA2 may inadvertently inactivate other essential parts of the protein. They authors should acknowledge this possibility in the text.
The inhibitors used in the cited studies (Kumari et al., 2018) are validated metacaspase inhibitors, such as Z-FA-FMK (Lopez-Hernandez et al., 2003). Activity against the other parts of PfMCA2 - which apart from the MCA domain shows no homology to other proteins - is therefore unlikely.
45) Line 624-625: the authors state that MyoF is 'lowly expressed in rings' - indeed this is the case in their MyoF-2xFKBP-GFP-2xFKBP line which the authors established has defects due to the tag, but it appears from their MyoF-3xHA tagged line that it is expressed in rings. The authors should therefore revise their statement, and be careful of making claims based on their defective line and using fluorescence imaging as their only metric. If they do want to make the statement that it is not there in rings, they should also do a western blot, which is much more sensitive since it amplifies the signal compared to an image of one parasite.
This comment is related to major point #24. We also would like to stress that while the MyoF-GFP line already shows a phenotype, the impression of defectiveness based on its location is due to a mix up (see major point #23).
We now provide a comprehensive time course of the MyoF-GFP signal (Figure 1C, S2A) showing that there is no detectable MyoF-GFP signal until the transition from ring to trophozoite stage. As this is all under the endogenous promoter, we do not think the partial functional inactivation of the tagging is the reason for the absence of the signal. If anything, we would have expected adding a stably folded structure such as GFP to increase the stability of the protein. The main reason for the discrepancy of MyoF signal in rings between the GFP-tagged line (of note there is also no detectable MyoF-GFP signal in MyoF-2xFKBP-GFP ring stage parasites (Figure S2B)) and the HA-tagged line likely is that IFA is much more sensitive than live GFP detection (similar to the high sensitivity the reviewer mentions in regards to WB). This discrepancy therefore is likely due to the fact that the lowly expressed MyoF only become apparent with the HA-tagged line due to the IFA. We therefore believe that MyoF is 'lowly expressed in rings' is an appropriate description of our results obtained with three different cell lines (MyoF-2xFKBP-GFP-2xFKBP, MyoF-2xFKBP-GFP and MyoF-3xHA). We hope this is sufficiently well reflected in the manuscript where we write ‘a low level of expression of MyoF in ring stage parasites.’ not that it is ‘not there in rings’ (line 174).
46) Line 635: arguably this is the 3rd variety and not the 2nd (the authors already mentioned 2 types - ones that are involved in HCCU AND ART and those involved in HCCU only). See comment for line 490-493 above.
See response for major comment #41, we now consistently used "or" instead of "and". See line 490-493 how this was resolved for what previously was line 635.
47) Line 785: Bloated food vacuole assay/E64 hemoglobin uptake assay method specify that a concentration of 33mM E64protease inhibitor was used. However, in reference 44, cited in the manuscript, a concentration of 33µM E64 was used. Please confirmed if this is just a typo or if 1000x E64 concentration was used which renders the experiment invalid.
We thank the reviewer for pointing this out, we corrected this typo and will look out for symbol font conversion errors for the resubmission.
48) Line 788: it is unclear from this section what is considered a bloated food vacuole - is there an area above which the FV is considered bloated? Do the authors do these measurements manually or use an addon in FIJI/ImageJ? What is the cutoff for if a FV is bloated? Please clarify. Additionally, for the representative images + rapalog for Figures 2H and 4H, it would be useful to see where the authors delineate the FV (add a white circle showing what is actually measured).
The bloated FV assay is well established (Jonscher et al., 2019; Birnbaum et al., 2020; Sabitzki et al., 2023). Although the bloating of the FV is a human judgment call, it is actually quite obvious: bloating appears as an easily spotted bulging of the FV in DIC. As also minor bloating is scored as 'bloated', it is a very conservative assay. Using an-add on to measure this is not straight forward. It is unclear how this bulging effect of the FV in DIC could be spotted by a software and due to the obviousness to human operators, potentially lengthy and complicated efforts to design appropriate machine learning options were not undertaken. The situation faced by the scorer of the assay is evident from Figure S4F-G which contains close to 50 "on rapalog" cells and close to 50 control cells, giving representative cells from all replicas of bloated FV assays with KIC12. Please note that these images shows the most complicated situation as far as bloated assays go, because the phenotype is not 100% (see Figure 3F) compared to e.g. KIC7 inactivation which leads to lack of bloating in almost all cells (see (Birnbaum et al., 2020) Figure 3E) but nevertheless the difference is still obvious. We are aware that in such situations (less than absolute inhibition) this assay scoring of "yes" or "no" is a surrogate for the actual level of inhibition and may be more subjective. This is why in this case we also did the FV size measurements (which are less dependent on human judgment) to further support this and give a better quantifiable measure. Of note, the bloated food vacuole judgments are done "blinded", i.e. the examiner does not know which sample they are looking at.
In response to this reviewer's point we now also added the FV size refinement of the assay for MyoF inactivation which is one of the cases where inhibition of bloating is not in 100% of the cells (see major comment #27). Please also note here the advantage of the rapidly acting knock sideways technique for these assays which shows the sum of effect 8 h after initiating inactivation and for which we carefully control size of the cells which shows that there is no significant growth reduction over the assay time, excluding secondary effects due to a generally reduced viability. Compared to slower acting systems suggested to have been used instead (see introductory part and significance of this review), the rapid speed of knock sideways reduces the risk of potential pleiotropic or compensatory effects due to the time needed for proteins to be depleted if the gene or mRNA is targeted instead.
The suggestion to include a ‘white circle’ (raised also as minor comment#27) is useful as an aid to see the food vacuole. However, in contrast to the Figures in (Birnbaum et al., 2020) (where we did add such a circle), we here included the DHE staining images in the figure, labelling the parasite cytosol which readily shows the FV (the FV corresponds to the region where there is no DHE staining). As this shows the position of the FV we would prefer to not obscure the DIC images with additional features to permit the reader to see the difference between bloated or non-bloated food vacuoles and keeping the image as natural as possible.
49) Line 863-864: this sentence seems to be out of place.
We thank the reviewer for pointing this out, the details of nucleus staining were moved to the correct part.
50) Line 875: the authors state that there is a light blue wedge, when the circle consists of grey and black wedges. Please revise this.
This has been corrected.
51) Line 1059-1061: it is unclear whether the individual growth curves are different clones or whether they are just the same experiment repeated? If it is the latter, then why are they not combined, as is traditionally done?
These are the individual replicates of the growth curves shown in Figure 1G of the same cell lines done on a different occasion. We always try to show as much of the primary data as possible and believe that showing individual data points from the different experiments is better than only the combined values which obscure the actual course of each experiment.
52) Line 919-924: the authors mention a blue and red line, but there is only a black line in figure 3D. Moreover, the experiment of using the LYN mislocaliser was only done for KIC12 according to the manuscript. Additionally, the y axis of the figure states relative growth day 4[%] compared to rapalog, but then on the x axis there are several days. In the text it says there is no growth defect until the second cycle, but from this graph it appears the growth defect is evident as early as 1 day post rapalog treatment. Can the authors please clarify and correct the issues pointed out.
We thank the reviewer for pointing this out, this was due to a copy & paste error in the figure legend that was now amended. We also fixed the incorrect axis label. For the last part (growth defect) please see detailed answer to Major comment#31 raising the same concern for KIC11 (in synchronous parasites the defect only takes effect once the cells reached the relevant stage whereas in asynchronous cultures there are always cells in the relevant stage that due to the rapid effect of the knock sideways already have a growth phenotype).
53) Figure 1 panel B & C: the label of the figure where the signal from MCA2Y1344STOP-GFP is shown with the DAPI signal overlayed is deceptive since it suggests that this is the signal of full length MCA2. Please change the label of this panel from MAC2/DAPI to MCA2Y1344STOP/DAPI. The same is true for Panel C for the image labeled MCA2/K13 - please change this to MCA2Y1344STOP/K13.
Done as requested.
54) Figure 2B: what stages are these parasites? Please state this in the figure. Based on the MyoF pattern, it looks like rings in the upper panel and trophs in the bottom pannel. Why were schizonts not shown?
Both are trophozoites (early trophozoite in top panel and late trophozoite in bottom panel). This is now labelled in what now is figure 1B. As stated above, schizont stages are less relevant for the topic of this manuscript and in order to prevent the manuscript from getting more disjointed and keeping it more focussed on the main topic, we decided to not include a schizont in the manuscript. Nevertheless, we included an example image below.
[Figure MyoF_p40px schizont]
55) Figure 2D&F: it is not very meaningful when growth assays are shown as a final bar after 4 days of growth. It is much more useful and informative to see a growth curve instead (as is shown in the supplementary), since it shows if the defect is apparent in the first growth cycle or later. With the way the data is currently shown, this is not apparent. I would advise the authors to switch the graph in 2F out of a combined graph of all the biological replicates growth curves for S3D - showing error bars.
While we in principle fully agree with the reviewer in showing the course of the full experiment (which is available in Figure S2E), the key here is to show the overall difference. Hence, we would like to keep this comparison of the overall effect on growth in what now is Figure 1E and G. It is part of the argument to the doubts this reviewer raises to the function of MyoF (mainly in the overall assessment and the significance statement) to show that the phenotype is actually very consistent (partial inactivation through tagging or further inactivation using knock sideways increases endocytosis phenotypes, correlating with parasite viability).
Please also note, that the growth curves upon knock sideways shown in Figure 1G, S2E are performed with asynchronous parasite cultures, which doesn’t allow us to draw direct conclusions about growth cycle effects.
Nevertheless, we now also included the suggested combined data representation in Figure S2E.
56) Figure 3: why were the calculation of FV area, parasite area and FV/parasite area only done for KIC12 and not done for MyoF? It would be interesting to see if any of these values are different for MyoF - whether the parasites are smaller in area and therefore FV smaller. Please present them Figure 2. Images should be already available and would not require further experiments to be done, only the analysis.
This now has been done (confirming our results) and is included as Figure 1J-K, S2J. This point was also raised as major comment #37, please also see detailed answer there.
57) Figure 3B: why is there no spatial association assessment for KIC11 and K13 as was done for the MCA2 and MyoF? The authors should show a pie chart showing the degree of association here as was done for the other proteins.
This is now included in Figure 2C.
58) Figure 3D: The y axis of the figure states relative growth day 4[%] compared to rapalog, but then on the x axis the experiment takes place over several days. Is this a typo in the y axis? Additionally, the authors state in line 287-290 that the growth defect upon addition of rapalog is only seen in the second cycle, but from this graph it appears the growth defect is already evident 1 day post rapalog addition. The figure legend also does not make sense for this figure since it mentions a blue and a red line, when there is only a black line present. The legend also mentions the LYN mislocaliser which was used for KIC12 not KIC 11 (see above).
We apologise for the inadequate legend and colour issues, this was amended. This point was also raised in major comment #31 and #52, please find detailed answer there.
59) Figure 3E: the colour for Control and Rapalog 4 hpi are very similar and very hard to discern. Please choose an alternative colour or add a pattern to one of the samples. The y axis is also missing a label. Is this supposed to be parasitemia (%)?
We thank the reviewer for pointing this out, the missing label is now included and the colour has been adapted to make them better distinguishable.
60) Figure 4A: the ring shown in this figure does not appear to be a ring (it is far too large and appears to have multiple nuclei?). Do the authors have any other representative images to show instead?
This is in fact a ring, but we realize that we accidentally included an incorrect size bar in the ring image of Figure 4A (now Figure 3A) (size bar for 63x objective instead of the correct one for the 100x objective), we apologise for this oversight. We don’t think this parasite has multiple nuclei, instead the Hoechst signal shows the often elongated nucleus seen in rings that can appear as two foci in Giemsa stained smears which leads to the typical diagnostic feature of P. falciparum rings in diagnostics. In order to exclude any doubts about the nuclear localization of KIC12 in rings, we here attached a panel with more examples of KIC12-2xFKBP-GFP-2xFKBP ring stage parasites.
[Figure KIC12]
61) Figure 4B: why is there no spatial association assessment for KIC12 and K13 as was done for the MCA2 and MyoF? The authors should show a pie chart showing the degree of association here as was done for the other proteins. This should be done for the different life cycle stages considering the changing localisation of KIC12.
This is now provided in Figure S4A. As suggested by the reviewer, we independently quantified the association for ring stage, early trophozoite and late trophozoites stage. As there is no KI12 signal in schizonts, we did not include a quantification for this stage.
62) Figures 4C&E: it is extremely important to show the DNA stain in both these samples considering that a portion of KIC12 is in the nucleus! Please add the DAPI signal for these figures (as for all other figures!).
Please see major comment #64 for a detailed answer why we did not include DNA staining in the imaging used to assess mislocalization upon knock-sideways.
63) Figure 4E: this figure should be presented before 4D (considering the line being presented in 4E is used in an experiment in 4D). The authors should switch the order of these two.
We see the point the reviewer is raising here, Figure 4D (now Figure 3D) also contains the data with the Lyn mislocaliser while we first talk about the NLS mislocaliser. This permits a better comparison between the two mislocaliser lines. However, first explaining the Lyn-mislocaliser and then going back to the NLS would make it rather complicated for the reader to follow the storyline and therefore we would like to keep the order as it is. We realise that this means the reader has to go back one figure part for seeing the Lyn growth data, but believe this is worth the benefit that the data is there compared to the NLS result.
64) It is unclear why in many of the fluorescence images the authors do not show the DAPI signal - particularly when colocalising with K13 and when doing the knock sideways experiments. Please add these images to the figures - I would assume they have already been taken, so would simply involved adding the images to the panel.
We did not include DNA staining (DAPI or Hoechst) for any of the images used to assess the efficacy of mislocalization, as we would prefer to keep the parasites as representative of a viable parasites in culture as possible. Hence they were imaged without DNA stain (these stains are toxic). We would like to point out that a DNA stain is not necessary, as the mislocaliser already marks the nucleus (in the case of the NLS mislocaliser), actually even somewhat more accurately, as it fills the entire nuclear space rather than only the DNA which is marked by DAPI or Hoechst.
For LYN this admittedly is not the case, there the mislocaliser marks the plasma membrane. However, we think the proper control for efficient mislocalisation is the comparison between the GFP-tagged protein of interest and the mCherry mislocaliser to show mislocalisation, as previously done in our lab (e.g. (Birnbaum et al., 2017; Jonscher et al., 2019; Birnbaum et al., 2020)).
Due to their toxicity, we also avoided nuclear staining in some other parts of the manuscript when we were of the opinion that a nucleus signal was not necessary.
65) Throughout the manuscript, there is no western blot confirming the correct size of their modified proteins. This should be provided.
We did perform Western blot analysis for both MCA2 cell lines. MCA2 is the only gene-product for which we generated a disruption for this work, and together with the severe truncation from previous work, we provided a Western blot-based confirmation of the correct size.
The MCA2 disruptions are at least partially dispensable for in vitro parasite growth, hence if degradation occurred, this might not have been noticed. In that case we considered it relevant to show that the truncations were of the expected size. The other proteins in the main figures are essential for growth. Hence, if the tagging approach would lead to unexpected changes in protein integrity (which we assume is what was intended by this concern to be assessed with a Western blot), the parasites expressing the tagged MyoF, KIC11 and KIC12 would - due to their importance for asexual blood stage development - not have been obtained. Hence, we can assume the integrity of the tagged protein is very unlikely to have been affected in a functionally relevant way.
66) None of the figures are appropriate for individuals with colour blindness, limiting their accessibility to the paper. Please change the colour schemes for all fluorescent images using magenta/green or an alternative colour combination appropriate for colourblind individuals.
We thank the reviewer for this comment. This has now been amended, individual channels of fluorescence microscopy images are now shown in greyscale, while the overlay was changed to green/magenta.
Minor Comments
1) line 29: remove 'are'.
Done.
2) Line 29: the text says "HCCU is critical for parasite survival but is poorly understood, with the K13 compartment proteins are among the few proteins so far functionally linked to this process." The sentence should be: 'HCCU is critical for parasite survival but is poorly understood, with the K13 compartment proteins among the few proteins so far functionally linked to this process."
Done.
3) line 44: remove 'the'
Done.
4) Line 48: consider mentioning here that malaria is caused by the parasite Plasmodium - otherwise the first mention of parasite in line 52 is confusing for the non-specialist reader.
Done.
5) Line 49: estimated malaria-related death and case numbers are from the 2021 WHO World malaria report. You cite the 2020 WHO World malaria report.
We now cite the newest WHO report.
6) Line 53: please insert the word 'have' between now and also.
Done.
7) Line 54: please change 'was linked' to is linked
Done
8) Line 72: I would specify that free heme is toxic to the parasite. Especially as you mention that hemozoin is nontoxic.
Sentence would be "where digestion results in the generation of free heme, toxic to the parasite, which is further converted into nontoxic hemozoin"
Done.
9) Line 90: authors should either say "in previous works" or "in a previous work"
The text has been altered to say: “ in a previous work”.
10) Line 91: "We designated these proteins as K13 interaction candidates (KICs)"
Done.
11) Line 95: please change 'rate' to number
Done.
12) Line 109: Please include a coma before (ii).
Done.
13) Line 112: as shown by Rudlaff et al in the paper you are citing, PPP8 is actually associated with the basal complex. You can say that "(ii) were either linked or had been shown to localise to the inner membrane complex (IMC) or the basal complex (PF3D7...).
Done.
14) Line 114: Protein PF3D7_1141300 is called APR1 in the manuscript but ARP1 in Supplementary Table 1. Please correct.
Done.
15) Line 131: please define SNP - this is the first use of the acronym.
Done.
16) Line 133-134: South-East Asia instead of "South Asia"
Done.
17) Line 135: please explain what TGD is - it is referred to over and over again in the manuscript without ever being explained.
We apologise for this oversight. We now explain what is meant with TGD at the suggested point of the manuscript.
18) Line 145: change 'Western blot' to western blot - only Southern blot is capitalised since it is named after an individual, while the other techniques are not.
To the best of our knowledge this issue has not been resolved, some Journals capitalize the “W” (e.g. Science), while others don’t (e.g. Nature). We would prefer to continue to capitalize the “W”, as this is consistent with the original publication from (Burnette, 1981), but if there are strong objections, we would be happy to change this____.
19) Line 152: add "the" between 'and spatial'
Done.
20) Line 158: please define SLI as selected linked integration, since it is the first use of the acronym.
Done.
21) Line 178: introduce a coma after protein. Sentence should be "Proliferation assays with the MCAY1344STOP-GFPendo parasites which express a larger portion of this protein, yet still lacking the MCA domain (Figure 1), indicated no growth ...
Done.
22) Line 195: the authors could mention that MyoF was previously called MyoC in the Birnbaum 2020 paper. I wanted to check back in the Birnbaum 2020 paper and could not find MyoF
Good point, this was done.
23) Line 200: "Expression and localisation of the fusion protein was analysed by fluorescent microscopy". Why expression was not analysed also by western Blot same as for MCA2?
Please see major comment #64 for a detailed answer.
24) Line 204: I could not find any mention of MyoF (Pf3D7_1329100) in reference 65. Please remove reference 65 if not correct. Also reference 66 looks at Plasmodium chabaudii transcriptomes so I would specify that "This expression pattern is in agreement with the transcriptional profile of its Plasmodium chabaudii orthologue"
Reference 65 (Wichers et al., 2019) provides an RNAseq transcriptome dataset for asexual blood stage development of 3D7 (originating from the same source as the 3D7 used in this study). While Ref 66 (Subudhi et al., 2020) indeed contain transcriptomic data from P. chabaudi, the authors also provide a nice 2h window RNAseq transcriptome dataset for asexual blood stage development of Plasmodium falciparum. Both datasets are therefore suitable as reference for the statement about myoF transcription pattern. Both datasets are also easily accessible and show the pattern in a graph in PlasmoDB.
25) Line 208: Please indicate a reference for P40 being a marker of the food vacuole
Done.
26) Line 220-224: The authors should consider changing to " Taken together these results show that MyoF is in foci that are mainly close to K13 and, at times, overlapping, indicating that MyoF is found in a regular close spatial association with the K13 compartment."
The suggested wording introduces "mainly" for "frequently" and likely was in part motivated by the discrepancy in location between cell lines that we hope we now could clarify to be only minor (see major point #23). We therefore think the original wording appropriately summarises the findings (line 178): “*Taken together these results show that MyoF is in foci that are frequently close or overlapping with K13, indicating that MyoF is found in a regular close spatial association with the K13 compartment and at times overlaps with that compartment.” *
27) Line 255: In Figure 2H, and subsequent figures showing bloated FV assay, I would delineate the food vacuole with dashed line as in Birnbaum et al. 2020 to help the reader understanding where the food vacuole is.
In contrast to the Figures in Birnbaum et al. 2020, we here included the DHE staining (parasite cytosol) in images of bloated FV assays which visualizes the FV. We therefore decided to avoid any further marking, to keep the image as unprocessed as possible (see also major point 48).
28) Line 265-266: Here the title says that KIC11 is a K13 compartment associated protein, but the title of Figure 3 says KIC11 is a K13 compartment protein. I noticed that you make the difference between K13 compartment protein et K13 compartment associated protein for MyoF for example which is not clearly associated with the K13 compartment. Which one is it for KIC11?
The interpretation of the reviewer is correct, we indeed graded this subconsciously based on level of overlap. Based on the newly added quantification shown in Figure 2C, we describe KIC11 now as K13 compartment protein.
29) Line 309-310: indicate a reference for your statement "which is in contrast to previously characterised essential K13 compartment proteins".
Done, we now included Birnbaum et al. 2020 as reference for this.
30) Line 377: Figure 4I, please correct 1st panel Y axis legend
Done.
31) Line 404: replace "dispensability" with dispensable
Done.
32) Line 416: can the authors provide any speculation as to why they observed these proteins as hits in the BioID experiments?
As some of these proteins were less well or less consistently enriched, they could be background of the experiment. Alternatively, some could be proteins that only transiently interact with the K13 compartment.
33) Line 451: Where the "97% of proteins containing these domains also contain an Adaptin_N domain and function in vesicle adaptor complexes as subunit a" come from. Do you have a reference?
The statement now includes references and reads (with small changes to original submission): "More than 97% of proteins containing these domains also contain an Adaptin_N (IPR002553) domain (Blum et al., 2021) and in this combination typically function in vesicle adaptor complexes as subunit α (Hirst and Robinson, 1998; Traub et al., 1999) (Figure 5D) but no such domain was detectable in KIC5."
34) Line 465-467: the same could be said for KIC4 as it also has a VHS domain.
The critical issue is the combination of domains and their position within the protein. While KIC4 also contains a VHS domain, the VHS domain in KIC4 is N-terminal, not in a central position and it is also not the first structural domain to be identified in KIC4. The similarity to adaptin domains was already described ((Birnbaum et al., 2020) and annotated in PlasmoDB) and these domains are also involved in vesicle formation and trafficking. These aspects of the statement can therefore not be extended to KIC4. With regards to VHS domains being involved in vesicle trafficking, this is already stated in line 538: «KIC4 contained an N-terminal VHS domain (IPR002014), followed by a GAT domain (IPR004152) and an Ig-like clathrin adaptor α/β/γ adaptin appendage domain (IPR008152) (Figure 5A-C, Figure S8). This is an arrangement typical for GGAs (Golgi-localised gamma ear-containing Arf-binding proteins) which are vesicle adaptors first found to function at the trans-Golgi (Dell’Angelica et al., 2000; Hirst et al., 2000).»
35) Line 477-479: Can be rephrased to "However, we found this protein as being likely dispensable for intra-erythrocytic parasite development and no colocalisation with K13 could be demonstrated, suggesting a limited role for PF3D7_1365800 in endocytosis. Or something like that. Makes it clearer.
We rephrased this sentence and it now reads (line 592): “However, we found this protein as being likely dispensable for intra-erythrocytic parasite development and no colocalisation with K13 was observed, suggesting PF3D7_1365800 is not needed for endocytosis“.
36) Line 535: Have AP-2a or AP-2b been shown to be at the K13 compartment?
AP2m is at the K13 compartment (Birnbaum et al., 2020). Adaptor complexes are heterotetramers and their subunits do not typically function on their own and this is conserved across evolutionarily distant organisms. In agreement that this is also the case in P. falciparum, Henrici et al. (Henrici et al., 2020a) showed that both, AP-2a and AP-2b, were present in an AP2µ Co-IP, indicating that the AP2 complex consist of the ‘classical’ subunits in P. falciparum. Therefore, the presence of all subunits at the K13 compartment is very likely, although this has only been experimentally confirmed for AP2µ. Of note, for Toxoplasma gondii the presence of AP-2a and AP-2b at the micropore has been experimentally confirmed (Wan et al., 2023; Koreny et al., 2023) and interaction suggested by presence in the same IP as DRPC (Heredero-Bermejo et al., 2019).
37) Line 569: reference 43 is wrong
We thanks the reviewer for pointing this out – we removed Ref 43.
38) Line 746: typo "ot" instead of or.
Changed.
39) Line 801: method for Domain Identification using AlphaFold specify that RMSDs of under 5Å over more than 60 amino acids are listed in the results. However, there is a typo in Figure 5B for KIC5 where it says "RMSD 4.0 Å over 8 aa". Please correct.
Done. In addition, we have now applied a more stringent cut-off of 4Å over more than 60 amino acids to ensure a higher reliability of our hits. This decision was based on results from our preprint (Behrens and Spielmann, 2023). Because of this the phosphatase domain in KIC12 is no longer included in this manuscript and accordingly the following sentence has been deleted. “In KIC12 we identified a potential purple acid phosphatase (PAP) domain. However, with the high RMSD of 4.9 Å, the domain might also be a divergent similar fold, such as a C2 domain, which targets proteins to membranes.”
40) Line 856: In Figure 1E, please use the same Y axis legend as in Figure 2D "relative growth at day 4 [%] compared with 3D7"
Done.
41) Figure S1: Some PCR gels check for integration are presented as 5', 3' and ori whereas other gels are presented as ori, 5' and 3'. This is confusing.
We agree that ideally the order of sample loading should be consistent and we apologise for this. The explanation for this is that these gels were run by different people at different times before we were able to better standardize the loading scheme. However, in the interest of not unnecessarily using resources for something that has a similar meaning, we would prefer not to repeat these PCRs and re-run them only for consistency reasons (as the conclusion is not affected by the different loading schemes).
42) Figure S1: Why was the expression of only MCA2 was verified by Western blot? What about the other proteins?
See response to major comment 56.
43) Line 493: Considering KIC11 was not involved in HCCU or ART resistance it might be worth mentioning in this section that it is of note that there are no domains detected that would be involved in endocytosis.
We agree that this is the case, however it is also the case for all other proteins that either are not involved in endocytosis and/or lowered susceptibility to ART. We therefore now added a summary statement addressing this in line 602: “In contrast, the K13 compartment proteins where no role in ART resistance (based on RSA) or endocytosis was detected, KIC1, KIC2, KIC6, KIC8, KIC9 and KIC11, do not contain such domains (Figure 5E).” We did not add this at the suggested part of the manuscript as at that point the domain search results are not yet introduced and doing this each time for all the individual proteins would disconnect the flow of the manuscript.
44) Line 503-506: is it wise to generate more drugs that target a pathway that is already highly susceptible to mutations? The authors should add a statement explaining how this might be avoided.
The only protein for which mutations do not have a large fitness cost is K13 (see also our preprint on fitness cost of ubp1 mutation (Behrens et al., 2023) and even with K13 the level of resistance seems to be limited by amino acid deprivation when endocytosis is reduced (Mesén-Ramírez et al., 2021). We therefore do not think that this pathway is particularly prone for mutations. Further, the number of commercial drugs targeting the "endproduct" of endocytosis (hemoglobin digestion and detoxification of heme) highlight it as the most prominent vulnerability for drug-based intervention if we go by number of commercially available drugs acting on things associated with a single process.
45) Throughout, scale bars are stated in the figure legends at the end of the legend. This is a slightly confusing format. The authors should consider stating the scale bar for each sub-legend where a fluorescence image is taken.
Done.
** Referees cross-commenting**
After reading reviewer 2 and 3's comments, I think there are significant overlaps in the key points raised in terms of questions about fusion proteins and their potential partial mis-localisation, better descripton of results and target selection. Overall I think we agree that the work has potential, but in its current form does not represent a major advance. It would be immensely helpful if the manuscript would be carefully edited for a better flow and linear description of results.
We now rearranged the manuscript for better flow but would like to highlight that the many requests for smaller experimental issues (and "better description of results") worked somewhat in the opposite way of a more linear description. We hope the rearranged version acceptably balances these two issues. The issues raised in regards to target selection and potential partial mis-localisation are addressed in our responses mainly to this reviewer. Please also see comments on systems used at the end of the rebuttal.
Reviewer #1 (Significance (Required)):
The authors set out to test whether other proteins that are in the vicinity of K13 are involved in mediating ART resistance and endocytosis. This is an interesting question. However, other than MCA2 which was already known to be involved in mediating ART resistance (and was not tested for its involvement in endocytosis), none of their candidate proteins seem to be involved in mediating both these functions. The authors show that the other proteins tested appear important for parasite growth, with KIC12 and MyoF involved in mediating endocytosis. While these findings are novel, the KS approach used by the authors casts some doubt over the findings, and would mean that these findings would have to be re-tested with a more reliable approach, such as the GlmS system or generating a conditional knockout using the DiCre system. Despite not advancing our understanding of ART resistance, or identifying further players involved in this process, this manuscripts provides two candidates that are involved in mediating endocytosis and a further candidate that appears to be important for parasite growth. Further work on these proteins will be required to understand their exact roles. As stated above, there is currently limited interest for these results (limited to researchers working on endocytosis in apicomplexan parasites and possibly the wider endocytosis field from an evolutionary perspective), however with further work, this could increase the impact and interest of this work substantially.
The authors do not describe any novel methods/approaches within this work.
In the significance statement the reviewer indicates that other systems would have been more reliable for the work here. This is addressed in our response above and in a detailed considerations on the properties of conditional inactivation systems at the end of the rebuttal. The systems used in this work were not only chosen because they permit rapid targeting of many different proteins, but because they have merits that are beneficial for our assays. In fact many of the functional assays in this manuscript are difficult or impossible to carry with the suggested conditional inactivation systems (please note that we have extensive experience with the systems considered preferable:
-
DiCre (Birnbaum et al., 2017; Mesén-Ramírez et al., 2019; Mesén-Ramírez et al., 2021; Wichers et al., 2022; Kimmel et al., 2023)
-
glmS (Wichers et al., 2021c; Wichers et al., 2021a; Wichers et al., 2022; Wichers-Misterek et al., 2023)).
Reviewer #2 (Evidence, reproducibility and clarity (Required)):
In a previous publication the Spielmann lab identified the molecular mechanism of ART resistance in P. falciparum by connecting reduced levels of the protein K13 to decreased endocytosis (uptake of hemoglobin from the RBC cytosol), which results in reduced ART susceptibility. Using quantitative BioID the authors further identified proteins belonging to a K13 compartment, highlighting an unusual endocytosis mechanism.
In the present manuscript the authors follow up on this work and closely examine ten more proteins of the K13/Eps15-related "proxiome". They successfully link MCA2 to ART resistance in vitro, while the proteins MyoF and KIC12 are involved in endocytosis but do not confer in vitro ART resistance when impaired. They further characterize one candidate (KIC11) that partially colocalizes with K13 in trophozoites but to a lesser degree in schizonts. Growth assays suggest an important function for KIC11 in late stages of the intraerythrocytic developmental cycle. Five analyzed proteins however do not colocalize with the K13 compartment, while a sixth was refractory to endogenous tagging.
Using AlphaFold predictions of the KIC protein structures the author identify domains in most constituents of the K13 compartment, highlighting vesicle trafficking-related features that were not identified on primary sequence level before.
The combination of functional data together with structure predictions leads them to propose a refinement of the K13 compartment as being divided into proteins participating in endocytosis and proteins that have an unknown function.
We thank the reviewer for the assessment of the manuscript and the constructive comments.
Major comments:
1) -Table 1 is missing
We apologise for this mistake; Table 1 is now included.
2) -Lines 117-123: Given the total list of uncharacterized candidates encompasses 13 proteins, can the author gives the reason why only the top 10 and not all 13 were characterized in this study?
A similar point has been raised by Reviewer 1 in major comment #12, please see our response there for an explanation why we chose which targets.
3) -Line 174: 20% of observed MCA2 foci show no overlap with K13 and 21% only partially overlap, can the author confirm that the observed MCA2 foci in schizonts are the ones that co-localize with K13. (Addition of a schizont stage image in Fig 1C would be sufficient).
We now extended Figure 4C with images of MCA2-Y1344STOP-GFP+mCherryK13 parasites covering the schizont and merozoite stage, showing that the majority of the MCA2 foci in schizonts are also mCherry-K13 positive.
4) -The localization and observed phenotype of KIC11 is interesting but unfortunately the authors do not explore it further. Does KIC11 localize with markers of e.g. the secretory organelles (micronemes or rhoptries) in schizonts and could therefore be involved in RBC invasion?
While we intended to focus mainly on the endocytosis aspect of these proteins, we see the reviewer's point and now generated new cell lines enabling assessment of spatial association of KIC11 with markers for rhoptry (ARO), micronemes (AMA1), and inner membrane complex (IMC1c). This revealed that the KIC11-GFP signal in schizonts does not overlap with apical organelle markers and the signal does not resemble a typical apical localization. In addition, we assessed all three organelle markers after inactivating KIC11 by knock sideways which showed that KIC11 inactivation has no apparent effect on the appearance of these markers, suggesting no major alterations in schizont morphology in respect to apical markers. These results are now presented as Figure S3A and in line 304 of the results.
5) Can the author distinguish if KIC11 is involved in RBC invasion or in establishment of the ring-stage parasite?
In order to look into this, we performed egress/invasion assays, quantifying schizont and ring stage parasites in tightly synchronized parasites at two different time points (pre-egress: 38-42 hpi & post-egress: 46-50 hpi). This revealed a significant decrease in newly formed ring stage parasite per ruptured schizont in parasites with inactivated KIC11, while the egress efficacy remained unaffected. This indicated an invasion or very early ring stage development defect (new Figure 2H, Figure S3G). To further determine at which point exactly the phenotype occurs (ie during invasion or early after invasion) would require extensive experimentation that goes beyond the scope of this study (e.g. invasion assays using video microscopy with a representative number of parasites or sophisticated flow based quantification assays). We hope by excluding egress and gross changes of apical organelles as well as no indication for similar number of early rings (indicating it is invasion or a very early ring-establishment phenotype) will sufficiently narrow down the phenotype for labs interested in invasion to more definitely answer this question.
Minor comments:
1) Table S1: Please add the criterion for the order of proteins (abundance in "proxiome"?) in the table as a separate column. I would also suggest adding a new column that highlights the 10 proteins investigated in this study as I found the color-coding slightly confusing.
Done as suggested: we now include the “average log2 Ratio normalized Kelch13” values from the four DiQ-BioID experiments performed with K13 in (Birnbaum et al., 2020), as well as the suggested column to highlight the investigated proteins. Please also see reviewer 1 major point # 12 for additional information on the selection criteria and how this was added to the manuscript.
2) -154-155: There is a discrepancy between the text and Fig1C regarding the % of partial overlapping and non-overlapping foci.
We thank the reviewer for pointing this out, this was corrected.
3) -The y-axis label is missing in Fig 3E
Done.
4) -Fig 4I left graph, the superscript 2 is missing in μm2
We thank the reviewer for pointing this out, this is now changed.
5) -Did the author colocalize KIC11 in schizonts with other proteins found in the K13 compartment group of proteins not involved in endocytosis/ART resistance? This may help to further subgroup these proteins.
This is an interesting point but would actually be technically challenging to do. For this we would need to generate a KIC11endo parasite line for each of these KICs and then do co-localisation in schizonts. However, the outcome of this likely would not be very clear. The reason for this is as follows. There are foci of KIC11 that do overlap with K13 in schizonts. One can expect that these foci show KIC11 at the K13 compartment and that the other KICs would overlap with KIC11 in these K13 foci in schizonts. Hence, we would also need to see K13 to find the non-K13 compartment KIC11 foci and see if these contained the KIC of interest. This is technically challenging because it would mean we would need a third fluorescent protein which is not that trivial to do. Due to the difficulty to do this and the large amount of work involved and the already considerable amount of data in this manuscript, we believe this will be better suited for a different study.
6) -As a general comment: to make the beautiful IFAs more accessible to a broader readership, I would encourage the authors to switch the color-coding to green/magenta/blue or an equivalent color system or add grayscale images.
This was done as suggested, all fluorescence images are now provided as greyscale images and the overlays are shown in magenta/green.
Reviewer #2 (Significance (Required)):
Characterizing the molecular components involved in Plasmodium endocytosis will not only reveal interesting biology in these highly adapted parasites, but will more importantly lead to a better understanding and potentially open new avenues for intervention of ART resistance. The here presented manuscript is a carefully executed follow-up on previous work done in Dr. Spielmann's lab focusing on the K13 compartment. The authors use established assays to characterize novel components and reveal three new players in endocytosis with one mediating ART resistance in vitro. The proposition that parts of the K13 compartment have a function other than endocytosis is interesting, but will have to await more data from future studies. Taken together this manuscript adds significantly to our understanding of endocytosis in P. falciparum.
This work is of interest for cell and molecular biologists working on Apicomplexa, but especially for the Plasmodium community.
We thank the reviewer for this positive assessment.
I am a cell and molecular biologist working on Toxoplasma gondii
Reviewer #3 (Evidence, reproducibility and clarity (Required)):
Summary: The authors characterized 4 proteins from P. falciparum via cellular (co-)localization, endocytosis, parasite growth, and artemisinin resistance assays. These proteins have been identified as candidates for Kelch13 compartment and a possible role in endocytosis in their previously work with quantitative BioID for potential proximity to K13 and Eps15 (Birnbaum et al. 2020). In the current work, additional 6 proteins were not confirmed as being associated to the K13 compartment. This experimental work was complemented by an in-silico analysis of protein domains based on AlphaFold algorithm. For this protein structure evaluation all proteins were chosen, which were experimentally confirmed to be linked to the K13 compartment in the current publication and previous work. With the work 3 novel proteins linked to artemisinin resistance or endocytosis could be functionally described (KIC12, MCA2, and MyoF) and a number of hypotheses were generated.
We thank the reviewer for the assessment of the manuscript and the constructive comments.
Major comments:
The quality of the presented work is solid, the experimental design is adequate, and methods are presented clearly. The publication contains a lot of results both presented in text and in the figures and it is not always straight forward for the reader to follow the descriptions due to many details presented and a lack of context for some of these experiments.
We thank the reviewer for this overall positive assessment.
We now reordered the results section in an attempt to increase the flow of the manuscript. We also made changes to improve the context for the results. Given the further (very valid) requests for data on schizonts and invasion, there was an increased danger for a less linear manuscript that we hope to have acceptably managed with the re-arrange.
Specific suggestions for consideration by the authors to improve the manuscript. Abstract: 1) R 31: Mention how the 4 proteins were identified as candidates, you need to refer to previous work to clarify this
To clarify this the sentence was changed to (line 31): "Here we further defined the composition of the K13 compartment by analysing more hits from a previous BioID, showing that MyoF and MCA2 as well as Kelch13 interaction candidate (KIC) 11 and 12 are found at this site."
2) R38: "Second group of proteins" is confusing - different from the 4 mentioned above? Significance to endocytosis unclear. Please unify terminology in the manuscript, see also comment below on proxiome.
We changed the wording to clarify the group issue in the abstract as follows line 34: "Functional analyses, tests for ART susceptibility as well as comparisons of structural similarities using AlphaFold2 predictions of these and previously identified proteins showed that canonical vesicle trafficking and endocytosis domains were frequent in proteins involved in resistance or endocytosis (or both), comprising one group of K13 compartment proteins, While this strengthened the link of the K13 compartment to endocytosis, many proteins of this group showed unusual domain combinations and large parasite-specific regions, indicating a high level of taxon-specific adaptation of this process. Another group of K13 compartment proteins did not influence endocytosis or ART susceptibility and lacked detectable vesicle trafficking domains. We here identified the first protein of this group that is important for asexual blood stage development and showed that it likely is involved in invasion.”
3) Abstract can only be understood after reading the full publication
We attempted to amend this by expanding the abstract, particularly the changes highlighted in the previous two points.
Results: 4) Table 1 is missing from the submitted materials
We apologise for this mistake. Table 1 is now included.
5) Consider to shorten and stratify the result section to focus on the significant data
We rearranged the results in an attempt to streamline this section and are now starting with MyoF in the revised manuscript. However, as highlighted by the requests from reviewer 1, many details need to be available to support our conclusions. For instance the fact that GFP-tagging partially inactivated MyoF asked for further data to support our conclusion (HA-tagged version, showing that the location of the GFP-tagged version was consistent with the HA-tagged version, showing to what extent the different constructs affected growth and correlated with number of vesicles and bloating, see new figure 1M) or that KIC12 has two locations. Overall, we are therefore hesitant to remove data or description from the result part.
6) Unclear how the localization and functionalization assays might be impaired by the fusion proteins Significance of ART resistance assay is not clear, in presence of strong growth effects due to inactivation or truncation of genes/proteins
As indicated also in the example given in the previous point (this reviewer #5), the use of different cell lines (GFP-tagged live cells and small epitope tag in IFA) for targets with an indication for an effect of the tagging confirm that the location we assigned is reasonable. In the case of MyoF, the HA-tagged line, the partial inactivation due to GFP and the further inactivation in the GFP-tagged line by knock sideways show plausible increase of phenotypes (vesicle accumulation and bloated FV assays). Thereby the GFP-tagged line can be seen as a partial inactivation line that further supports our conclusions and overall this paints a consistent picture of the function of this protein in endocytosis (see new Figure 1M better illustrating this). Please note that the difference in location shown by this line compared to the HA-tagged proteins is only small (see also reviewer 1 major point 23ff). See also general discussion on tags at the end of this rebuttal.
Significance of ART resistance assay: The ‘ART resistance assay’ is done comparing +/- ART (DHA) in identical parasites (originating from the same culture and the same condition). Hence, any growth effects are cancelled out and effects in reducing ART susceptibility would - if at all - be underestimated (see more detailed response to point 28, reviewer 1 and controls in Birnbaum et al., 2020 where we tested an unrelated essential protein, unrelated chemical insult and rapalog on 3D7 and did not detect any effect on RSA survival).
MCA 7) Stratify results, order by significance of findings, it appears to be described in chronological order, improve readability/flow, eg ART resistance if mentioned in r138, but only reported in r183ff
We attempted to stratify, but then the reason for generating the partial MCA2 disruption parasite line becomes very arbitrary and would leave the reader wondering why we at all truncated the protein at two thirds of the protein. Hence, we do not see a way around this chronological reporting. However, this part is now not at the start of the experimental results section anymore, possibly making it overall a bit more palatable.
MyoF 8) R195 to 197 - consider moving to discussion as it is distracting here
This was shortened and additional information (asked for by reviewer 1, major point 22) to clarify that MyoF was previously called MyoC, was added (line 147): “The presence of MyosinF (MyoF; PF3D7_1329100 previously also MyoC), in the K13 proxiome could indicate an involvement of actin/myosin in endocytosis in malaria parasites. "
9) Term proxiome is introduced above, but not used in result section - suggest to unify language, eg r195 uses "K13 compartment DiQ-BioIDs" instead, which is not very convenient for the reader
We carefully reviewed this and made this more consistent.
10) What is the enrichment factor? Please provide for this and the following proteins, eg in Table 1
The enrichment factor is log2 enrichment over control and this is now provided in table S1 (see also detailed answer for Reviewer 1 major point 12).
11) R225 to 243 - overall significance of the growth experiments with mislocaliser is not clear, consider removing from manuscript or explain relevance more clearly
See also point 28, reviewer 1: This experiment is actually quite important. It shows that if we conditionally inactivate the GFP-tagged MyoF, the growth is further reduced, as stated in line 208. It might have been confusing that the mislocalisation is only partial, but this is equivalent to a partial knock down and hence is useful. This becomes even more relevant with the specific assays following in the next paragraph: while the tagging of MyoF already resulted in vesicles, conditional inactivation with KS generated even more vesicles, showing that the same phenotype was rapidly increased when MyoF was further inactivated by a different means and this also correlated with growth. Hence, this is actually a very consistent phenotype that despite some shortcomings of the tools available to analyse this protein (due to the partial inactivation by the GFP tag) in our eyes looks very convincing. We now added a graph showing the correlation of growth and phenotypes to illustrate this (Figure 1L).
We also tried to make this clearer by changing line 200 to: “Hence, conditional inactivation of MyoF further reduced growth despite the fact that the tag on MyoF already led to a substantial growth defect, indicating an important role for MyoF during asexual blood stage development.” And line 208 to:“ This was even more pronounced upon conditional inactivation of MyoF by KS (Figure 1H), suggesting this is due to a reduced function of MyoF.”
12) KIC11/KIC12 Enrichment factor?
The enrichment (’average log2 Ratio normalized Kelch13 from Birnbaum et al. 2020’) is 1.65 for KIC11 and 1.32 for KIC12, which is now also explicitly shown in column D of Table S1.
** Referees cross-commenting**
I would like to applaud reviewer #1 for a great, very thorough review and lots of detailed suggestions. I agree with the conclusions mentioned in the significance evaluation from reviewer #1 and #2: the work presented does not contain novel methods and the scope is rather narrow with the current results. (I am working on clinical studies with novel antimalarial agents)
Reviewer #3 (Significance (Required)):
On the one hand side, the authors have wrapped up some of the remaining protein candidates of the K13 compartment and could verify 4 of 10 proteins. The work is of interest for the scientific community working on endocytosis and malaria drug resistance mechanisms. Overall, the conclusions and findings from the previous work, Birnbaum et al. 2020, could be confirmed and extended mainly using the methods previously described. On the other hand, the authors made use of progress in protein structure predictions and identified domains linking the K13 compartment proteins to putative functions. The overlaid protein folds of the newly identified domains in figure 5 look convincing, but I can't comment on the technical details or cut-off used for this in-silico analysis.
Extended general remarks on the systems used for this work:
Mainly reviewer 1 suggest (in the general comments and the significance statement) that other systems would have been better suited to use for this work, namely glmS and diCre and also has concerns about the large tag which is seconded by a comment of reviewer 3. In light of this we here provide some extended considerations on the properties for conditional systems and tagging in regards to the goals of this work.
We would like to point out that we do have experience with the systems considered better-suited by the reviewer (one of the first authors has extensively used glmS (Wichers et al., 2021c; Wichers et al., 2021a; Wichers et al., 2022; Wichers-Misterek et al., 2023) and our lab was one of the first to adopt the diCre system in P. falciparum parasites and we regularly us it (Birnbaum et al., 2017; Mesén-Ramírez et al., 2019; Kimmel et al., 2023)). Clearly, these methods have a lot of strengths but there are a number of issues to be considered for the assays we use in this work (see the next section on conditional inactivation systems). In a nutshell, we believe diCre would give a more reliable readout of the absolute level of "essentiality" (i.e. importance for growth) but is unsuitable or at least difficult to use for the assays that reveal the function of our interest in this work. GlmS basically combines the drawbacks of diCre and knock sideways and hence for most targets is not expected to give a better readout of level of "essentiality" but is similarly difficult to use for our specific assays. The fact that both of these systems are possible to use without adding a tag to the target may be an advantage but without tag one loses some very important features that can be critical to understand the outcome with a given system (see considerations on the tag further below).
Conditional inactivation systems:
- __ speed of inactivation:__ glms acts on mRNA and diCre on the gene level, which makes them slower than techniques acting directly on the protein such as DD or KS. With diCre, mRNA and protein is still left, even if the gene is very rapidly excised. For instance for Kelch13 it takes 3-4 days after excising the gene until protein levels have waned enough that this manifests in a reduced growth (Birnbaum et al., 2017). While in some instances diCre permits same cycle analyses if the protein has a very rapid turn-over (e.g. Rab5a, (Birnbaum et al., 2017)), control in a few hours is still difficult. For vesicle accumulation and bloated food vacuole assays, which are done over comparably short time frames and with specific stages, it is rather challenging to hit the correct time of induction to have all the cells at the correct stage with suitably (and uniformly, ie all cells) sufficiently reduced target protein levels during the assay time. Slow acting systems are also more prone to secondary effects. The more immediate the inactivation, the closer it is to the core of the affected function. With vesicle trafficking processes this is particularly relevant as all vesicle trafficking in a cell is interconnected and there are always recycling pathways that maintain the membrane and protein homeostasis of individual compartments. Particularly for endocytosis there seem to be compensatory capacities at least in other organisms (see e.g. (Chen and Schmid, 2020)). One reason why knock sideways was developed is that it permitted to avoid compensatory changes when vesicle adaptors are inactivated (Robinson et al., 2010).
The comparably short time frame for malaria parasites to go through different stages during blood stage development also is an issue relevant for inactivation speed. The advantage of speed and the danger of obscured phenotypes is highlighted by our work on VPS45 which showed that in trophozoites this protein is involved in the transport of hemoglobin to the FV whereas in late stages it also has a role in secretory processes. Both of these functions we were able to specifically assess in the same growth cycle using KS to rapidly inactivate the protein (Bisio et al., 2020) but with a slower system would have been more complicated to dissect.
Speed of effect with glmS: unless the KS does not work well, glmS is slower acting than KS (it does not target the already synthesised protein which can remain in the cell) and also often suffers from only partial inactivation, hence the benefit of using it here is unclear. The option to have an untagged protein is a plus, however it also is a minus, as assessing efficiency (particularly in live cells e.g. for bloated assays etc a fluorescent tag is the only direct option to assess inactivation of target) is critical to ensure the phenotype manifests at the stage of interest.
lethality/absolute phenotypic effects are detrimental to some assays to study the functions we are interested in for this work: no RSA can be conducted, if the gene is lost and the parasites die. Again, with diCre, one could attempt to hit the point when the parasites have lost sufficient amounts of the target protein when they are placed under ART but then the parasites need to continue growing for ~3 days, which is not possible if the cKO is lethal except for very slowly turning over proteins. However, in that latter case, the parasites likely still had full functionality of the target protein at the beginning of the RSA, when the drug pulse happens and there would be no effect. Knock sideways solves these problems by permitting knock sideways inactivation only under ART (or with a few hours pre-incubation depending on the inactivation speed) to not yet affect growth in a severe manner but inhibiting the process the protein is involved in. It may be possible to use glmS for RSAs, but the slow speed would complicate it (it would not permit control of target protein levels in a matter of a few hours to inactivate the target protein and then re-install it).
None-absolute inactivation is also a strength for some functional assays. While we really like using diCre, in the case of EXP1 it made it necessary to complement the exp1 cKO parasites with low levels of EXP1 to be able to do functional assays without killing the parasites (Mesén-Ramírez et al., 2019; Mesén-Ramírez et al., 2021). While the lethality issue does not apply to glmS (like knock sideways, it also can be tuned), it is unclear what would be gained over knock sideways. Knockdown levels with glmS vary from gene to gene and cannot be predicted, it is in most cases considerably slower than KS, it requires glucosamine which becomes toxic at higher concentrations and might introduce off target effects and tracking protein levels during the assay would equally need GFP tagging.
Integration of properties of conditional systems
Given the above discussed properties, several factors have to be considered to be able to use a system for a given assay. Stage-specific transcription is one example. For diCre a protein not expressed in e.g. rings permits to remove the gene and the protein is never made in that parasite development cycle. We exploited this for instance for two proteins only expressed from the trophozoite stage onwards (Kimmel et al., 2023). However, if lethal (absolute effect problem), this also means one can also only see the phenotype on onset of expression of the target (e.g. if in mitosis, the first nuclear division in case the protein is absolutely essential for the process). This is just one example of such issues. Expression timing, turnover of the protein and homogeneity of stage-specific loss of protein will all influence how clearly the phenotype can be determined. All this will decide the exact time of loss/inactivation of the target protein to levels generating a phenotype and ideally therefore can be monitored during an assay (see considerations on tagging).
For these reasons vesicle accumulation or bloated food vacuole assays are difficult with slow systems as ideally the target should rapidly be inactivated at the trophozoite stage and the result monitored before the cells have moved to the schizont stage. For this a well responding knock sideways is ideal as the protein can be rapidly taken away (sometimes within seconds) to visualise the immediate, direct effect in the cell.
As shown for KIC11, there is also no disadvantage of using KS for proteins with other assays or proteins that result in different phenotypes. It permits stage-specific same cycle inactivation without having to worry about the turnover of mRNA and protein (Fig. 2F,G). Thus, besides the advantages of knock sideways for endocytosis related assays and RSAs, we also see no disadvantage of using knock sideways for the functional study of KIC11 which has a role other than endocytosis. KS also permits to specifically target the K13 pool of KIC12, something impossible or very difficult to do with other systems. Hence, we are of the opinion that the system for inactivation was adequate for most of the proteins analysed in this manuscript.
Large tag: we agree that GFP-tagging can be a disadvantage but in our opinion its benefits often outweigh the drawbacks because it permits easy and immediate (on individual cell level, if need be) monitoring of the presence/location of the target protein (e.g. after KS, but given the discrepancy of the timing between gene excision and protein loss, it might be even more important for techniques such as diCre). No fixing/permeabilisation (prone to artifacts, prevents immediate view of cells) to detect a target with specific antibodies or via a small tag is needed with GFP. Similarly, the use of Western blots to do this is time consuming and impractical if monitoring of left-over protein in the course of an assay such as a bloated food vacuole assay is needed.
In many cases, adding GFP has no negative effect. In addition, if the bulky folded structure of GFP is tolerated, it usually also tolerates the 2 to 4 12kDa FKBP domains in our standard tag. We also typically add a linker. This approach has worked for a large number of different proteins, including many essential ones for which we would not otherwise have obtained the integration cell lines (Birnbaum et al., 2017; Jonscher et al., 2019; Hoeijmakers et al., 2019; Birnbaum et al., 2020; Kimmel et al., 2023; Sabitzki et al., 2023). Hence, whenever a cell line is obtained with it, this tag in most cases is not a disadvantage. Admittedly an exception in this is MyoF and to some extent maybe MCA2 (we would like to stress that in the case of MCA2 the reason for not being able to obtain the full length tagged cell line is unclear: the protein can be severely truncated to less than 3% of its amino acid sequence and a GFP-tag is tolerated on the version with 2/3s of the protein left, which gives no good reason why the full length was not obtained; a potential reason could be a dominant negative effect). However, we obtained the full length with a small tag detected by IFA for both, MyoF and MCA2 and the location of these agreed well with the GFP tagged versions, indicating that the GFP-tagged versions are useful to show the location of these proteins in live cells.
There are also tricks to attempt monitoring the effect of e.g. diCre without tagging the target. For instance, if a fluorescent protein is connected to excision without actually being fused to the target (ie excision of the gene leads to its expression of e.g. GFP), which would avoid adding a tag to the target itself. However, the problem with this is that expression of GFP does only show excision, but mRNA producing the target protein and left over target protein may still be there in the cell. All in all, the GFP-tag on the target, while with some drawbacks, is still our preferred method to control to monitor the target protein in the cell (in principle permitting quantification of ablation efficiency on the individual cell level).
Conclusion on these considerations for this manuscript
Based on these considerations we do not see the immediate benefit of changing the system for the conclusions drawn from this study and are unsure if they are indeed better suited for this work as suggested. While a more exact readout of "essentiality" might be possible with the diCre system we are of the opinion this is less important than learning the function of a protein which - as outlined above - we believe to be considerably more difficult with diCre and even more so with glmS considering our target functions. The same applies to target specific cellular pools of a protein as done here for KIC12. Clearly MyoF is one example where the employed systems shows limitations, but with the new Figure part showing consistency in phenotype with degree of inactivation (importantly with two different forms of inactivation) and the clarification that the location of the GFP-tagged and HA-tagged versions are actually quite similar in location, we do not think employing an extra system is warranted for the conclusions of this work. Admittedly, the apparent lack of need in ring stags might give an opening to attack MyoF using diCre (by excision before its major expression peak), but depending on lethality this might preclude extended analyses (possibly vesicle assays, for sure not RSAs).
In the end the question is, if our approach provides the function of target analysed in this work and based on the data in our manuscript and the arguments in the rebuttal, we are reasonably confident that this is the case. It is not very likely the other mentioned techniques would result in a different conclusion on the function of the here studied proteins. In fact, we expect other commonly used techniques to be less suitable for the key assays in this work.
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Wittgenstein, Luhmann, Conrad Gessner, Leibniz, Linnaeus and Walter Benjamin are some I can think of off the top of my head.
reply to u/muhlfriedl by way of reply to u/chounosumuheya at https://www.reddit.com/r/Zettelkasten/comments/13s6dsg/comment/jlpt8ai/?utm_source=reddit&utm_medium=web2x&context=3
Examples of zettelkasten users
S.D. Goitein, Beatrice Webb, Ludwig Wittgenstein, Harold Innis, Victor Margolin, Eminem, Aby Warburg, Antonin Sertillanges, Jacques Barzun, C. Wright Mills, Gotthard Deutsch, Roland Barthes, Umberto Eco, Vladimir Nabokov, Gerald Weinberg, Michael Ende, Twyla Tharp, Hans Blumenberg, Keith Thomas, Arno Schmidt, Mario Bunge, Sönke Ahrens, Dan Allosso for a few more. If you go with those who used commonplace books and waste books, which are notebook-based instead of index card-based, there are thousands upon thousands more.
Historically the easier question might be: what creators didn't use one of these systems and was successful?!? The broad outlines of these methods go back much, much farther than Niklas Luhmann. These patterns are not new...
Personally, I've used my own slip box to write large portions of the articles on my website. I also queried it to compile this reply.
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Note: This rebuttal was posted by the corresponding author to Review Commons. Content has not been altered except for formatting.
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Reply to the reviewers
We thank the reviewers for their comments and constructive suggestions to improve the manuscript. We are encouraged to see that both reviewers acknowledge how the results from our manuscript uses state-of-art technologies to advance molecular underpinnings of centriole length, integrity and function regulation. Both reviewers also highlighted that the manuscript is well laid out and presents clear, rigorous, and convincing data. Reviewer#1 described our manuscript of highest experimental quality and broad interest to the field of centrosome and cell biology form a basic research and genetics/clinical point of view. Here, we explain the revisions, additional experimentations and analyses planned to address the points raised by the referees. We will perform most of the experimentations and corrections requested by the reviewers. We have already made several revisions and are currently working on additional experiments.
Our responses to each reviewer comment in bold are listed below. References mentioned here are listed in the references section included at the of this document.
Reviewer #1 (Evidence, reproducibility and clarity (Required)):
Summary: __In this manuscript, Arslanhan and colleagues use proximity proteomics to identify CCDC15 as a new centriolar protein that co-localizes and interacts with known inner scaffold proteins in cell culture-based systems. Functional characterization using state-of-the-art expansion microscopy techniques reveals defects in centriole length and integrity. The authors further reveal intriguing aberrations in the recruitment of other centriole inner scaffold proteins, such as POC1B and the SFI1/centrin complex, in CCDC15-deficient cells, and observe defects in primary cilia. __
We thank the reviewer for the accurate summary of the major conclusions of our manuscript.
Major points:
1) The authors present a high-quality manuscript that identifies a novel centriolar protein by elegantly revealing and comparing the proximity proteomes of two known centriolar proteins, which represents an important component for the maintenance of centrioles.
We thank the reviewer for highlighting that our manuscript is of high quality and presents important advances for the field.
__2) Data are often presented from two independent experiments (n = 2), which is nice, but also the minimum for experiments in biology. It is strongly recommended to perform at least three independent experiments. __
We agree with the reviewer that analysis of data form three experimental replicates is ideal for statistical analysis. We performed three replicates for the majority of experiments in the manuscript. However, as the reviewer pointed out, we included analysis from two experiments for the following figures:
- Fig. 4H: quantification of CCDC15 total cellular levels throughout the cell cycle by western blotting
- Fig. 5A: CCDC15-positive centrioles in control and CCDC15 siRNA-transfected cells
- Fig. 6B: % centriolar coverage of POC5, FAM161A, POC1B and Centrin-2 in control and CCDC15 siRNA-transfected cells
- Fig. 6C, 6E: Centrin-2 or SFI1-positive centrioles in control and CCDC15 siRNA-transfected cells
- Fig. 6J, K: normalized tubulin length and percentage of defective centrioles in cells depleted for CCDC15 or co-depleted for CCDC15 and POC1B
- Fig. 7F, H: SMO-positive cilia and basal body IFT88 levels in control and CCDC15 siRNA-transfected cells
- Fig. S3H: centriole amplification in HU-treated control and CCDC15 siRNA-transfected cells (no)
- Fig. S3A: centrosomal levels upon CCDC15 depletion There are two reasons for why we performed two experimental replicates for these experiments: 1) results from the two experimental replicates were similar, 2) quantification of data by U-ExM is laborious. To address the reviewer’s comments, we will perform the third experimental replicate for the sets of data that led to major conclusions of our manuscript, which are Figures 4H, 6C, 6E, 6J, 6K, 7F, 7H and S3A.
3) The protein interaction studies presented in Fig. 3 could be of higher quality. While it is great that the authors compared interactions to the centriolar protein SAS6, which is not expected to interact with CCDC15, the presented data raise many questions.
__a) In most cases, co-expression of tagged CCDC15 stabilizes the tested interaction partners, such that the overall abundance seems to be higher. The increase in protein abundance is substantial for Flag-FAM161A (Fig. 3D) and GFP-Centrin-2 (Fig. 3E) and is even higher for the non-interactor SAS6 (Fig. 3G), while it cannot be assessed for GFP-POC1B (Fig. 3F). Hence, the higher expression levels under these conditions make it more likely that these proteins are "pulled down" and therefore do not represent appropriate controls. __
We agree with the reviewer that the differences in protein abundance of the prey proteins upon expression of CCDC15 relative to control might impact the interpretation of the interaction data. To address this concern, we will perform the following experiments:
- To account of the potential stabilizing effects of CCDC15 expression, we will change the relative ratio of plasmids expressing proteins of interest and assess the expression of bait and prey protein levels. We will then repeat the co-immunoprecipitation experiments in conditions where prey expression levels are similar.
- To avoid the potential stabilizing effects of CCDC15 overexpression, we will perform immunoprecipitation experiments in cells expressing GFP or V5-tagged inner scaffold proteins and assess their potential physical or proximity interaction by blotting for endogenous CCDC15. __b) All Co-IP experiments are lacking negative controls in the form of proteins that are not pulled down under the presented conditions. __
For the co-IP experiments, we only included a specificity control for the interaction of the bait protein with the tag of the prey protein (i.e. GBP pulldown of GFP or GFP-CCDC15-expressing cells). As the reviewer suggested, we will also include a specificity control for the interaction of bait with the tag of the prey protein for co-immunoprecipitation experiments (i.e. GFP pulldown of cells expressing GFP-CCDC15 with V5-BirA* or V5-BirA*-FAM161A).
__c) The amounts of co-precipitation of the tested proteins appears very different. Could this reflect strong or weak interactors, or does it reflect the abundance of the respective proteins in centrioles? __
We agree with the reviewer that the quantity of the co-precipitated prey proteins might be a proxy for the interaction strength if the abundance of the bait proteins is similar. However, the expression levels of bait and prey proteins in co-transfected cells are different and thus, cannot be used to derive a conclusion on the interaction strength. For the revised manuscript, we will repeat the IP experiments and comment on this in the discussion section.
__4) The observation that IFT88 is supposedly decreased at the base of cilia in CCDC15-depleted cells requires additional experiments/evidence. Fig. 7G shows the results of n = 2 and more importantly, a similar reduction of gamma-tubulin in siCCDC15. Could the observed reduction in IFT88 be explained by a decrease in accessibility to immunofluorescence microscopy? Would the reduction in IFT88 at the base also be apparent when the signals were normalized to gamma-tubulin signals? __
To address the reviewer’s concern, we quantified the basal body gamma-tubulin and IFT88 levels in control and CCDC15-depleted cells and plotted the basal body IFT88 levels normalized to gamma-tubulin levels in Fig. 7H. Similar to the reduction in IFT88 levels, gamma-tubulin-normalized IFT88 levels was significantly less relative to control cells. Moreover, the gamma-tubulin basal body levels were similar between control and CCDC15 cells. We revised the gamma-tubulin micrographs in Fig. 7G to represent this. These results indicate that the reduction in basal body IFT88 levels upon CCDC15 depletion in specific.
__5) The observed Hedgehog signaling defects are described as follows: "CCDC15 depletion significantly decreased the percentage of SMO-positive cells". It is similarly described in the figure legend. If this was true, the simplest explanation would be that it reflects the reduction in ciliation rate (which is in a similar range). If SMO-positive cilia (instead of "cells") were determined, the text needs to be changed accordingly. __
As the reviewer pointed out, we quantified SMO-positive cilia, but not cells. We are sorry for this typo. We corrected SMO-positive cells as SMO-positive cilia in the manuscript text, Fig. 7 and figure legends.
__6) OPTIONAL: While expansion microscopy is slowly becoming one of the standard super-resolution microscopy methods, which is particularly well validated for studying centrioles, the authors should consider confirming part of their findings (as a proof of principle, surely not in all instances) by more established techniques. This could serve to convince critical reviewers that may argue that the expansion process may induce architectural defects of destabilized centrioles, as observed after disruptions of components, such as in Fig. 6. Alternatively, the authors could cite additional work that make strong cases about the suitability of expansion microscopy for their studies, ideally with comparisons to other methods. __
- SIM imaging was previously successfully applied for nanoscale mapping of other centriole proteins including CEP44, MDM1 and PPP1R35 (Atorino et al., 2020; Sydor et al., 2018; Van de Mark et al., 2015). To complement the U-ExM analysis, we have started imaging cells stained for CCDC15 and different centriole markers (i.e. distal appendage, proximal linker, centriole wall) using a recently purchased 3D-SIM superresolution microscope. We already included the SIM imaging data for CCDC15 localization in centrosome fractions purified from HEK293T cells in Fig. S5B. In the revised manuscript, we will replace confocal imaging data in Fig. 3A and 3B with SIM imaging data.
- As the reviewer noted, expansion microscopy has been successfully used for the analysis of a wide range of cellular structures and scientific questions including nanoscale mapping of cellular structures across different organisms. In particular, U-ExM of previously characterized centrosome proteins various centriole proteins have significantly advanced our understanding of centriole ultrastructure. In our manuscript, we used the U-ExM protocol that was validated for centrioles by comparative analysis of U-ExM and cryo-ET imaging by our co-authors (Gambarotto et al., 2019; Hamel et al., 2017). To clarify these points, we included the following sentence along with the relevant references in the introduction: “Application of the U-ExM method to investigate known centrosome proteins has started to define the composition of the inner scaffold as well as other centriolar sub-compartments (Chen et al., 2015; Gambarotto et al., 2021; Gambarotto et al., 2019; Kong and Loncarek, 2021; Laporte et al., 2022; Mahen, 2022; Mercey et al., 2022; Odabasi et al., 2023; Sahabandu et al., 2019; Schweizer et al., 2021; Steib et al., 2022; Tiryaki et al., 2022; Tsekitsidou et al., 2023).”
Minor points:
1) Text, figures, and referencing are clear and accurate, apart from minor exceptions.
We clarified and corrected the points regarding text, figures and references as suggested by the two reviewers.
__ 2) The title suggests a regulator role for CCDC15 in centriole integrity and ciliogenesis, which has formally not been shown. __
We revised the title as “CCDC15 localizes to the centriole inner scaffold and functions in centriole length control and integrity”.
__3) As the authors observe changes in centriole lengths in the absence of CCDC15, it would be very insightful to compare these phenotypes to other components that affect centriolar length, such as C2CD3, human Augmin complex components (as HAUS6 is identified in Fig. 1) or others. These could be interesting aspects for discussion, additional experiments are OPTIONAL. __
We agree with the reviewer that comparative analysis of centriole length phenotypes for CCDC15 and other components that regulate centriole length will provide insight into how these components work together at the centriole inner core. To this end, we phenotypically compared CCDC15 loss-of-function phenotypes to that of other components of the inner scaffold (POC5, POC1B, FAM161A) that interact with CCDC15. In agreement with their previously reported functions in U2OS or RPE1 cells, we found that POC5 depletion resulted in a 4% slight but significant increase in centriole length and POC1B depletion resulted in a 15% significant decrease. In contrast, FAM161A depletion did not alter centriole length (siControl: 447.8±59.7 nm, siFAM161A 436.3±64 nm). Together, our analysis of their centriolar localization dependency and regulatory roles during centriole length suggest that CCDC15 and POC1B might form a functional complex as positive regulators of centriole length. In contrast, POC5 functions as a negative regulator and might be part of a different pathway for centriole length regulation. We integrated the following sub-paragraph in the results section and also included discussion of this data in the discussion section:
“Moreover, we quantified centriole length in control cells and cells depleted for POC5 or POC1B. While POC5 depletion resulted in longer centrioles, POC1B resulted in shorter centrioles (POC5: siControl: 414.1 nm±38.3, siPOC5: 432.7±44.8 nm, POC1B: siControl: 400.6±36.1 nm, siPOC1B: 341.5±44.39 nm,). FAMA161A depletion did not alter centriole length (siControl: 447.8±59.7 nm, siFAM161A 436.3±64 nm). Together, these results suggest that CCDC15 might cooperate with POC1B and compete with POC5 to establish and maintain proper centriole length.”
__ 4) While the reduced ciliation rate in the absence of CCDC15 is convincing, the authors did not investigate "ciliogenesis", i.e. the formation of cilia, and hence should re-phrase. The sentence in the discussion that "CCDC15 functions during assembly" should be removed. __
To clarify that we only investigated the role of CCDC15 in the ability of cells to form cilia, we replaced sentences that indicates “CCDC15 functions in cilium assembly” with “CCDC15 is required for the efficiency of cilia formation”.
__5) The existence of stably associated CCDC15 pools with centrosomes (Fig. 2) requires further evidence. The recovery of fluorescence after photobleaching in FRAP experiments is strongly dependent on experimental setups and is only semi-quantitative. A full recovery is unrealistic, hence, it is ideally compared to a known static or known mobile component. I personally think this experiment -as it is presented now- is of little value to the overall fantastic study. The authors may consider omitting this piece of data. __
We agree with the reviewer that FRAP data by itself does not prove the existence of stably associated CCDC15 pool. As controls in these experiments, we use FRAP analysis of GFP-CCDC66, which has a 100% immobile pool at the cilia and 50% immobile pool at the centrosomes as assessed by FRAP (Conkar et al., 2019). To address these points, we toned down the conclusions derived from this experiment by revising the sentence as follows:
Additionally, we note that the following data provides support for the stable association of CCDC15 at the centrioles:
- About 49.6% (± 3.96) of the centrioles still had CCDC15 fluorescence signal at one of the centrioles upon CCDC15 siRNA treatment (Fig. 5A, 5B). The inefficient depletion of the mature centriole pool of CCDC15 is analogous to what was observed upon depletion of other centriole lumen and inner scaffold proteins including WDR90 and HAUS6 (Schweizer et al., 2021; Steib et al., 2020). __6) The data that CCDC15 is a cell cycle-regulated protein is not very convincing (see Fig. 3H), as the signals area weak and the experiment has been performed only once (n= 1). This piece of data does not appear to be very critical for the main conclusions of the manuscript and may be omitted. Otherwise, this experiment should be repeated to allow for proper statistical analysis. __
We will perform these experiments two more times, quantify cellular abundance of CCDC15 in synchronized populations from three experimental replicates and plot it with proper statistical analysis.
__7) Experimental details on how "defective centrioles" are determined are missing. __
We included the following experimental details to the methods section:
“Centrioles were considered as defective when the roundness of the centriole was lost or the microtubule walls were broken or incomplete. In the longitudinal views of centrioles, defective centrioles were visualized as heterogenous acetylated signal along the centriole wall or irregularities in the cylindrical organization of the centriole wall (Fig. 5F). We clarified these points in the methods section.
__ 8) For figures, in which the focus should be on growing centrioles (see Fig. 4), it could be helpful to guide the reader and indicate the respective areas of the micrographs by arrows. __
We added arrows to point to the respective areas of the micrographs in Fig. 4F.
__ 9) Page18: "centriole length shortening" could be changed to "centriole shortening". __
We corrected this description as suggested.
__10) It is unclear how the authors determine distal from proximal ends of centrioles in presented micrographs (see Fig. 5D). __
We determined the proximal and distal ends of the centrioles by taking the centriole pairs as a proxy. Even though we only represent a micrograph containing a single centriole in some of the U-ExM figures including Fig. 5D, the uncropped micrographs contain two centrioles, which are oriented orthogonally and tethered to each other at their proximal ends in interphase cells. We added the following sentence to the methods section to clarify this point:
*“Since centrioles are oriented orthogonally and tethered to each other at their proximal ends in interphase cells, we also used the orientation of the centriole pairs as a proxy to determine the proximal and distal ends of the centrioles.” *
__11) Fig. 7A is missing scale bars and Fig.7 overall is lacking rectangle indicators of the areas that are shown at higher magnification in the insets. __
We added scale bar to Fig. 7A and rectangle indicators for zoomed in regions in Fig. A, E, G.
12) Fig. 7C displays cilia that appear very short, especially when comparing to the micrographs and bar graphs presented. The authors may want to explain this discrepancy.
We thank the reviewer for the comment. The zoomed in representative cilia is 4.1 µM in control cells and 1.4 µM in CCDC15-depleted cells. Therefore, the representative cilia is in agreement with the quantification of cilia in Fig. 7C.
Reviewer #1 (Significance (Required)): • From a technical point of view the authors use two state-of-the-art technologies, namely proximity labeling combined with proteomics and ultrastructure expansion microscopy, that are both challenging and very well suited to address the main questions of this study. ____ • General assessment: The presented study is of highest experimental quality. Despite being very challenging, the expansion microscopy and proximity proteomics experiments have been designed and performed very well to allow solid interpretation. The results of the central data are consistent and allow strong first conclusions about the putative function of the newly identified centriolar protein CCDC15. The study presents a solid foundation for future hypothesis-driven, mechanistic analysis of CCDC15 and inner scaffold proteins in centriole length control and maintaining centriole integrity. The only limitation of the study is that the technically simpler experiments should be repeated to allow proper statistical assessment, which can be addressed easily. • Advance: This is the first study that identifies CCDC15 as a centriolar protein and localizes it to the inner scaffold. It further describes a function for CCDC15 in centriole length control and shows its importance in maintaining centriole integrity with consequences for stable cilia formation in tissue culture. The study provides further functional insights into the interdependence of inner scaffold proteins and the role of CCDC15 in the recruitment of the SFI1/centrin distal complex. • Audience: The manuscript will be of broad interest to the fields of centrosome and cell biology, both from a basic research and genetics/clinical point of view due to the association with human disorders. The state-of-the-art technologies applied will be of interest to a broader cell and molecular biology readership that studies subcellular compartments and microtubules. • Reviewer's field of expertise: Genetics, imaging, and protein-protein interaction studies with a focus on centrosomes and cilia.
We thank the reviewer for recognizing the importance of our work and for supportive and insightful comments that will further strengthen the conclusions of our manuscript. Our planned revisions will address the only major technical limitation raised by the reviewer that requires adding one more experimental replicate for analysis of the data detailed in major point#1. Notably, we also thank the reviewer to specifying the experiments that are not essential or will be out of the scope of our manuscript as “optional”.
Reviewer #2 (Evidence, reproducibility and clarity (Required)):
Summary:
__In this study, Arslanhan et al. propose CCDC15 as a novel component of the centriole inner scaffold structure with potential roles in centriole length control, stability and the primary cilium formation in cultured epithelial cells. Using proximity labelling they explore the common interactors of Poc5 and Centrin-2, two resident molecules of the centriole inner scaffold, to hunt for novel regulators of this structure. The authors leverage expansion microscopy-based localization and siRNA-dependent loss-of-function experiments to follow up on one such protein they identify, CCDC15, with the aforementioned roles in centriole and cilia biology.
This study is designed and laid out nicely; however, to be able to support some of the important claims regarding their proximity labelling results and exploration on the roles of CCDC15, there are several major technical and reproducibility concerns that deem major revision. Similarly, the introduction (perhaps inadvertently) omits much of the recent studies on centriole size control that have highlighted the complexity of this biological problem. As such, addressing the following major points will be essential in further considering this work for publication. __
__We thank the reviewer for recognizing the importance of our work and appreciate the positive reflections on our manuscript and the feedback comments that were well thought-out and articulated and will further strengthen the conclusions of our manuscript. Our planned revisions focus on addressing the reviewer’s comments especially in further supporting our conclusions for proximity-labeling, phenotypic characterization and immunoprecipitation experiments, examining CCDC15 centriole localization in an additional cell line and investigating how CCDC15 works together during centriole length control with known components of the inner scaffold. __
Major points:
__1a) The authors use Poc5 and Centrin-2 molecules as joint baits to reveal the interactome of the centriole inner scaffold, however the work lacks appropriate experimental and analytical controls to argue that this is a proximity mapping "at the centriole inner scaffold". In its current state, it is simply an interactome of total Poc5 and Centrin-2, and it might be misleading to call it an interactome at the centriole inner scaffold (the statistical identification of shared interactors cannot do full justice to their biology at the centrosome). Appropriate expression data needed to delineate how large the centrosomal vs. cytoplasmic (or nucleoplasmic) fraction is for either of these molecules, both without and upon the addition of biotin (to see whether the bulk of interaction data stem from the cytoplasm/nucleoplasm or the centrioles themselves). The authors can test this by selectively blotting a lysate fraction containing the centrosomes after centrifugation, and compare them with the simultaneous blot of the supernatant (which were readily used for the blots presented in Fig. 1B). This experiment also becomes very relevant for the case of Centrin-2, as it also heavily localizes to the nucleoplasm as the authors found out (see Fig. 1A and Fig. S1A). __
__ Additionally, an orthogonal approach should be taken to perform bio-image analysis on their biotin/streptavidin imaging data to demonstrate the exact ratios between the centrosomal vs. cytoplasmic/nucleoplasmic biotin activation with appropriate signal normalization between the biotin/streptavidin images. This is particularly important, as although the authors claim that these cells stably express the V5BirA*, it seems that there is partial clonality to the expression. Some cells in both the Poc5 and Centrin-2 fusion constructs appear to lack the V5/Streptavidin signals upon Biotin addition (such as the two cells in the centre right in Poc5, and again a cell in the centre right for Centrin-2 images). In its current form, Fig. 1A lacks signal quantification and does not report any information about the replicates and distributions of the data. I worry that this may raise concerns on the reproducibility if published in its current form. __a) We agree with the reviewer that the proximity maps of POC5 and
a) Centrin-2 are not specific to the centriole inner scaffold and thus, do not represent the inner scaffold interactome. The proximity maps identified interactions across different pools of POC5 and Centrin-2 in nucleus, cytoplasm and centrosomes (Fig. 1, S1). To highlight these important points, we already included extensive analysis of the different cellular compartments and biological processes identified by the POC5 and Centrin-2 proximity maps in the results section (pg. 9-10).
We think that there are two reasons that caused the misinterpretation of the use of these proximity maps as the “inner scaffold interactome”: 1) the way we introduced the motivation for proximity mapping studies, 2) proposing the use of the resulting interactomes as resources for identification of the full repertoire of the inner scaffold proteins. To clarify these points, we revised the manuscript in all relevant parts that might have led to misinterpretation. Following are the specific revisions:
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To clarify that the proximity maps are not specific to the inner scaffold pools of POC5 and Centrin-2, we revised the title of the results section for Fig. 1 and 2 as follows: “Proximity mapping of POC5 and Centrin-2 identifies new centriolar proteins”.
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To indicate that POC5 and Centrin-2 localizes to the cytoplasm and/or nucleus in addition to the centrosome, we added the following sentence to the result section: “In addition to centrosomes, both fusion proteins also localized to and induced biotinylation diffusely in the cytoplasm and/or nucleus (Fig. 1A).”
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In the introduction, we revised the following sentence “Here, we used the known inner scaffold proteins as probes to identify the molecular makeup of the inner scaffold in an unbiased way.” as follows: *“Here, we used the known inner scaffold proteins as probes to identify new components of the inner scaffold”. *
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To highlight the different cellular pools of POC5 and Centrin-2 and identification of their interactors in these pools, we included the following sentence in the results section: “As shown in Fig. S1, Centrin-2 and POC5 proximity interactomes were enriched for GO categories that are relevant for their published functions during centrosomal, cytoplasmic and/or nuclear biological processes and related cellular compartments (Azimzadeh et al., 2009; Dantas et al., 2013; Heydeck et al., 2020; Khouj et al., 2019; Resendes et al., 2008; Salisbury et al., 2002; Steib et al., 2020; Yang et al., 2010; Ying et al., 2019).”
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We replaced the “interactome” statement with “proximity interaction maps” or “proximity interactors” throughout the manuscript to prevent the conclusion that the proximity maps represent the inner scaffold interactome. b) As the reviewer noted, most centrosome proteins have multiple different cellular pools including the centrosome. For most proteins like gamma-tubulin and centrin, their cytoplasmic/nucleoplasmic pools are more abundant than their centrosomal pools (Moudjou et al., 1996; Paoletti et al., 1996). For the Firat-Karalar et al. Current Biology 2015 paper, I compared the biotinylation levels of centrosomal fractions versus cytoplasmic fractions and confirmed that this is also true in cells expressing myc-BirA* fusions of CDK5RAP2, CEP192, CEP152 and CEP63 (unpublished) (Firat-Karalar et al., 2014). For the revised manuscript, we will compare the biotinylation level of centrosomal, nuclear and cytoplasmic pools of V5Bir*-POC5 and V5BirA*-Centrin-2 using the stable lines. To this end, we will use published centrosome purification protocols. We will include this data in Fig. S1 to highlight that the proximity interactomes represent the different pools of the bait proteins and to show the relative levels of the baits across their different pools.
c) BioID approach has been successfully used to probe centrosome interactions by my lab and other labs in the field. In fact, proximity interaction maps of over 50 centrosome proteins were published as resource papers by Pelletier&Gingras labs (Gheiratmand et al., 2019; Gupta et al., 2015). Analogous to our strategy in this manuscript, these studies generated proximity maps of centrosome proteins by creating cell lines that stably express BioID-fusions of centrosome proteins followed by streptavidin pulldowns from whole cell extracts and mass spectrometry analysis. Since majority of centrosome proteins also have pools in multiple cellular locations, the published BioID proximity maps for centrosome proteins are not specific to centrosomes. However, the proximity maps included all known centrosome proteins and identified new proteins, which shows that centrosome interactions are represented in pulldowns form whole cell lysates. Moreover, maps form whole cell lysates are also advantageous as they are are unbiased and can be used in future studies as resources for studying the functions and interactions of the bait proteins in different contexts.
In the Firat-Karalar et al. Current Biology 2015 paper, I combined centrosome purifications with BioID pulldowns to enrich for the centrosomal interactions in the proximity maps of centriole duplication proteins(Firat-Karalar et al., 2014). However, I started the purification with cells transiently transfected with the BioID-fusion constructs, which resulted in high ectopic expression of the fusions in the cytoplasm and/or nucleus. Therefore, centrosome enrichments were useful as an additional step before mass spectrometry. Comparative analysis of the data for proximity maps of 4 centrosome proteins generated from stable lines or centrosome fractions of transiently transfected cells substantially overlap as compared in the Gupta et al. Cell 2015 study and were more comprehensive (Table S2) (Gupta et al., 2015). Therefore, we are confident that the proximity interactomes we generated for POC5 and Centrin-2 include their centrosomal interactions.
__1b) Similarly, it is not clear whether the expression of Poc5 and Centrin-2 fusion molecules somehow interfere with their endogenous interactions or function. At least some loss-of-function (e.g., RNAi) experiments should be performed where the depletion of endogenous proteins should be attempted to rescue by the fusion constructs. This will help evaluate whether the fusion proteins can rescue the depletion of their endogenous counterparts and behave as expected from a wild-type scenario. __
The reviewer raises an important concern regarding the physiological relevance of the POC5 and Centrin-2 proximity maps. In the manuscript, we showed and discussed the validation of their proximity interactomes by two lines of evidence, which are: 1) the interactomes identified the previously described cellular compartments, biological processes or interactors of POC5 and Centrin-2, 2) the interactomes led to the identification of CCDC15 as a new inner scaffold protein.
As the reviewer indicated, stable expression of POC5 and Centrin-2 in the presence of their endogenous pools might affect cellular physiology and thereby the landscape of the interactomes. We plan to address this using the following experiments:
a) We will perform a set of functional assays to assess whether stable V5BirA*-Centrin-2 and V5BirA*-POC5 cells behaves like control cells in terms of their centrosome number, cell cycle profiles and mitotic progression. We will specifically quantify:
- centrosome number (immunofluorescence analysis for gamma-tubulin and centrin)
- their mitotic index (immunofluorescence analysis by DAPI)
- spindle polarity and percentage of multinucleation (immunofluoerescence analysis for microtubules, gamma-tubulin and DAPI)
- cell cycle profiles (flow cytometry and immunofluorescence)
- apoptosis (immunoblotting for caspase 3) Together, results from these experiments indicate that the V5BirA*-POC5 or Centrin-2-expressing stable lines do not exhibit defects associated with their stable expression.
b) We will perform expansion microscopy in V5BirA*-Centrin-2 and V5BirA*-POC5 cells to assess whether the fusion protein specifically localizes to the centriole inner scaffold, which will provide support for the presence of inner scaffold proteins in their proximity maps. Specifically, we plan to stain the fusion proteins by V5 or BirA antibodies and include the data for the antibody that works for expansion microscopy. This experiment will address whether their stable expression results in specific localization of these proteins at the centriole inner scaffold.
1c) Overall, as the entire claim around the proximity mapping revolve around its assumption about the centriole inner scaffold, these controls seem imperative to substantiate the ground truth of the biology presented in the manuscript.
In the revised manuscript, we toned down and made it clear that Centrin-2 and POC5 proximity maps are not specific to the inner scaffold and do not represent the inner scaffold interactome. Since the maps were generated from the whole cell extract, they will provide a resource for future studies aimed at studying functions and mechanisms of POC5 and Centrin-2 across their different cellular pools including the centrosome.
We would like to also highlight that the proximity maps of POC5 and Centrin-2 are not the major advances of our manuscript. The major advance of our manuscript is the identification of CCDC15 as a new inner scaffold protein that is required for regulation of centriole size and architectural integrity and thereby, for maintaining the ability of centrioles to template the assembly of functional cilia. Importantly, our results identified CCDC15 as the first dual regulator of centriolar recruitment of inner scaffold protein POC1B and the distal end SFI1/Centrin complex and provided important insight into how inner scaffold proteins work together during centriole integrity and size regulation. The new set of experiments we will perform for the revisions of the paper will strengthen these conclusions.
__2) I am curious about the choices of the cell lines in this work. The proximity mapping to reveal CCDC15 as a candidate protein for centriole inner scaffold was performed in HEK293T cells (human embryonic kidney), however its immunostaining was performed using RPE1 and U2OS cells (human retinal and osteosarcoma epithelial cells respectively). This raises questions regarding the generality of CCDC15 as a centriole inner scaffold protein. Could CCDC15 be simply unique to the centriole inner scaffold of epithelial cells such as RPE1 and U2OS cells? Or could the authors demonstrate any information/data on whether it's similarly localized to the inner scaffold in embryonic kidney cells or other cell types? If not, the claims should be moderated to reflect this fine detail. __
To test whether CCDC15 localizes to the inner scaffold in other cell types, we performed U-ExM analysis of CCDC15 localization relative to the centriolar microtubules in differentiating multiciliated epithelial cultures (MTEC). As shown in Fig. S3A, CCDC15 localized to the inner scaffold in the centrioles in MTEC ALI+4 cells. Given that the inner scaffold proteins including CCDC15 and previously characterized ones have not been studied in multiciliated epithelia, this result is important and provides support for potential role of the inner scaffold in ensuring centriole integrity during ciliary beating. Additionally, we examined CCDC15 localization by 3D-SIM in centrosomes purified from HEK293T cells, which showed that CCDC15 localizes between the distal centriole markers CEP164 and Centrin-3 and proximal centriole markers gamma-tubulin and rootletin (Fig. S3B).
3) Discussions and data on the localization of CCDC15 to centriolar satellites appear anecdotal and not fully convincing (Fig. S2D). Given that the authors test the relevance of PCM1 for CCDC15's centriolar localization, it is key to have quantitative data supporting their claim that centriolar satellites can help recruit CCDC15 to the centriole. Could the authors quantify what proportion of CCDC15 localize to the centriolar satellites? One way to do this could be to quantify the colocalization coefficience of CCDC15 and PCM1 signals.
We only observed co-localization of CCDC15 with the centriolar satellite marker PCM1 in cells transiently transfected with mNG-CCDC15. In Fig. S2E, we included the quantification of the percentage of U2OS and RPE1 cells that exhibit co-localization of PCM1 (100% of U2OS cells, about 80% of RPE1 cells). Like CCDC15, ectopic expression of WDR90 revealed its centriolar satellite localization, suggesting a potential link between centriolar satellites and inner scaffold proteins that can be investigated in future studies (Steib et al., 2020). We now included these results in the discussion section as follows:
“As assessed by co-localization with the centriolar satellite marker PCM1, mNG-CCDC15 localized to centriolar satellites in all U2OS cells and in about 80% of RPE1 cells (Fig. S2C-E). Association of CCDC15 with centriolar satellites is further supported by its identification in the centriolar satellite proteomes(Gheiratmand et al., 2019; Quarantotti et al., 2019).”
Even though endogenous staining for CCDC15 did not reveal its localization to centriolar satellites, following lines of data support the presence of a dynamic and low abundance pool of CCDC15 at the centriolar satellites: 1) CCDC15 was identified in the centriolar satellite proteome and interactome (Gheiratmand et al., 2019; Quarantotti et al., 2019). 2) CCDC15 centrosomal targeting is in part regulated by PCM1 (Fig. S2F, S2G). For majority of the proteins identified in the centriolar satellite proteome, their satellite pool can only be observed upon ectopic expression. This might be because their centriolar satellite pool is of low abundance and transient as satellite interactions are extensively identified only in proximity mapping studies, but not in traditional pulldowns
__4) Similar to above (#3), there is no quantitative information on the co-localization or partial co-localization of the signal foci in Fig. 3A and 3B. The authors readily study CCDC15's localization in wonderful detail in their expansion microscopy data, so they could actually consider taking out Fig. 3A and 3B, as the data seem redundant without any quantification. __
To address the reviewer’s concern, we included plot intensity profile analysis of CCDC15 and different centriole markers along a line drawn at the centrioles in Fig. 3A and 3B, which shows the extent of their overlap. As part of our revision plan, we will replace the confocal imaging data in Fig. 3A and 3B with 3D-SIM imaging data of CCDC15 relative to different centriole markers together with plot profile analysis. We already included 3D-SIM imaging of centrosomes purified form HEK293T cells in Fig. S3B. 3D-SIM imaging data will complement the localization data revealed by U-ExM.
__5) Do the authors also feel that CCDC15 localize to the core lumen in a somehow helical manner (Fig. 1A, Fig. 1F top and bottom panels, Fig. 5A etc.)? Le Guennec et al. 2020's helical lattice proposal for the inner scaffold further reaffirms that CCDC15 is indeed a likely major component of the inner scaffold. In my view, authors should state this physical similarity explicitly to further support their findings on CCDC15. __
As the reviewer indicated, cryo–electron tomography and subtomogram averaging of centrioles from four evolutionarily distant species showed that centriolar microtubules are bound together by a helical inner scaffold covering ~70% of the centriole length (Le Guennec et al., 2020). Although U-ExM data do not have enough resolution to show that CCDC15 localizes in a helical manner, we agree with the reviewer that the discussion of this possibility is important and thus we included the following sentence in the results:
“Longitudinal views suggest potential helical organization of CCDC15 at the inner scaffold, which is consistent with its reported periodic, helical structure (Le Guennec et al., 2020).”
__6a) The data on the link between the CCDC15 recruitment and the centriole growth (Fig. 4F) or the G2 phase of the cell cycle (Fig. 4H) are not fully convincing without quantitative data. For Fig. 4F, the authors should consider plotting the daughter centriole length vs the daughter CCDC15 intensities against each another, to see whether more elongated daughters truly tend to have more CCDC15. __
To address the reviewer’s concern, we will plot the daughter centriole length versus CCDC15 intensity at different stages of centriole duplication. In asynchronous cultures that we analyzed with U-ExM, we were not able to find enough cells to perform such quantification. To overcome this limitation, we will perform U-ExM analysis of cells fixed at different points after mitotic shake-off and stained for CCDC15 and tubulin. We will include minimum 10 different representative U-ExM data for different stages of centriole duplication in the revised manuscript along with quantification of length versus signal.
As detailed in the results section, the goal of these experiments was to determine when CCDC15 is recruited to the procentrioles during centriole duplication, but not to suggest a role for CCDC15 in centriole growth. We clarified this by including the following sentence:
“To investigate the timing of CCDC15 centriolar recruitment during centriole biogenesis, we examined CCDC15 localization relative to the length of procentrioles that represent cells at different stages of centriole duplication (Fig. 4F).”
__6b) For Fig. 4H, the argument regarding the cell cycle regulation requires quantification of the bands from several WB repeats, normalized to the expression of GAPDH within each blot (this is particularly relevant, as the bands of CCDC15 do not look dramatically different enough to draw conclusions by eye). __
We will perform these experiments two more times, quantify cellular abundance of CCDC15 in synchronized populations from three experimental replicates and plot it with proper statistical analysis.
__7a) The authors find herein that CCDC15 depletion lead to centrioles that are ~10% shorter than the controls. With the depletion of Poc5 and Wdr90 (other proposed components of the inner scaffold), the centrioles end up larger however (Steib et al., 2020). If the role of inner scaffold in promoting centriole elongation is structural, why are these two results the opposite of each other? I realize there is a brief discussion about this at the end of the paper, however, this requires a detailed discussion and speculation on the relevance of these findings. It would be key to clarify whether the inner scaffold as a structure inhibits or promotes centriole growth - or somehow both? If so, how? __
We agree with the reviewer that comparative analysis of centriole length phenotypes for CCDC15 and other components that regulate centriole length will provide insight into how these components work together at the centriole inner core. To this end, we phenotypically compared CCDC15 loss-of-function phenotypes to that of other components of the inner scaffold (POC5, POC1B, FAM161A) that interact with CCDC15. In agreement with their previously reported functions in U2OS or RPE1 cells, we found that POC5 depletion resulted in a 4% slight but significant increase in centriole length and POC1B depletion resulted in a 15% significant decrease. In contrast, FAM161A depletion did not alter centriole length (siControl: 447.8±59.7 nm, siFAM161A 436.3±64 nm). Together, our analysis of their centriolar localization dependency and regulatory roles during centriole length suggest that CCDC15 and POC1B might form a functional complex as positive regulators of centriole length. In contrast, POC5 functions as a negative regulator and might be part of a different pathway for centriole length regulation. We integrated the following sub-paragraph in the results section in pg. 19 and also included discussion of this data in the discussion section in pg. 23:
“Moreover, we quantified centriole length in control cells and cells depleted for POC5 or POC1B. While POC5 depletion resulted in longer centrioles, POC1B resulted in shorter centrioles (POC5: siControl: 414.1 nm±38.3, siPOC5: 432.7±44.8 nm, POC1B: siControl: 400.6±36.1 nm, siPOC1B: 341.5±44.39 nm,). FAMA161A depletion did not alter centriole length (siControl: 447.8±59.7 nm, siFAM161A 436.3±64 nm). Together, these results suggest that CCDC15 might cooperate with POC1B and compete with POC5 to establish and maintain proper centriole length.”
__7b) There might be some intriguing opposing regulatory action of Poc5 and CCDC15 as demonstrated here, where CCDC15 depletion leads to slightly over-recruitment of Poc5, and vice versa. Does this suggest that a tug-of-war going on between different molecules that localize to the inner scaffold? Does this provide some dynamicity to this structure, which might in turn regulate centriole length both positively and negatively? This may be analogous to how opposing forces of dyneins and kinesins provide robust length control for mitotic spindles. I am speculating here, but hopefully these may provide some useful grounds for further discussion in the paper. If the authors deem it interesting experimentally, they can test whether the two molecules indeed regulate centriole length by opposing each other's action, by a double siRNA of CCDC15 and Poc5 to see if this retains the centriole length at its control siRNA size (like how they do a similar test for Poc1's potential co-operativity with CCDC15 in Fig. 6J). __
We thank the reviewer for proposing excellent ideas on how inner scaffold proteins work together to regulate centriole length. As proposed by the reviewer, different proteins oppose each other analogous to how dynein and kinesin regulate mitotic spindle length. Loss-of-function and localization dependency data support that CCDC15 cooperates with POC1B, which was supported by phenotypic characterization of co-depleted cells (Fig. 6I-K).
The increase in POC5 levels and coverage at the centrioles upon CCDC15 depletion and vice versa (Fig. 7B, 7G) suggest that CCDC15 and POC5 compete with each other in centriole length regulation. As suggested by the reviewer, we attempted to test this by comparing centriole length in cells co-depleted for CCDC15 and POC5 relative to their individual depletions. Although we tried different depletion workflows, we were not able to co-deplete CCDC15 and POC5. Specifically, we tried transfecting cells with CCDC15 and POC5 siRNAs at the same time or sequentially for 48 h or 96 h. The centrioles in cells that survived co-depletion were positive for both CCDC15 and POC5. This might be because co-depletion of both proteins is toxic to cells. Since CCDC15 and POC5 are likely part of two different pathway in regulation of centrioles and also have other cellular functions, this might have caused cell death. We included the following statement in the discussion to address the excellent model proposed by the reviewer:
“Taken together, our results suggest that CCDC15 cooperates with POC1B and competes with POC5 during centriole length regulation. Moreover, they also raise the exciting possibility that centriole length can be regulated by opposing activities of inner scaffold proteins. Future studies that explore the relationship among centriole core proteins are required to uncover the precise mechanisms by which they regulate centriole integrity and size.”
__8) In their introduction section, the authors discuss how relatively little is known about the size control of centrioles, however they fail to mention a series of recent primary literature that uncover striking, new mechanisms and novel molecular players that highlight the complexity of centriole size control. This complexity appears to arise from the existence of multitude of length control mechanisms that influence the cartwheel or the microtubule length individually, or simultaneously via yet-to-be further explored crosstalk mechanisms. a. As such, when the authors talk about the procentriole size control in the introduction, they should discuss and refer to the following studies, in terms of: • How theoretical and experimental work demonstrate that procentriole length may vary dependent on the levels of its building block Sas-6 in animals (Dias Louro et al., 2021 PMID: 33970906; Grzonka and Bazzi, 2022 bioRxiv). • How a homeostatic Polo-like kinase 4 clock regulates centriole size during the cell cycle (Aydogan et al., 2018 JCB PMID: 29500190), and how biochemistry and genetics coupled with mathematical modelling unravel a conserved negative feedback loop between Cep152 and Plk4 that constitutes the oscillations of this clock in flies (Boese et al., 2018 PMID: 30256714; Aydogan et al., 2020 PMID: 32531200) and human cells (Takao et al., 2019 PMID: 31533936). __
__b. Similarly, when the authors refer to centriole size control induced by microtubule-related proteins, they should highlight the further complexity of this process by referring to: • How a molecule located at the microtubule wall, Cep295/Ana1, can regulate centriole length in flies (Saurya et al., 2016 PMID:27206860) and human cells (Chang et al., 2016 PMID:27185865) - like all the other centriolar MT molecules that the authors discuss in the manuscript. • How a crosstalk between Cep97 and Cep152 influences centriole growth in fly spermatids (Galletta et al., 2016 PMID:27185836). • How a crosstalk between CP110-Cep97 and Plk4 influences centriole growth in flies (Aydogan et al., 2022 PMID:35707992), and this molecular crosstalk is conserved, at least biochemically, in human cells (Lee et al., 2017 PMID:28562169). __
We thank the reviewer for highlighting the papers that uncovered new mechanisms and players of centriole size and integrity control as well as for the detailed explanation of how different studies led to these discoveries in different organisms. We should have discussed these proteins, functional complexes and mechanisms in our manuscript and cited the relevant literature. We inadvertently focused on literature that uncovered centriole length regulation by MAPs and the inner scaffold. In the introduction section of the revised manuscript where we introduced centriole size regulation in pg. 5, we summarized the major findings on the role of different MAPs, cartwheel and PLK4 homeostatic clock in ensuring formation of centrioles at the correct size in different organisms.
__Minor points: __
__1) Introduction section: Literature reference missing for the sentence starting with "Importantly, the stable nature of centrioles enables them to withstand...". __
We cited research articles that show the importance of centriole motility during ciliary motility and cell division.
“Importantly, the stable nature of centrioles enables them to withstand mechanical forces during cell division and upon ciliary and flagellar motility (Abal et al., 2005; Bayless et al., 2012; Meehl et al., 2016; Pearson et al., 2009).
__2) Fig. S1 legend: A typo as follows: CRAPome banalysis should read CRAPome analysis. __
We corrected this typo.
__3) Fig. S2: Info on the scale bar in the legend is missing in Fig. S2A. Scale bars for different panels are missing in general in Fig. S2A. __
We added scale bar information for Fig. S2A and to all other supplementary figure legends that lack scale bar information.
__4) Fig. 3A and 3B: When displaying the data, coloured cartoon diagrams would be beneficial to guide the reader who are not fully familiar with the spatial orientation of these proteins. __
As suggested by the reviewer, we will remove the confocal imaging data for CCDC15 localization from Fig. 3A and 3B. For the revised version, we will include 3D-SIM imaging data along with a diagram that represents the spatial orientation of CCDC15 relative to the chosen centriole markers.
__5) Fig. 3H: No information about the sample number (number of cells or technical repeats examined) reported. __
We included information on the number of experimental replicates and cells analyzed.
__6) Fig. S3B legend: A typo as follows: CCD15-depelted RPE1 cells should read CCDC15-depleted RPE1 cells. __
We corrected this typo.
__7) Fig. S3B legend: A typo as follows: cellswere fixed with should read cells were fixed with. __
We corrected this typo.
__8) There are many spelling mistakes and typos throughout the paper. I have listed a few examples above, but please carefully read through the manuscript to correct all the errors. __
Thank you for indicating the spelling mistakes we missed to correct for initial submission. In the revised manuscript, we carefully read through the manuscript to correct the mistakes.
__9) Fig. S3E: The orange columns depicting % of cells with Sas-6 dots look awkward. Why the columns look larger than the mean line? Please correct as appropriate. __
The total percentage of cells in the two categories (orange and purple) we counted is 100%, which corresponds to the column value at the y-axis. Therefore, the value for each experimental replicate for the orange category is less than 100% and is marked below the 100% line.
__10) Although authors provide microscopy information for the U-ExM and FRAP experiments, there is no information about the microscopy on regular confocal imaging experiments which should be detailed in Materials and Methods. Also, there is no information about the lenses, laser lines and the filter sets that were used in the imaging experiments. These should be provided as well. __
In the methods section, we now included detailed information for the microscopes we used and imaging setup (lenses, laser lines, filter sets, detectors, z-stack size, resolution).
11)
- __ Fig. 2A: lacks a scale bar. __
- __ Fig. 2C legend: lacks info on the scale bar length. __
- __ Fig. 5A legend: lacks info on the scale bar length. __
- __ Fig. 7A: lacks a scale bar. __
- __ Fig. 7G legend: lacks info on the scale bar length. __
- __ Fig. S2C-E: lack scale bars. __
- __ Fig. S3D, F and H: lack scale bars. (Fig. S4 in the revised manuscript)__
- __ Fig. S3J legend: lacks info on the scale bar length. (Fig. S4 in the revised manuscript)__
- __ Fig. S4A, B, D and E: lack scale bars. (Fig. S5 in the revised manuscript)__
- __ Fig. S4C legend: lacks info on the scale bar length. (Fig. S5 in the revised manuscript)__
- __ Fig. S4G legend: lacks info on the scale bar length. (Fig. S5 in the revised manuscript)__ We added the scale bars and the size information to the figures and figure legends for the above figures.
Reviewer #2 (Significance (Required)): __The findings of this study join among the relatively new literature (e.g., Steib et al., 2020 and Le Guennec et al. 2020) on the nature of centriole inner scaffold and its potential roles in centriole formation, integrity and its propensity to form the primary cilium. Therefore, it will be of interest to a group of scientists studying these topics in the field of centrosomes/cilia.
My expertise is on the biochemistry and genetics of centriole formation in animals.__
We thank the reviewer for his/her comments and constructive feedback to improve our manuscript. We are encouraged to see that the reviewer acknowledges how the results from our manuscript advances our understanding of centriole length, integrity and function regulation.
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how did you teach yourself zettelkasten? .t3_11ay28d._2FCtq-QzlfuN-SwVMUZMM3 { --postTitle-VisitedLinkColor: #9b9b9b; --postTitleLink-VisitedLinkColor: #9b9b9b; --postBodyLink-VisitedLinkColor: #989898; }
reply to u/laystitcher at https://www.reddit.com/r/Zettelkasten/comments/11ay28d/how_did_you_teach_yourself_zettelkasten/
Roughly in order: - Sixth grade social studies class assignment that used a "traditional" index card-based note taking system. - Years of annotating books - Years of blogging - Havens, Earle. Commonplace Books: A History of Manuscripts and Printed Books from Antiquity to the Twentieth Century. New Haven, CT: Beinecke Rare Book and Manuscript Library, 2001. - Locke, John, 1632-1704. A New Method of Making Common-Place-Books. 1685. Reprint, London, 1706. https://archive.org/details/gu_newmethodmaki00lock/mode/2up. - Erasmus, Desiderius. Literary and Educational Writings, 1 and 2. Edited by Craig R. Thompson. Vol. 23 & 24. Collected Works of Erasmus. Toronto, Buffalo, London: University of Toronto Press, 1978. https://utorontopress.com/9781487520731/collected-works-of-erasmus. - Kuehn, Manfred. Taking Note, A blog on the nature of note-taking. December 2007 - December 2018. https://web.archive.org/web/20181224085859/http://takingnotenow.blogspot.com/ - Ahrens, Sönke. How to Take Smart Notes: One Simple Technique to Boost Writing, Learning and Thinking – for Students, Academics and Nonfiction Book Writers. Create Space, 2017. - Sertillanges, Antonin Gilbert, and Mary Ryan. The Intellectual Life: Its Spirit, Conditions, Methods. First English Edition, Fifth printing. 1921. Reprint, Westminster, MD: The Newman Press, 1960. http://archive.org/details/a.d.sertillangestheintellectuallife. - Webb, Beatrice Potter. Appendix C of My Apprenticeship. First Edition. New York: Longmans, Green & Co., 1926. - Schmidt, Johannes F. K. “Niklas Luhmann’s Card Index: The Fabrication of Serendipity.” Sociologica 12, no. 1 (July 26, 2018): 53–60. https://doi.org/10.6092/issn.1971-8853/8350. - Hollier, Denis. “Notes (On the Index Card).” October 112, no. Spring (2005): 35–44. - Wilken, Rowan. “The Card Index as Creativity Machine.” Culture Machine 11 (2010): 7–30. - Blair, Ann M. Too Much to Know: Managing Scholarly Information before the Modern Age. Yale University Press, 2010. https://yalebooks.yale.edu/book/9780300165395/too-much-know. - Krajewski, Markus. Paper Machines: About Cards & Catalogs, 1548-1929. Translated by Peter Krapp. History and Foundations of Information Science. MIT Press, 2011. https://mitpress.mit.edu/books/paper-machines. - Goutor, Jacques. The Card-File System of Note-Taking. Approaching Ontario’s Past 3. Toronto: Ontario Historical Society, 1980. http://archive.org/details/cardfilesystemof0000gout.
And many, many others as I'm a student of intellectual history.... If you want to go spelunking on some of my public notes, perhaps this is an interesting place to start: https://hypothes.is/users/chrisaldrich?q=tag%3A%22note+taking%22 I also keep a reasonable public bibliography on this and related areas: https://www.zotero.org/groups/4676190/tools_for_thought
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- Feb 2023
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www.biorxiv.org www.biorxiv.org
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Note: This rebuttal was posted by the corresponding author to Review Commons. Content has not been altered except for formatting.
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Reply to the reviewers
We thank all the reviewers for having raised constructive criticism to fortify the main message and improve the clarity of the manuscript. We appreciate that all reviewers found that our work addresses an important topic and is of interest to a broad audience. We believe that we have thoroughly addressed the concerns of the reviewers, especially with regard to 1) performing another SMC3 chromatin immunoprecipitation and sequencing (ChIP-seq) replicate and control, 2) including a later time point for the transcriptional data, and 3) performing additional characterization of the growth phenotype of the SMC3 conditional knockdown.
Reviewer #1
(Evidence, reproducibility and clarity (Required)):*
Summary The present work by Rosa et al., provides convincing data about the presence and functional relevance of the cohesin complex in Plasmodium falciparum blood stages. In accordance with other organisms, the composition of the cohesin complex containing SMC1, SMC3 RAD21 and putatively STAG could be confirmed via pulldown and mass spectrometry. Basic characterization of endogenous tagged SMC3 demonstrated the expression and nuclear localization during IDC, as well as the relatively stable accumulation at centromeric regions, consistent with the known cohesin function in chromatid separation. Furthermore, dynamic and stage-dependent binding to intergenic regions observed in ChIPseq and major transcriptome aberrations upon knockdown of SMC3 (__Response: __As we regularly perform ChIP-seq experiments in the lab, we have generated multiple negative control datasets. In our opinion, the most stringent negative control for an HA-tagged protein is performing ChIP with an HA antibody in a WT strain. We have recently published an in-depth analysis of this (and other) negative ChIP-seq controls (Baumgarten & Bryant, 2022, https://doi.org/10.12688/openreseurope.14836.2). We show in this publication that non-specific ChIP-seq experiments (such as negative controls) result in an over-representation of HP1-heterochromatinized regions due to differences in sonication efficiency of heterochromatin and technical challenges with mapping regions with high levels of homology. In the anti-HA in WT ChIP negative control (performed at 12hpi), we do not see any enrichment at centromeric regions, but rather at heterochromatinized regions where clonally variant gene families are located. We performed peak calling analysis and found no significant overlap between the negative control ChIP-seq and the SMC3-3HA ChIP-seq data at 12hpi.
In addition, we have now performed a second biological replicate of the SMC3-3HA ChIP-seq with a different clone at all time points. We compared this data to that from the original clone and found significant overlap of the peaks called (see what is now Table 4 and Supp. Fig. 3A). We generated a stringent list of peaks that were shared between both clones at each time point and repeated all downstream analyses (see what are now Tables 5-8). We found that our conclusions were largely unchanged. Text describing these experiments and analyses have been added throughout the results section.
- Proposed mechanism of repressive effect of SMC3 early in IDC on genes, that get de-repressed in late stages: To claim this mode of function, it would be necessary to include a KD on late stage parasites. If there is an early repressive role of SMC3, upregulated genes should not be affected by late SMC3-KD. __Response: __To be clear, we are most interested in the transcriptional role of SMC3 during interphase, where results are not confounded by its potential role in mitosis. However, we did collect a 36hpi time point in the SMC3-3HA-glmS and WT strain, with and without glucosamine. We have added this last time point and the WT data from the other two time points to the manuscript (see Tables 11-13). Unfortunately, and for reasons unknown, the WT replicates treated with glucosamine showed a significantly advanced “transcriptional age” compared to the other replicates at 36hpi (see what is now Supp. Fig. 5B). Thus, we did not feel comfortable performing the RNA-seq analysis as we did with the other two time points (i.e. subtracting up- and down-regulated genes from the WT control from the SMC3-3HA-glmS data sets). We have added this information to the results section (Lines 256 and 261). As the WT parasites treated with glucosamine were approximately 8 hours in advance of the untreated WT parasites for the 36hpi time point, any up- and down-regulated genes might have been due to differences in the cell cycle rather than due to glucosamine treatment. The glmS system of inducible knockdown is widely used in P. falciparum; however, to our knowledge, no lab has investigated whether glucosamine treatment affects transcription in wildtype cells over the course of the IDC. Thus, for accurate phenotypic characterization of any protein with this system with regard to transcriptomics, we thought it was important to provide an RNA-seq dataset to define the cohort of genes affected by glucosamine treatment in WT parasites. We hope that our study will demonstrate the importance of using stringent controls when using inducible knockdown systems.
To address the question of whether genes that are upregulated upon depletion of SMC3 at early stages are affected at the 36hpi time point, we performed differential expression analysis of the SMC3-3HA-glmS parasites with and without glucosamine at 36hpi (we have added this data in Table 11). Again, significantly up- and down-regulated genes were not filtered using the WT dataset. With this analysis, we see only three genes from the list of invasion-related genes (Hu et al., 2010) that are up-regulated, but none of them have a significant q-value (Tab 5 of Table 18). Thus, depletion of SMC3 in late stage parasites does not lead to up-regulation of the same genes that are upregulated at 12 and 24hpi. We have added this information to the text (Line 273).
Furthermore, the hypothesized repressive effect of SMC3 does not explain the numerous genes downregulated in KD.
__Response: __As we state on line 350, we do not observe enrichment of SMC3 at downregulated genes, suggesting an indirect or secondary effect of SMC3 KD on these genes.
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Due to the fact, that the KD was induced at the exact same timepoint and analysed 12h and 24h after induction it is possible that identified, differentially expressed genes at 24h are not directly regulated by SMC3, but rather due to a general deregulation of gene expression. Did the authors attempt to analyse gene expression upon induction at ring, trophozoite and schizont stage? Response: __As we state on line 230, in order to achieve SMC3 KD at the protein level, we had to treat the parasite with glucosamine for two cell cycles (approximately 96 hours). After two cell cycles of glucosamine treatment, the parasites were tightly synchronized and sampled 12 and 24 hours later. Thus, SMC3 KD takes place over the course of multiple days, but parasites are collected after stringent synchronization. Giemsa staining and bioinformatic analysis (line 250) of the RNA-seq data from parasites (with or without glucosamine) harvested at 12 and 24 hpi show that these parasites were synchronous and that there were no gross differences in genome-wide transcript levels. It is certainly possible that differentially expressed genes at 12 or 24hpi are not directly regulated by SMC3, and this is precisely why we perform ChIP-seq of SMC3: to provide evidence of direct involvement via binding, as stated on line 281. __
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*Based on rapid parasite growth, the authors hypothesize a higher invasion rate due to upregulation of invasion genes. This hypothesis is not supported by quantitative invasion assays or quantification of invasion factors on the protein level. An alternative explanation could be a shorter cell cycle (__Response: __We have repeated the growth curve analysis with additional clones and no longer observe a growth phenotype in the SMC3 knockdown condition. We have added images of Giemsa-stained parasites from the knockdown time course we performed to what is now Supp. Fig. 5A. We see no obvious differences in cell morphology caused by glucosamine treatment in the WT or SMC3-3HA-glmS parasites.
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Correlation of SMC3-occupancy/ATAC/expression profile of the exemplary genes rap2 and gap45 (Figure 4C,D,E): is this representative for all upregulated genes? __Response: __SMC3 occupancy shown at rap2 and gap45 is representative for all upregulated genes (see Fig. 4A and B). It is difficult to provide a general representation of the average expression profiles of all up-regulated genes over the course of the IDC, but Fig. 3E shows that the vast majority of up-regulated genes normally reach their peak expression in late stage parasites. With regard to ATAC-seq profiles, we have performed a metagene analysis of chromatin accessibility (data taken from (Toenhake et al., 2018)) at all up-regulated genes at time points that closely correspond to the time points used in our study: 15, 25, and 35, and 40 hpi (new Fig. 4C). This metagene analysis confirms what we observe at individual genes: increasing chromatin accessibility over the course of the IDC at these genes’ promoters. While metagene analyses offer important information, we always try to show the raw data (as in new Figs. 4D-F) from individual examples as proof of principle.
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Given that SMC3 appears to be not essential for parasite growth, the authors could generate a null mutant for SMC3, which might allow for easier analysis of differences in gene regulation, cell cycle progression and/or invasion efficiency. __Response: __As we explain on line 327, very little cohesin is required for normal growth and/or mitosis in our study and two studies in S. cerevisiae and D. melanogaster. However, SMC3 is essential in S. cerevisiae. We were unable to knock out SMC3, and a recent mutagenesis study suggests that SMC3 and SMC1 are essential to the parasite during the intraerythrocytic developmental cycle (Zhang et al. Science, 2018). This is why we chose an inducible knockdown system.
*Reviewer #1 (Significance (Required)):
Own opinion The authors provide a basic characterization of the cohesin component SMC3 using NGS methods to investigate chromatin binding sites and its potential influence on gene expression. *
__Response: __We respectfully disagree that our study offers only a basic characterization of SMC3. We combine IFA, mass spectrometry, and both ChIP-seq and RNA-seq of SMC3 across the entire intraerythrocytic developmental cycle to provide the most detailed and comprehensive functional analysis of SMC3 in P. falciparum to date.
The localisation of SMC3 at centromers as described previously (Batugedara 2020) was confirmed. However, the dynamic binding to other regions in the genome, potentially mediated by other proteins, could not be resolved unequivocal with only one replicate of ChIPseq per time point.
__Response: __With regard to the replicates for ChIP-seq, please see our response to this same point above.
Similarly, the RNAseq data demonstrate the relevance of SMC3 for gene expression, but no clear picture of a regulatory mechanism can be drawn at his point. Lacking information about the mode of binding as well as the setup of transcriptome analysis (only two time-shifted sampling points after simultaneous glmS treatment for 96h resulting in incomplete knockdown) cannot definitely elucidate, if SMC3/cohesin is a chromatin factor that affects transcription of genes in general or a specific repressor of stage-specific genes. __Response: __We agree that we have not established a regulatory mechanism for how SMC3 achieves binding specificity. However, the combination of inducible knockdown (as SMC3 is essential to the cell cycle) and differential expression analysis with ChIP-seq from the same time points across the intraerythrocytic developmental cycle is the most stringent and standard approach in the field of epigenetics for determining the direct role of a chromatin-associated protein in gene expression. We provide a detailed explanation of how the transcriptome analysis was set up in the Results (lines 229-234) and Materials and Methods (lines 715-719) section. With regard to our sampling points being “time-shifted,” we provide bioinformatic analysis (line 246-251, what is now Supp. Fig. 5B) of the RNA-seq data from untreated and glucosamine-treated parasites showing highly similar “ages” with regard to progression through the intraerythrocytic developmental cycle. While we of course also monitor progression through the cell cycle with Giemsa staining (Supp. Fig. 5A), this bioinformatic analysis is the most stringent method of determining specific times in the cell cycle.
*The work will be interesting to a general audience, interested in gene regulation and chromatin remodelling
The reviewers are experts in Plasmodium cell biology and epigenetic regulation.*
Reviewer #2
(Evidence, reproducibility and clarity (Required)):
Rosa et al, Review Commons The manuscript by Rosa et al. addresses the function of the cohesion subunit Smc3 in gene regulation during the asexual life cycle of P. falciparum. Cohesin is a conserved protein complex involved in sister chromatin cohesion during mitosis and meiosis in eukaryotic cells. Cohesin also modulates transcription and DNA repair by mediating long range DNA interactions and regulating higher order chromatin structure in mammals and yeast. In P. falciparum, the Cohesin complex remains largely uncharacterized. In this manuscript, the authors present mass spectrometry data from co-IPs showing that Smc3 interacts with Smc1 and a putative Rad21 orthologue (Pf3D7_1440100, consistent with published data from Batugedara et al and Hilliers et al), as well as a putative STAG domain protein orthologue (PF3D7_1456500). Smc3 protein appears to be most abundant in schizonts, but ChIPseq indicates predominant enrichment of Smc3 in centromers in ring and trophozoite stages. In addition, Smc3 dynamically binds with low abundance to other loci across the genome; however, the enrichment is rather marginal and only a single replicate was conducted for each time point making the data interpretation difficult. Conditional knock-down using a GlmS ribozyme approach indicates that parasites with reduced levels of Smc3 have a mild growth advantage, which is only evident after five asexual replication cycles and which the authors attribute to the transcriptional upregulation of invasion-linked genes following Smc3 KD. Indeed, Smc3 seems to be more enriched upstream of genes that are upregulated after Smc3 KD in rings than in downregulated genes, indicating that Smc3/cohesin may have a function in supressing transcription of these schizont specific genes until they are needed. The manuscript is concise and very well written, however it suffers from the lack of experimental replicates for ChIP experiments and a better characterization of the phenotype of conditional KD parasites. * Major comments • In the mass spectrometry analysis, many seemingly irrelevant proteins are identified at similar abundance to the putative rad21 and ssc3 orthologues, and therefore the association with the cohesion complex seems to be based mostly on analogy to other species rather than statistical significance. Hence, it would be really nice to see a validation of the novel STAG domain and Rad21 proteins, for example by Co-IP using double transgenic parasites.*
__Response: __While our IP-MS data did not yield high numbers of peptides, the top most enriched proteins were SMC3 and SMC1. As we state on line 157, two previous studies have already shown a robust interaction between SMC1, SMC3, and RAD21 in Plasmodium, supporting the existence of a conserved cohesin complex. While the identification of the STAG domain-containing protein is interesting, the purpose of our IP-MS was less about redefining the cohesin complex in P. falciparum and more about confirming that the epitope-tagged SMC3 we generated was incorporated correctly into the cohesin complex and was specifically immunoprecipitated by the antibody we later use for western blot, immunofluorescence, and ChIP-seq analyses. However, to validate the results of ours and others’ mass spectrometry results, we generated two new parasite strains – SMC1-3HA-dd and STAG-3HA-dd – and an antibody against SMC3 (see what is now Supp. Fig. 1). We performed co-IP and western blot analysis with these strains and show an interaction between SMC1 and SMC3 and STAG and SMC3 (see what is now Supp. Fig. 2). This information has been added to the manuscript on lines 162-167.
- *The ChIPseq analysis presented here is based on single replicates for each of the three time points. The significance cutoffs for the peaks are rather high (q __Response: __In our experience, a significance cutoff of FDR As we regularly perform ChIP-seq experiments in the lab, we have generated multiple negative control datasets. In our opinion, the most stringent negative control for an HA-tagged protein is performing ChIP with an HA antibody in a WT strain. We have recently published an in-depth analysis of this (and other) negative ChIP-seq controls (Baumgarten & Bryant, 2022, https://doi.org/10.12688/openreseurope.14836.2). We show in this publication that non-specific ChIP-seq experiments (such as negative controls) result in an over-representation of HP1-heterochromatinized regions due to differences in sonication efficiency of heterochromatin and technical challenges with mapping regions with high levels of homology. In the anti-HA in WT ChIP negative control (performed at 12hpi), we do not see any enrichment at centromeric regions, but rather at heterochromatinized regions where clonally variant gene families are located. We performed peak calling analysis and found no significant overlap between the negative control ChIP-seq and the SMC3-3HA ChIP-seq data at 12hpi.
In addition, we have now performed a second biological replicate of the SMC3-3HA ChIP-seq with a different clone at all time points. We compared this data to that from the original clone and found significant overlap of the peaks called (see what is now Table 4 and Supp. Fig. 3A). We generated a stringent list of peaks that were shared between both clones at each time point and repeated all downstream analyses (see what are now Tables 5-8). We found that our conclusions were largely unchanged. Text describing these experiments and analyses have been added throughout the results section.
The SMC3 ChIP from Batugedara et al., 2020 was performed with an in-house generated antibody (not a commercially available, widely validated antibody as we use) at a single time point in the IDC: trophozoites. Batugedara et al. performed one replicate and did not have an input sample for normalization. Rather, it seems that they incubated beads, which were not bound by antibody or IgG, with their chromatin and used any sequenced reads from this beads sample to subtract from their SMC3 ChIP signal as means of normalization. According to ENCODE ChIP-seq standards, this is not a standard nor stringent way of performing ChIP-seq and the subsequent analysis. Because they did not generate a dataset for their ChIP input, it is not possible to call peaks as we do in our study and compare those peaks with ours.
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The authors argue that during schizogony, cohesin may no longer be required at centromers, explaining the low ChIPsignal at this stage (Line 301). However, during schizogony parasites undergo repeated rounds of DNA replication (S-phase) and mitosis (M-phase) to generate multinucleated parasites; and concentrated spots of Smc3 are observed in each nucleus in schizonts by IFA. In turn, the strong presence of Smc3 at centromers in ring stage parasites is surprising, particularly since the Western Blot in Figure 1D shows most expression of Smc3 in schizonts and least in rings; and Smc3 is undetectable in rings by IFA. Yet, the ChIP signal shows very strong enrichment at centromers, long before S phase produces sister chromatids. What could be the reason for this discrepancy? Again, ChIP replicates and controls would be helpful in distinguishing technical problems with the ChIP from biologically relevant differences. __Response: __We discuss in lines 337-342 not that cohesin is no longer required at centromeres during schizogony, but that its removal from centromeres may be required specifically for separation of sister chromatids, as is seen in other eukaryotes. We also discuss that the unique asynchronous mitosis in Plasmodium may lead to a mixed population of parasites at the time point sampled where there may be some centromeres with SMC3 present and some where it is absent to promote sister chromatid separation. Even though SMC3 may be evicted from centromeres to promote sister chromatid separation, it is likely re-loaded onto centromeres once this process is complete. This is most likely why we see foci of SMC3 in each nucleus of mature schizonts by IFA. With regard to the discrepancy between SMC3 levels in rings seen in total nuclear extracts (by western blot) and at centromeres (by ChIP-seq): the total level of a protein in the nucleus does not necessarily dictate the genome-wide binding pattern or the level of enrichment of that protein at specific loci in the genome. Moreover, if one molecule of SMC3 binds to each centromere, 14 molecules would be needed in a ring stage parasite while over 500 would be needed in a schizont (assuming that there are ~36 merozoites present). SMC3 binds to centromeres in interphase cells in other eukaryotes as well, and we speculate that this binding may play a role in the nuclear organization of centromeres, as we discuss starting on line 333.
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It is surprising that a conserved protein like Smc3 shows such a subtle phenotype, given that it is predicted to be essential and its orthologues have a function in mitosis. Generally, only limited data are presented to characterize the Smc3 KD parasites, and more detail should be included. For example validation of the parasite line using a PCR screen for integration and absence of wt, parasite morphology after KD, and/or analysis of the KD parasites for cell cycle status. __Response: __First, we have repeated our growth curve analysis several times and with more clones and have concluded that there is not a significant growth phenotype in SMC3 KD parasites (see what is now Supp. Fig. 4B). As we discuss on line 342, very little intact cohesin complex seems to be required for normal growth and mitosis in S. cerevisiae and D. melanogaster, which is probably why we do not see an obvious growth or morphological phenotype. Because we could not generate SMC3 knockout parasites, there may be just enough SMC3 left to perform its vital function in our KD strain. We have added PCR data to demonstrate integration of the 3HA tag- and glmS ribozyme-encoding sequence in the clonal strains we are using for all experiments (see what is now Supp. Fig. 1A). Sanger sequencing was performed on these PCR products to confirm correct sequences. We also added images of Giemsa-stained parasites in untreated and glucosamine-treated parasites at all time points to demonstrate a lack of an obvious morphological phenotype in SMC3 KD parasites (see what is now Supp. Fig. 5A).
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Synchronization was performed at the beginning of the growth time course, which would be expected to result in a stepwise increase in parasitemia every 48 hours; however, the parasitemia according to Fig. 4F rises steadily, which would indicate that the parasites are actually not very synchronous. __Response: __We did indeed tightly synchronize these parasites and hope that the stepwise increase in parasitemia is seen better in our new growth curve analysis (see what is now Supp. Fig. 4B).
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The question of whether Smc3 causes a shorter parasite life cycle (quicker progression) or more invasion is important and could be experimentally addressed by purifying synchronous schizont stage parasites and determining their invasion rates as well as morphological examination of the Giemsa smears over the time course. __Response: __We have repeated our growth curve analysis several times and with more clones and have concluded that there is not a significant growth phenotype in SMC3 KD parasites (see what is now Supp. Fig. 4B).
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Please also compare Smc3 transcriptional levels in transgenic parasites to those in wt parasites to rule out that the genetic modification has lead to artificial upregulation of Smc3 transcription. __Response: __We have added this data to what is now Supp. Fig. 4C, showing that there is no significant difference in SMC3 transcript levels between WT and SMC3-3HA-glmS strains. We have added this information to the text of the manuscript (Line 243). As we also generated an SMC3 antibody, we could demonstrate that there is no appreciable difference in SMC3 protein levels between WT and SMC3-3HA-glmS strains (see what is now Supp. Fig. 1D).
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According to Figure S2, even more genes were deregulated at the 12 hpi time point in the WT parasites than in Smc3 parasites, and even to a much higher extent. What "transcriptional age" did the WT control parasites have at each time point? __Response: __We have now included the transcriptional age of all strains, replicates, and treatments in what is now Supp. Fig. 5B. At the 12 hpi time point in particular, regardless of glucosamine treatment, the SMC3-3HA-glmS and WT parasites were highly synchronous. The only large discrepancy we see in transcriptional age is between untreated and glucosamine-treated WT parasites at 36 hpi, which is why we did not include this time point in our transcriptional analysis. We were also surprised by the number of genes that were de-regulated with simple glucosamine treatment. The glmS system of inducible knockdown is widely used in P. falciparum; however, to our knowledge, no lab has investigated whether glucosamine treatment affects transcription in wildtype cells over the course of the IDC. Thus, for accurate phenotypic characterization of any protein with this system with regard to transcriptomics, we thought it was important to provide an RNA-seq dataset to define the cohort of genes affected by glucosamine treatment in WT parasites. We hope that our study will demonstrate the importance of using stringent controls when using inducible knockdown systems.
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A negative correlation with transcription is well established in S. cerevisiae, particularly at inducible genes. How does Smc3 enrichment generally look like for genes that show maximal expression at each of the time point? __Response: __We have performed a metagene analysis of SMC3 enrichment at all genes at each respective time point, which we divided into quartiles of expression based on their FPKM values in the RNA-seq data from the corresponding time point in untreated SMC3-3HA-glmS parasites. This quartile analysis considers all genes, including genes that are not transcribed at all and regardless of whether a gene has a significant SMC3 peak or is differentially expressed upon SMC3 knockdown. At the 12 hpi time point, we do see an inverse correlation between SMC3 enrichment and gene transcription level, but this enrichment is most pronounced across genes bodies. We see the highest SMC3 enrichment at genes in the 4th (lowest) quartile category. For the other two time points, we do not see any obvious pattern of SMC3 enrichment with regard to transcriptional status.
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Line 590: according to the methods, a 36 hpi KD time point was also harvested. Why are the data not shown/analysed? __Response: __To be clear, we are most interested in the transcriptional role of SMC3 during interphase, where results are not confounded by its potential role in mitosis. However, we did collect a 36hpi time point in the SMC3-3HA-glmS and WT strain, with and without glucosamine. We have added this last time point and the WT data from the other two time points to the manuscript (see Tables 11-13). Unfortunately, and for reasons unknown, the WT replicates treated with glucosamine showed a significantly advanced “transcriptional age” compared to the other replicates at 36hpi (see what is now Supp. Fig. 5B). Thus, we did not feel comfortable performing the RNA-seq analysis as we did with the other two time points (i.e. subtracting up- and down-regulated genes from the WT control from the SMC3-3HA-glmS data sets). We have added this information to the results section (Lines 256 and 261). As the WT parasites treated with glucosamine were approximately 8 hours in advance of the untreated WT parasites for the 36hpi time point, any up- and down-regulated genes might have been due to differences in the cell cycle rather than due to glucosamine treatment. The glmS system of inducible knockdown is widely used in P. falciparum; however, to our knowledge, no lab has investigated whether glucosamine treatment affects transcription in wildtype cells over the course of the IDC. Thus, for accurate phenotypic characterization of any protein with this system with regard to transcriptomics, we thought it was important to provide an RNA-seq dataset to define the cohort of genes affected by glucosamine treatment in WT parasites. We hope that our study will demonstrate the importance of using stringent controls when using inducible knockdown systems.
Minor Comments • Line 103/104: the hinge domain and ATPase head domain are mentioned, please annotate these in Figure 1A.
__Response: __We have annotated the hinge and ATPase domains.
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Figure 1D: the kDa scale is missing from the H3 WB. __Response: __We have added a kDa scale.
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What is the scale indicated by different colors in Fig. 2A? __Response: __The different colors (blue, coral, and green) only represent the 12, 24, and 36hpi time points, respectively. This color scheme is used throughout the manuscript. If the reviewer is referring to the color gradation within each circos plot, this does not indicate a specific scale. The maximum y-axis value for all circos plots is 24, as indicated in the figure legend.
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Line 189: it would also be interesting how many peaks are "conserved" between the different time points studied, so not only to compare the gene lists of closest genes but also the intersecting peaks and then the closest genes to the intersecting peaks. __Response: __We have added this information in Table 7 and in the manuscript starting on Line 203. Using the new dataset of consensus peaks between two replicates, there were 88 genes associated with an SMC3 peak across all three time points, most of which were close to a centromeric region.
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What is the distribution of the peaks over diverse genetic elements, such as gene bodies, introns, convergent/ divergent/ tandem intergenic regions? In yeast, cohesion is particularly enriched in convergent intergenic regions, so it would be interesting to see how this behaves in P. falciparum. __Response: __We would have liked to define how many peaks were in intergenic versus genic regions of the genome, but the dataset of “genes” from PlasmoDB includes UTRs. Thus, we would need a better annotation of the genome to perform this analysis. Regardless, we calculated the average SMC3 peak enrichment (shared between both replicates) in intergenic regions between convergent and divergent genes (see what is now Supp. Fig. 3B and Table 6). As we now state in the manuscript on line 198, we see a slight enrichment in regions between convergent genes at all time points, but the differences were not significant.
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Line 130 intra-chromosomal interactions (word missing) __Response: __Thank you for pointing this out. We have corrected this.
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Contrary to Figure 1D, the WB in Figure 3A indicates strong expression of Smc3 in rings. Please comment on this discrepancy. __Response: __While extracts from all time points were run on the same western blot in Fig. 1D and thus developed for the same amount of time, this was not the case for Fig. 3A. In Fig. 3A, the samples were run on different blots and exposed for different times, so while we can compare SMC3-HA levels between – and + glucosamine for each time point, the levels at 12 hpi cannot be quantitatively compared to those at 24 or 36hpi.
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What time point after glucosamine addition represents the WB in Fig. 3A? __Response: __The “12hpi” parasites were sampled approximately 108 hours post glucosamine addition and the “24hpi” parasites sampled approximately 120 hours post glucosamine addition. Basically, the parasites were treated with glucosamine for 96 hours, synchronized, and then harvested 12 and 24 hours later.
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Line 233 / Suppl Figure 3: Isn't it a bit concerning that the untreated control parasites at 24 hpi statistically corresponded to 18-19 hpi? And to what timepoint did the wt parasites correspond? __Response: __We are not concerned by this, and we have included the WT parasites in what is now Supp. Fig. 5B for better comparison. In the analysis presented in Supp. Fig. 5B, regardless of glucosamine presence or absence, the differences among replicates and strains at 12 and 24hpi are, in our opinion, minimal, amounting to one or two hours of the 48-hour IDC. In our extensive experience with RNA-seq across the P. falciparum lDC, this synchronization is extremely tight. As we describe on line 430 of the Materials and Methods, there is a ±3 hour window in our synchronization method, meaning that parasites harvested at 24hpi could be anywhere from 21-27hpi. In addition, the dataset that was used for comparison (from Bozdech et al., 2003) was generated in 2003 in a different laboratory using different strains with microarray. While comparing more recent RNA-seq data to this classic study has become well-established practice and is useful for comparing transcriptional age between replicates and strains, it is inevitable that the calculated “hpi” from (Bozdech et al., 2003) will differ somewhat from our experimental “hpi”. We have indeed seen this small discrepancy in predicted transcriptional age in several of our RNA-seq datasets (unrelated to this study) from trophozoites harvested at 24hpi.
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Line 264: "whether naturally or via knockdown" - the meaning of this sentence is not entirely clear __Response: __We are referring to depletion of SMC3 at promoters, either naturally (i.e. lack of binding at the promoter at 36hpi that is not the result of SMC3 knockdown, as we show in Fig. 4B) or via SMC3 knockdown, which is not natural but artificial.
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Figure 4 Legend: A, B, C etc. are mixed up. Response: Thank you for pointing this out. We have corrected this.
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Figure 4D: the differences seem to be marginally significant, even not significant at all (q=0.8) for gap45 at 12hpi. __Response: __If one defines a significance cutoff of q = 0.05 (as is common practice in differential expression analyses), then the differences are significant. For a small minority of invasion genes (such as gap45), we do observe significance at either 12 hpi or 24 hpi, but not both. Thus, we have removed the word “significant” from the descriptions of each dataset in Tab 1 of what is now Table 18. however, we do not believe that this rules out a role for SMC3 at such a gene during interphase. What is now Table 18 offers a longer list of invasion-related genes, most of which are more “significantly” affected than rap2 and gap45.
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Figure 4F shows FACS data using SYBR green as a DNA stain. The authors could exploit this data to look at the relative DNA content per cell as a measure of parasite stage, since more mature parasites will have more DNA (mean fluorescence intensity). How did the corresponding parasite cultures look in Giemsa smears? Response: We have repeated our growth curve analysis several times and with more clones and have concluded that there is not a significant growth phenotype in SMC3 KD parasites (see what is now Supp. Fig. 4B). We have added images of Giemsa-stained parasites in untreated and glucosamine-treated parasites at all time points to demonstrate a lack of an obvious morphological phenotype in SMC3 KD parasites (see what is now Supp. Fig. 5A).
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Are RNAseq replicates biological replicates from independent experiments or technical replicates? __Response: __RNA-seq replicates are technical replicates from the same parasite clone.
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Why does the number of genes analysed for differential gene expression differ between the comparisons? __Response: __If the reviewer is referring to the discrepancy between the total number of genes for different time points [for example, between what is now Table 9 (12hpi) and Table 10 (24hpi)], this is because in the RNA-seq/differential expression analysis, there have to be reads mapping back to a gene in order for that gene to be included in the analysis. Thus, if a gene is not transcribed at a given time point in the treated or untreated samples, it will not be included in the analysis. Gene transcription fluctuates significantly over the course of the IDC, so different time points will have different total numbers of transcribed genes.
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Line 372: Do you mean the proteins or the genes? AP2-I has a peak at 24 hpi and 36 hpi, and its interacting AP2 factor Pf3D7_0613800 at all time points. __Response: __We are referring to the genes. With the new ChIP-seq analysis including the second replicate, there are no consensus SMC3 peaks associated with ap2-I, bdp1, or Pf3D7_0613800 (see what is now Table 7).
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Line 480: no aldolase was shown. __Response: __We have removed this sentence.
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Line 838: include GO analysis in methods __Response: __We have added this.
Reviewer #2 (Significance (Required)): The paper addresses the function of the cohesin complex in gene regulation of malaria parasites for the first time. Due to the conserved nature of the complex, the data may be interesting for a broad audience of scientists interested in nuclear biology and cell division/ gene regulation.
Reviewer #3
(Evidence, reproducibility and clarity (Required)):
*Summary:
In the presented manuscript by Rosa et al. the authors investigate the longstanding question of how P. falciparum achieves the tight transcriptional regulation of its genome despite the apparent absence of many canonical sequence specific transcription factor families found in other eukaryotes. To do this the authors investigate the role of the spatial organization of the genome in this context, by performing a functional characterization of the conserved cohesion subunit SMC3 and its putative role in transcriptional regulation in P. falciparum. Using Cas9 mediated genome editing the authors generated a SMC3-3xHA-glmS parasite line, which they subsequently used to show expression of the protein over the asexual replication cycle by western blot and IFA analysis. In addition, using co-IP experiments coupled with mass spectrometry they identified the additional components of the cohesion complex also found in other eukaryotes as interaction partners of SMC3 in the parasite, thereby confirming the presence of the conserved cohesin complex in P. falciparum. By using a combination of ChIP-seq and RNA-seq experiments in SMC3 knockdown parasites the authors furthermore show that a reduction of SMC3 resulted in the up-regulation of a specific set of genes involved in invasion and egress in the early stages of the asexual replication cycle and that this up-regulation in transcription is correlated with a loss of SMC3 enrichment at these genes. From these observations the authors conclude, that SMC3 binds dynamically to a subset of genes and works as a transcriptional repressor, ensuring the timely expression of the bound genes. Overall, the presented data is intriguing, of high quality and very well presented. However, there are some points, which should be addressed to bolster the conclusions drawn by the authors.
Major points: I was not able to find the deposited datasets in the BioProject database under the given accession number. This should obviously be addressed and would have been nice to be able to have a look at these datasets also for the review process. *__Response: __We apologize for not giving the reviewers access. As the manuscript has been made available as a pre-print (which includes data accession numbers), but has not yet been published, we have not activated access to the data on the database.
*SMC3-ChIP-seq experiments:
"168 were bound by SMC3 across all three time points (Fig. 2D). However, most SMC3-bound genes showed a dynamic binding pattern, with a peak present at only one or two time points (Fig. 2B,D)."
Here it would be interesting to actually have more than one replicate of each of these ChIP-seq time points. This could provide a better idea of how "dynamic" these binding patterns actually are. Furthermore, I was missing a list of these 168 genes, which are constantly bound by SMC3. Anything special about those? What actually happens to this subset of genes in the SMC3 knockdown parasites? Do they show similar transcriptional changes?*
__Response: __We have now performed a second biological replicate of the SMC3-3HA ChIP-seq with a different clone at all time points. We compared this data to that from the original clone and found significant overlap of the peaks called (see what is now Table 4 and Supp. Fig. 3A). We generated a stringent list of peaks that were shared between both clones at each time point and repeated all downstream analyses (see what are now Tables 5-8). We found that our conclusions were largely unchanged. Text describing these experiments and analyses have been added throughout the results section. Using the new dataset of consensus peaks between two replicates, there were 88 genes associated with an SMC3 peak across all three time points (see what is now Table 7). The genes that are associated with an SMC3 peak at all time points are, in general, those closest to centromeric/pericentromeric regions and show no obvious functional relationship to each other. Out of these 88 genes, four are significantly up- or downregulated at 12 hpi and 26 are significantly up- or downregulated at 24 hpi. The most significantly downregulated of these genes in both datasets is smc3 itself.
*SMC3-knockdown experiments:
In Sup. Fig. 1 there is a double band in the HA-western blot in the 2nd cycle -GlcN. sample. This second band is absent in all other HA-western shown. Have the authors any idea where that second band comes from?*
__Response: __As the reviewer says, we do not see this second band in most of our western blots. It is possible that it is just a small amount of degradation in the lysate.
In Figure 3A, the WB data shown is slightly contrasting the RNA-seq quantification (3B). The knock-down on protein level seems to be stronger in the 12 hpi samples here than in the 24 hpi samples. Although the band for HA-SMC3 is stronger at the 12 hpi TP there's no band visible in the + GlcN. sample. There's however in the 24 hpi samples. Could the authors comment on this?
Response: __With regard to the discrepancy of the knockdown and protein versus RNA level, it is quite common for transcript levels to not agree with protein levels. This is why we always confirm a transcriptional knockdown with western blot analysis using appropriate loading controls. We are not sure why there is a more dramatic knockdown of SMC3 at 12hpi than at 24hpi, as these samples came from the same culture, but were simply harvested 12 hours apart. __
*"Comparison of our RNA-seq data to the time course transcriptomics data from (Painter et al., 2018) revealed that SMC3 depletion at 12 hpi caused downregulation of genes that normally reach their peak expression in the trophozoite stage (18-30 hpi), with the majority of upregulated genes normally reaching their peak expression in the schizont and very early ring stages (40-2 hpi) (Fig. 3E). At 24 hpi, a similar trend is observed, with most downregulated genes normally peaking in expression in trophozoite stage (24-32 hpi) and the majority of upregulated genes peaking in expression at very early ring stage (2 hpi) (Fig. 3F)."
I'm not fully convinced by these presented results/conclusions. This dataset would greatly benefit from the inclusion of additional later time points.*
__Response: __To be clear, we are most interested in the transcriptional role of SMC3 during interphase, where results are not confounded by its potential role in mitosis. However, we did collect a 36hpi time point in the SMC3-3HA-glmS and WT strain, with and without glucosamine. We have added this last time point and the WT data from the other two time points to the manuscript (see Tables 11-13). Unfortunately, and for reasons unknown, the WT replicates treated with glucosamine showed a significantly advanced “transcriptional age” compared to the other replicates at 36hpi (see what is now Supp. Fig. 5B). Thus, we did not feel comfortable performing the RNA-seq analysis as we did with the other two time points (i.e. subtracting up- and down-regulated genes from the WT control from the SMC3-3HA-glmS data sets). We have added this information to the results section (Lines 256 and 261). As the WT parasites treated with glucosamine were approximately 8 hours in advance of the untreated WT parasites for the 36hpi time point, any up- and down-regulated genes might have been due to differences in the cell cycle rather than due to glucosamine treatment. The glmS system of inducible knockdown is widely used in P. falciparum; however, to our knowledge, no lab has investigated whether glucosamine treatment affects transcription in wildtype cells over the course of the IDC. Thus, for accurate phenotypic characterization of any protein with this system with regard to transcriptomics, we thought it was important to provide an RNA-seq dataset to define the cohort of genes affected by glucosamine treatment in WT parasites. We hope that our study will demonstrate the importance of using stringent controls when using inducible knockdown systems.
We performed differential expression analysis of the SMC3-3HA-glmS parasites with and without glucosamine at 36hpi (we have added this data in Table 11). Again, significantly up- and down-regulated genes were not filtered using the WT dataset. With this analysis, we see only three genes from the list of invasion-related genes (Hu et al., 2010) that are up-regulated, but none of them have a significant q-value (Tab 5 of Table 18). Thus, depletion of SMC3 in late stage parasites does not lead to up-regulation of the same genes that are upregulated at 12 and 24hpi. We have added this information to the text (Line 277).
*The presented upregulation of the egress and invasion related genes is hard to pinpoint to be a direct effect of transcriptional changes due to the SMC3 knockdown. While there's a slight upregulation of these genes they still seem to be regulated in their normal overall transcriptional program as shown in Figure 4D/E. *
__Response: __We provide evidence of a direct effect of SMC3 binding by combining differential expression analysis performed upon SMC3 knockdown with SMC3 ChIP-seq at corresponding time points. As we show in what is now Fig. 4C and D, promoter accessibility of these egress/invasion genes correlates with their transcriptional activity. However, SMC3 binding to the promoters of these same genes shows inverse correlation with their transcriptional activity (what is now Fig. 4B and D). While we believe that SMC3 does contribute to the repression of these genes at specific time points during the cell cycle, it is highly likely that SMC3 is just one protein of many that regulates these genes. Moreover, and especially since we do not see a growth phenotype in the SMC3 KD, it is possible that another protein or even SMC1 could compensate for loss of SMC3 at these promoter regions. We now state these possibilities on lines 346 383 of the Discussion.
*So the changes could in theory also be explained by the differences in cell cycle progression which are present between +/- GlcN. cultures (Sup. Fig. 3). The presented normalization to the microarray data is a well-established practice to correct for this but, as presented seems to have its limitation with these parasite lines (line 233, glucosamine treated parasites harvested at 24 hpi correspond statistically to approximately 18-19 hpi (Supp. Fig. 3).) *
__Response: __In the analysis presented in what is now Supp. Fig. 5B, regardless of glucosamine presence or absence, the differences among replicates and strains at 12 and 24hpi are, in our opinion, minimal, amounting to one or two hours of the 48-hour IDC. In our extensive experience with RNA-seq across the P. falciparum lDC, this synchronization is extremely tight. As we describe on lines 416-421 of the Materials and Methods, there is a ±3 hour window in our synchronization method, meaning that parasites harvested at 24hpi could be anywhere from 21-27hpi. In addition, the dataset that was used for comparison (from Bozdech et al., 2003) was generated in 2003 in a different laboratory using different strains with microarray. While comparing more recent RNA-seq data to this classic study has become well-established practice and is useful for comparing transcriptional age between replicates and strains, it is inevitable that the calculated “hpi” from (Bozdech et al., 2003) will differ somewhat from our experimental “hpi”. We have indeed seen this small discrepancy in predicted transcriptional age in several of our RNA-seq datasets from trophozoites harvested at 24hpi.
By including additional later time points, one could actually follow the expression profiles over the whole cycle and elucidate if there's an actual transcriptional up-regulation of the genes, or if the + GlcN. parasites show a faster cell cycle progression, with a shifted peak expression timing compared to the - GlcN. parasites. __Response: __We did collect a 36hpi time point in the SMC3-3HA-glmS and WT strain, with and without glucosamine. We have added this last time point and the WT data from the other two time points to what is now Supp. Fig. 5. Unfortunately, and for reasons unknown, the WT replicates treated with glucosamine showed a significantly advanced “transcriptional age” compared to the other replicates at 36hpi. Thus, we did not feel comfortable performing the RNA-seq analysis as we did with the other two time points (i.e. subtracting up- and down-regulated genes from the WT control from the SMC3-3HA-glmS data sets). We have added this information to the results section (Lines 256 and 261). As the WT parasites treated with glucosamine were approximately 8 hours in advance of the untreated WT parasites for the 36hpi time point, any up- and down-regulated genes might have been due to differences in the cell cycle rather than due to glucosamine treatment. The glmS system of inducible knockdown is widely used in P. falciparum; however, to our knowledge, no lab has investigated whether glucosamine treatment affects transcription in wildtype cells over the course of the IDC. Thus, for accurate phenotypic characterization of any protein with this system with regard to transcriptomics, we thought it was important to provide an RNA-seq dataset to define the cohort of genes affected by glucosamine treatment in WT parasites. We hope that our study will demonstrate the importance of using stringent controls when using inducible knockdown systems.
*"These genes show SMC3 enrichment at their promoter regions at 12 and 24 hpi, but not at 36 hpi (Fig. 4C), and depletion of SMC3 resulted in upregulation at both 12 and 24 hpi (Fig. 4D). Comparison of the SMC3 ChIP-seq data with published Assay for Transposase-Accessible Chromatin using sequencing (ATAC-seq) data (Toenhake et al., 2018) and mRNA dynamics data (Painter et al., 2018) from similar time points in the IDC revealed that SMC3 binding at the promoter regions of these genes inversely correlates with chromatin accessibility (Fig. 4C) and their mRNA levels (Fig. 4E), which both peak in schizont stages. These data are consistent with a role of SMC3 in repressing this gene subset until their appropriate time of expression in the IDC."
The presented correlations certainly make an intriguing point towards the authors conclusion that SMC3/cohesin depletion from the promoter regions of the genes results in a de-repression of these genes and their transcriptional activation. However, the SMC3 knockdown is not complete and only up to 69% as presented on RNA level in these parasites. Therefore a control experiment which needs to be done is to actually show the loss of SMC3 from the presented activated example genes in the knockdown parasites. This could easily be done by ChIP-qPCR or even ChIP-seq, to get a global picture of the actual changes in SMC3 occupation in the knockdown parasites in correlation with changes in transcript levels. *__Response: __While SMC3-3HA-glmS knockdown is not complete at the RNA level, it is fairly robust at the protein level, especially at 12hpi (Fig. 3A).
*"These data suggest that SMC3 knockdown results in a faster progression through the cell cycle or a higher rate of egress/invasion."
The authors could greatly strengthen their conclusions by investigating this thoroughly. Pinpointing the observed phenotype to an actual increase in invasion or egress would add to the authors main conclusion that the loss of SMC3 de-regulates the timing of gene expression for these invasion related genes thereby increasing their transcript levels and thus leading to a higher rate of egress/invasion. To determine cell cycle progression simple comparisons between DNA content using a flow cytometer at timepoints together with visual inspection of Giemsa stained blood smears would give a ggod indication towards changes in cell cycle progression. In addition invasion/egress assays by counting newly invaded rings per schizont could reveal, if there are changes in the rate of egress/invasion upon SMC3 knockdown.*
Response: __We have repeated our growth curve analysis several times and with more clones and have concluded that there is not a significant growth phenotype in SMC3 KD parasites (see what is now Supp. Fig. 4B). We have added images of Giemsa-stained parasites from the knockdown time course we performed to what is now Supp. Fig. 5A. We see no obvious differences in cell morphology caused by glucosamine treatment in the WT or SMC3-3HA-glmS parasites. As we discuss on line 327, very little intact cohesin complex seems to be required for normal growth and mitosis in S. cerevisiae and D. melanogaster, which is probably why we do not see an obvious growth or morphological phenotype. We believe that SMC3 is probably only a part of a complex controlling transcription of these invasion or egress genes. Thus, the up-regulation of these genes upon SMC3 KD might not be enough to lead to a significant growth or invasion phenotype. __
*Minor points:
In the MM section on the Cas9 experiments it says dCas9 where it should be Cas9 (line 425)*
__Response: __Thank you for pointing this out. We have corrected this.
It would be great to add which HP1 antibody was used in which dilution in the IFAs to the MM section. __Response: __We have added this information to the Materials and Methods section.
In Figure 4C for the gap45 gene there's is some green peak floating around which should not be there. __Response: __Thank you for pointing this out, we have corrected it.
*Reviewer #3 (Significance (Required)):
Significance: The manuscript investigates a very timely topic by trying to uncover new molecular mechanisms of transcriptional regulation in P. falciparum. Investigating the role of the cohesin complex/SMC3 in this context provides valuable new insights to the field. While the first part with the description of the SMC3 cell line and the co-IP experiments largely confirms published data on the existence and composition of the cohesin complex in Plasmodium and its enrichment at the centromeres, the second part is especially intriguing since it investigates the molecular function of SMC3 in more detail. The results pointing to a role of SMC3/cohesin as a transcriptional repressor are of great interest to the field and will open up new concepts for future investigation.*
*Audience: The work is particularly interesting for people interested in gene regulatory processes in Plasmodium and Apicomplexan parasites in general. At the same time it also nicely points towards shared principles of gene regulation to other eukaryotes in relation to the spatial organization of the genome making the work also very interesting for a broader audience with interest in the general principles of gene regulatory processes in eukaryotic organisms.
Expertise: P. falciparum epignetics and chromatin biology / gene regulation / Cas9 gene editing*
CROSS-CONSULTATION COMMENTS
All reviewers agree that the paper addresses an important topic and provides convincing evidence for enrichment of the cohesin component Smc3 at P. falciparum centromers. In contrast, evidence for a function of Smc3 as a transcriptional repressor of genes in the first part of the parasite life cycle is less well supported. All reviewers agree that the statistical significance of the ChIP experiments needs to be impoved by including biological replicates. In addition, the phenotype of the conditional knock-down should be analysed in more detail by clarifying whether faster cell cycle progression or higher invasion rate are responsible for the observed growth adavantage. Inclusion of transcriptional data from a later time point in addition to the presented data for 12 hpi and 24 hpi was also requested by all reviewers. Finally, several inconsistencies require clarification.
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- Aug 2022
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Reply to the reviewers
Reply to the reviewers
- General Statements
It is the common view of all three reviewers that we have not utilized adequate in vitro/biochemical evidence to support the idea that SATB1 protein undergoes liquid-liquid phase separation. We do agree with the reviewers that our manuscript lacks biochemical evidence to support such notion. Though we find it quite interesting and we would like to suggest for the first time in the field of chromatin organization and function, based upon the action of SATB1, that this protein does exist in at least two polypeptide isoforms (764 and 795 amino acids long) which display different phase separation propensity and therefore confer different actions in regulating the (patho)physiological properties of a murine T cell.
Every single research group that works on SATB1, considered so far only a single protein isoform, that is, the shorter isoform of 764 amino acids and no tools, such as isoform-specific antibodies have been developed to discriminate the two isoforms and thus being able to assign unique functions to each isoform. We do understand that such a report, suggesting the presence of two protein isoforms, with potentially quite diverse functions, would question (not necessarily by the authors of this manuscript, since no such comment is included in our manuscript) the conclusions drawn in the literature assigning all biochemical properties to a single, short isoform of SATB1. Moreover, all the genetically modified mice that have been analyzed so far (including our group), deleted both Satb1 isoforms. Our future research approaches should, from now on, consider unraveling the isoform-specific functions of SATB1 and their involvement in physiology and disease. This could also deem useful to explain the quite diverse, both positive and negative effects of SATB1 in transcription regulation. Another major objection of the reviewers was that we should provide cumulative supporting evidence for the existence of the long SATB1 isoform, or at least evaluate the specificity of our custom-made antibody.
Taking under consideration the aforementioned constructive criticism of the three reviewers we would like to perform (most of the suggested experiments have already been performed) additional experiments to support our claims in the manuscript. These experiments are described below as a point-by-point reply to each point raised by the reviewers.
In line with the aforementioned rationale, we propose the title of our manuscript to change into “Two SATB1 isoforms display different phase separation propensity”, if our manuscript is considered for publication.
- Description of the planned revisions
**Reviewer #1**:
4) Lack of in vitro reconstitution experiments with purified long and short SATB1
**PLANNED EXPERIMENT #1**
We do realize this shortcoming of our work. We have to note that purifying recombinant SATB1 protein is quite a challenging task, yet we 1. cloned both Satb1 cDNAs for the long and short isoforms, 2. we successfully expressed both proteins in great quantity and quality and we are willing to perform these experiments if our work is considered for publication.
This proposed experiment has also been requested by Reviewers #2 and #3.
**Reviewer #2**:
- Moreover, an important and direct experiment would be to clone the long isoform in a suitable vector and overexpress in the cell line (as done for the canonical isoform in Supp Fig 1a). This would unequivocally show the efficacy of the antibody and thus the following usage of the same for various assays.
**PLANNED EXPERIMENT #2**
This is a great suggestion. We have cloned the long and short Satb1 cDNAs in pEGFP-C1 vector. We will transfect these plasmids in NIH 3T3 fibroblasts and we will perform Western blot analysis, utilizing the antibody raised against the extra 31 amino acids long peptide present only in the long SATB1 isoform, for the following samples: 1. NIH-3T3 whole cell protein extracts, 2. protein extracts from NIH 3T3 fibroblasts transiently transfected with the pEGFP-C1 plasmid, 3. protein extracts from NIH 3T3 fibroblasts transiently transfected with the pEGFP-long_Satb1_ plasmid and 4. protein extracts from NIH 3T3 fibroblasts transiently transfected with the pEGFP-short_Satb1_ plasmid.
This experiment will consist another proof regarding the specificity of the antibody raised against the extra 31 amino acids long peptide present only in the long SATB1 isoform.
**Minor comments:**
- On pg 6, related to Figure 1, the authors mention 'It should also be noted that when investigating the SATB1 protein levels, we have to bear in mind that the antibodies targeting the N-terminus of SATB1 protein cannot discriminate between the short and long isoforms'. The authors reason that their sizes are too close. It is indeed possible, and widely studied in biochemistry to assess various factors on protein migration (such as PTMs). The authors should validate this aspect (as it is important as per their premise) and perform separation based on charge as well and also use a commercial antibody to validate the same.
(Experiments already performed)
We have adapted the text so that it does not imply that the two isoforms cannot be separated by size. This part in lines 102-107 then reads: “It should also be noted that when investigating the SATB1 protein levels, we have to bear in mind that the antibodies targeting the N-terminus of SATB1 protein cannot discriminate between the short and long isoforms, thus we can only compare the amount of the long SATB1 isoform to the total SATB1 protein levels in vivo conditions. To overcome this limitation and to specifically validate the presence of the long SATB1 protein isoform in primary murine T cells, we designed a serial immunodepletion-based experiment (Fig. 1e, Supplementary Fig. 1a).”
Moreover, in the revised version of the manuscript we now provide a number of additional proofs supporting the presence of the long isoform and also the specificity of the long isoform-specific antibody. As evident in the text cited above, in the revised Fig. 1e,f and revised Supplementary Fig. 1a,b; we present two immunodepletion experiments which should alone address the Reviewer’s concerns. Moreover, we added Supplementary Fig. 1c; demonstrating that the long isoform-specific antibody does not detect any protein in cells with conditionally depleted SATB1 (Satb1_fl/fl_Cd4-Cre+), supporting its specificity. The custom-made and publicly available antibodies targeting all SATB1 isoforms were also verified in Supplementary Fig. 1d. Moreover, the long isoform and all isoform antibodies display similar localization in the nucleus (Supplementary Fig. 1e; their co-localization based on super-resolution microscopy is also quantified in Supplementary Fig. 5a).
In our accompanying revised manuscript Zelenka et al., 2022 (https://doi.org/10.1101/2021.07.09.451769), we will provide yet another piece of evidence, consisting of bacterially expressed short and long SATB1 protein isoforms detected by western blot using either the long isoform-specific or the non-selective all SATB1 isoform antibodies.
**PLANNED EXPERIMENT #3**
Although we think that in the revised version of the manuscript, we have provided enough proof about the existence of the long isoform in primary murine thymocytes we would like to try the following approach as suggested by this Reviewer.
The pI of the two SATB1 isoform is quite similar. The pI of the short SATB1 isoform is 6.09 and for the long SATB1 isoform is 6.18. We will perform 2D PAGE coupled to Western blotting utilizing the antibodies detecting the long and all SATB1 isoforms. Given the fact that both isoforms are post-translationally modified to a various degree, it will be extremely difficult to discriminate between the long and short unmodified versus the long and short post-translationally modified proteins especially in the absence of a specific antibody only for the short isoform.
**Reviewer #3**
- Hexanediol is another assay frequently used in phase-separation studies. However, hexanediol has many deleterious effects on the cell, even at a fraction of the concentration normally used in phase-separation studies. Authors should show controls of cell viability, control proteins that do not phase-separate, etc. See https://www.jbc.org/article/S0021-9258(21)00027-2/fulltext.
Secondly, hexanediol treatment should cause phase-separated protein aggregates to disperse. It is difficult to determine from the images whether or not the aggregates actually disperse or there is just less protein. In any case, small aggregates remain even after treatment, and this appears different from most other hexanediol experiments reported in the literature where the signals become more dispersed and uniform. This is likely because the samples are fixed.
One of the main features of using hexanediol in phase-separation is to show that upon washout, LLPS aggregates can reform. Because the cells are fixed, the critical aspect of this assay is not performed. A washout and LLPS recovery would control for cell viability issues described above and would provide the opportunity to show that total SATB1 protein levels did not change, but its distribution did, which is the essence of this assay in the context of LLPS. This review from the Tjian group is very informative and may be a good resource:
http://genesdev.cshlp.org/content/33/23-24/1619
In line with our reply to point #1 of this Reviewer (page 26 of this document), we should again emphasize that we utilized the hexanediol treatment in primary murine developing T cells as this is the only way to investigate the properties of SATB1 speckles under physiological conditions. This also explains why some small insoluble structure remains after the hexanediol treatment. Note that under physiological conditions, there is a contribution of several protein variants (such as differential PTMs) out of which some will tend to form more stable structures while others could undergo LLPS. It is not clear how the washout experiment could be applied in the primary cell conditions that include cell fixation as the heterogeneity and big variation among cells would make such data analysis highly unreliable.
**PLANNED EXPERIMENT #1**
As we answered to point #4 of Reviewer 1 (page 2), we propose the following experiment. Although the purification of recombinant SATB1 protein is quite a challenging task, yet we 1. cloned both Satb1 cDNAs for the long and short isoforms, 2. we successfully expressed both proteins in great quantity and quality and we are willing to perform in vitro reconstitution experiments if our work is considered for publication.
- The major difference between the long and short isoform of SATB1 is the 31aa segment within the IDR. However the authors find that neither the long or short isoform SATB1 forms LLPS aggregates, and the IDR alone forms aggregates in the cytoplasm (Fig5) but they do not respond to Cry2 light activation. When forced to localize to the nucleus, it does not form aggregates as well (Fig6). The short isoform also did not form any aggregates. These results seem to argue against any isoform specific phase-separation. This experiment seems critical for the story, yet it does not support their overall conclusions. The authors might consider using a different cell line or perhaps do an in vitro assay using purified protein.
I am not certain what to make of the cytoplasmic aggregation, which appears to not form upon localization to the nucleus. Because of this, it is difficult to place weight on the significance of the S635A mutation and the role that a phosphorylation of SATB1 contributes to phase-separation, let alone function There are many additional points of concern, but the ones listed above are perhaps the most significant in terms of the overall conclusions of the paper.
In Fig. 5c we show that the full length long SATB1 isoform often aggregates unlike the short isoform. These data are accompanied with the results for the IDR region, where the situation is even more obvious (Fig. 5f,g). However, in the latter, we have to bear in mind the absence of the multivalent N-terminal part of the protein which seems to be essential for the overall phase behavior of the protein as indicated in Fig. 4b,c.
**PLANNED EXPERIMENT #1**
To further support LLPS of SATB1, we are considering performing the following in vitro experiment, as we answered to point #4 of Reviewer 1 (page 2). Although the purification of recombinant SATB1 protein is quite a challenging task, yet we 1. cloned both Satb1 cDNAs for the long and short isoforms, 2. we successfully expressed both proteins in great quantity and quality and we are willing to perform in vitro reconstitution experiments if our work is considered for publication.
- Description of the revisions that have already been incorporated in the transferred manuscript
**Reviewer #1 (Evidence, reproducibility and clarity)**:
This paper looks at an important nuclear matrix protein SATB1, which is a well known global chromatin organizer and help chromatin loop attach to the nuclear matrix. The paper starts with identification of novel short and long form of SATB1. Both the isoform consist of a prion like low complexity domains, but the long isoform additionally contain an extra EPF domain next the Prion like low complexity domain. The paper reports that in murine cells the long isoform is 3-4 fold more abundant than the short isoform. By using STED microscopy they show SATB1 foci lie next to transcription sites in the nucleus. They conclude by looking at the spherical shape of the SATB1 foci and the susceptibility of SATB1 staining after 1,6 hexanediol treatment that SATB1 forms the small foci in the nucleus due to LLPS. The authors also use RAMAN spectroscopy to conclude a change in nuclear chemical space in absence of SATB1 but without much explanation about which chemical bond or nuclear sub structure change correspond to the change in principal component analysis from Raman spectroscopy. The authors use the light inducible aggregation cry2 tag with the PrD domain of SATB1 and compare it with the Cry2-FUS-LC domain to conclude that the SATB1 LC domain can undergo LLPS. The authors hint at involvement of RNA and also DNA in the LLPS of the SATB1 but without going into any detail. Reviewer: The paper reports that in murine cells the long isoform is 3-4 fold more abundant than the short isoform.
Actually, in page 5 (lines 94-96) of the manuscript we write: “We confirmed that in murine thymocytes the steady state mRNA levels of the short Satb1 transcripts were about 3-5 fold more abundant compared to the steady state mRNA levels of the long Satb1 transcripts (Fig. 1d).” Although the steady state mRNA levels of the long isoform are less abundant compared to the shorter isoforms, the long isoform protein levels are almost comparable to the short isoform as deduced based on immunofluorescence experiments. Moreover, Using our two immunodepletion experiments we quantified the difference, estimating the long isoform being 1.5× to 2.62× less abundant than the short isoform (Fig. 1f and Supplementary Fig. 1b; compare lanes 2 & 3 at the lower panel). • Regarding the RAMAN spectroscopy experiments please see Minor Comment #1 of this Reviewer (page 10).
The key conclusions of the paper are- A) SATB1 undergoes LLPS. But this conclusion is drawn after correlative experiments as detailed below-
This conclusion is indeed made based on correlative experiments only for the primary murine T cells, which do not allow for any targeted experiments. However, the use of in vitro cell lines allowed us to validate these findings using the optogenetic approaches, utilizing additional experimentation.
1) observation of spherical punctae by STED-which could also seem spherical due to their small size. The resolution limit achieved by the STED microscopy used in this paper is not determined or mentioned clearly.
In the revised version of the manuscript, we have specified the resolution of our systems, for STED in Lines 745-746: ”This system enables super-resolution imaging with 35 nm lateral and 130 nm axial resolution.” and for SIM in Lines 759-761: “Images were acquired over the majority of the cell volume in z-dimension with 15 raw images per plane (five phases, three angles), providing ~120-135 nm lateral and ~340-350 nm axial resolution for 488/568 nm lasers, respectively.” The size of the observed speckles is thus above the resolution limit with sizes ranging between 40-80 nm.
The resolution of our systems is routinely verified by the following methods: The resolution of our OMX (SIM-3D) system was tested using ARGO-SIM slide containing a pattern of 36 µm long lines with gradually increasing spacing ranging from (left to right) 0 to 390 nm, with a step of 30 nm (Fig. 1 below). Our SIM system was able to clearly resolve two lines separated by 120 nm.
2) No live cell FRAP experiment with fluorescent SATB1 long or short isoform to show that these foci are liquid like
We did perform FRAP experiments for the SATB1 N-terminus optogenetic construct as demonstrated in Fig. 4f. We did not perform FRAP in the primary murine T cells as this is not technically feasible without creating a new mouse line with fluorescently labeled protein. In the revised version of the manuscript, we additionally performed FRAP experiments for the full length short and long isoform of SATB1 labeled with EGFP and transfected into the NIH-3T3 cell line (Supplementary Figure 6f).
5) LLPS is strongly coupled to the cellular concentration of the proteins. Authors should quantify the cellular concentration of the long and short isoform in the cells.
We did consider protein concentration in our analyses of optogenetic constructs in Fig. 4b,d,e and Supplementary Fig. 6a,b,c. Quantifying the physiological cellular concentration of short and long SATB1 protein isoforms in primary T cells is impossible due to the inherent inability to discriminate between the isoforms by two antibodies, in the absence of Satb1 isoform-specific knockout mice.
However, an approximation of the cellular concentration can be obtained from our immunodepletion experiments. On top of the original immunodepletion experiment that we now present in Supplementary Fig. 1a,b; in the revised version of the manuscript we have repeated the experiment in Fig. 1e,f. Comparison of the two bands for the long and short SATB1 isoforms in the lower panel of the western blot figures suggest that the long SATB1 isoform protein levels are 1.5× to 2.62× less abundant than the short isoform, according to the original and new immunodepletion experiment, respectively. This is now also included in the main text in Lines 110-116: “This experiment can also be used for approximation of the cellular protein levels of SATB1 isoforms in primary murine thymocytes. Comparison of the two bands for long (lane 2) and short SATB1 (lane 3) isoform in the lower panel of Fig. 1f and Supplementary Fig. 1b, suggests that the long SATB1 isoform protein levels may be about 1.5× to 2.62× less abundant than the short isoform, according to the two replicates of our immunodepletion experiment, respectively.”
Major conclusion B)- SATB1 regulates transcription and splicing.
This was also shown previously and in this paper they show the close proximity of the transcription site and SATB1 foci by microscopy. Hexanediol treatment which lead to loss of colocalization between FU foci and SATB1 is also taken as an evidence in regulation of transcription is not right as the transcription foci itself can be dissolved using 1,6 Hexanediol. Although the rate of transcription is not measured quantitatively.
As mentioned in comment #3 (page 29) of this Reviewer, unfortunately there is no better tool to investigate these questions in primary cells than using microscopy approaches in conjunction with hexanediol treatment. However, we should also note that there is an accompanying manuscript from our group that is currently being under revision in another journal (preprint available: Zelenka et al., 2021; https://doi.org/10.1101/2021.07.09.451769). In the preprint manuscript, we showed that: 1. the long SATB1 isoform binding sites have increased chromatin accessibility than what expected by chance (Fig. 3b), 2. there is a drop in chromatin accessibility at SATB1 binding sites in Satb1 cKO mouse (Fig. 3c) and 3. this drop in chromatin accessibility is especially evident at the transcription start sites of genes (Supplementary Fig. 1i)
We believe that, together these data suggest a direct involvement of SATB1 in transcription regulation. Also note the vast transcriptional deregulation that occurs in Satb1 cKO T cells, affecting the expression of nearly 2000 genes (Fig. 2f, this revised manuscript). That is why we believe that the co-localization analysis, using super-resolution microscopy, presented in Fig. 2c and quantified in Fig. 3g, represents a nice additional support to our claims. Moreover, in the revised version of the manuscript we now present a positive correlation between SATB1 binding and deregulation of splicing (Supplementary Fig. 4d) which also supports its direct involvement in the regulation of transcriptional and co-transcriptional processes.
In the revised version of the manuscript we have made this clear in Lines 182-194: “Satb1 cKO animals display severely impaired T cell development associated with largely deregulated transcriptional programs as previously documented19,37,38. In our accompanying manuscript19, we have demonstrated that long SATB1 isoform-specific binding sites (GSE17344619) were associated with increased chromatin accessibility compared to randomly shuffled binding sites (i.e. what expected by chance), with a visible drop in chromatin accessibility in Satb1 cKO. Moreover, the drop in chromatin accessibility was especially evident at the transcription start site of genes, suggesting that the long SATB1 isoform is directly involved in transcriptional regulation. Consistent with these findings and with SATB1’s nuclear localization at sites of active transcription, we identified a vast transcriptional deregulation in Satb1 cKO with 1,641 (922 down-regulated, 719 up-regulated) differentially expressed genes (Fig. 2f). Specific examples of transcriptionally deregulated genes underlying SATB1-dependent regulation are provided in our accompanying manuscript19. Additionally, there were 2,014 genes with altered splicing efficiency (Supplementary Fig. 4d-e; Supplementary File 3-4). We should also note that the extent of splicing deregulation was directly correlated with long SATB1 isoform binding (Supplementary Fig. 4d).”
Major conclusion C)-Post transcriptional modification is important for SATB1 function.
This point is just barely touched upon in the last figure of the paper
We would not call the identification of the novel phosphorylation site as a main conclusion of our manuscript. Though, it is already known that posttranslational modifications of SATB1 are important for its function as they can function as a molecular switch rendering SATB1 into either an activator or a repressor (Kumar et al., 2006; https://doi.org/10.1016/j.molcel.2006.03.010).
In the revised manuscript, we support the effect of serine phosphorylation on the DNA binding capacity of SATB1 by another experiment. We have performed DNA affinity purification experiments utilizing primary thymocyte nuclear extracts treated with phosphatase (Supplementary Fig. 7b). We found that SATB1’s capacity to bind DNA (RHS6 hypersensitive site of the TH2 LCR) is lost upon treatment with phosphatase (Supplementary Fig. 7c). These results are in line with the data presented in Supplementary Fig. 7d, indicating the lost ability of SATB1 to bind DNA upon mutating the discovered phosphorylation site S635. Given the importance of posttranslational modifications of proteins on LLPS, we found it relevant to include it in our manuscript. Even more so, when we identified SATB1 aggregation, upon mutation of this phospho site (Fig. 6d).
Overall I find that the major conclusion-point A and B, is based on very indirect experiments and needs much more convincing data and the role of SATB1 LLPS in cells should be demonstrated more rigorously. And conclusion C is barely described and needs a lot more cell biological and genetic evidence.
One of the major assets of our work is that most of our data are based on the analysis of primary murine T cells and thus investigating the biological roles of the endogenous SATB1 protein, under physiological conditions. We apologize that we did not make it clear to this Reviewer, that our system has certain inherent limitations due to the utilization of primary cells.
I do not recommend publishing the paper in current state. The story needs much more experiment to convincingly prove the major conclusions. Further, the MS needs more careful thinking and presentation to make it streamlined.
We hope that in the revised version we have significantly improved the quality of our manuscript by implementing the suggested changes.
Minor comments: One of the major flaw of the paper is the use too many techniques without proper explanation. E.g. use of STED and RAMAN microscopy need controls and explanation on what is being quantified. The use of Raman microscopy to quantify the nuclear environment of nucleus is not related to the chromatin organization or LLPS of SATB1 at all. And no information is provided at all which aspect of nuclear organization is being measured in Raman and what it means for the LLPS of SATB1.
We do provide quite a thorough explanation of Raman spectroscopy and the underlying quantification in Lines 224-231: “we employed Raman spectroscopy, a non-invasive label-free approach, which is able to detect changes in chemical bonding. Raman spectroscopy was already used in many biological studies, such as to predict global transcriptomic profiles from living cells42, and also in research of protein LLPS and aggregation43–47. Thus we reasoned that it may also be used to study phase separation in primary T cells. We measured Raman spectra in primary thymocytes derived from both WT and Satb1 cKO animals and compared them with spectra from cells upon 1,6-hexanediol treatment. Principal component analysis of the resulting Raman spectra clustered the treated and non-treated Satb1 cKO cells together, while the WT cells clustered separately (Fig. 3h).” We also do provide controls as the method was performed on both treated and untreated WT and Satb1 cKO cells.
Regarding the RAMAN spectroscopy experiments we now provide more information on the changes of chemical bonds altered between wild type and Satb1 cKO thymocytes. Following principal component analysis, we have extracted the two main principal components that were used for the clustering of our data. The differences are presented in Supplementary Fig. 5d.
We do realize that RAMAN spectroscopy, although a quite novel approach utilized to study LLPS, has not been used to study LLPS in live cells. If deemed proper we are willing to avoid presenting these results in this manuscript.
Similarly for Hexanediol treatment, duration of treatment is missing. Hexanediol can also dissolve the liquid like transcription foci. And hence a decrease in correlation between SATB1 foci and FU foci cannot be taken as a measure of SATB1 foci connection to transcription alone
The duration of hexanediol treatment was 5 minutes as presented in Line 724 and in the revised version of the manuscript also in Lines 1206-1207. We should also note that additionally, we performed experiments with different hexanediol concentrations and timing varying from 1 minute to 10 minutes with results consistent with the data presented.
It is not very clear how many times the STED or Raman microscopy is done on how many samples and biological replicates. Similarly for RNA sequencing number of samples and description of controls are missing. Also if the sequencing data is made publicly available is not clear.
Data availability is clearly stated in Lines 506-509: “RNA-seq experiments and SATB1 binding sites are deposited in Gene Expression Omnibus database under accession number GSE173470 and GSE173446, respectively. The other datasets generated and/or analyzed during the current study are available upon request.”
The Reviewer’s token is “wjwtmeeeppovzqx”.
RNA sequencing was performed in a biological triplicate for each genotype as stated in the GEO repository and now also in Line 566 of the revised manuscript.
In Lines 180-181, we also state that it was performed on Satb1 cKO animals and WT mice as a control: “we performed stranded-total-RNA-seq experiments in wild type (WT) and Satb1fl/flCd4-Cre+ (Satb1 cKO) murine thymocytes”.
In Lines 739-740, we now also state that all imaging approaches were performed on at least two biological replicates (different mice) and please also note the fact that all findings were based on data from both STED and 3D-SIM methods, allowing to minimize detection of artifacts. In the Raman spectroscopy figure, each point represents measurements from an individual cell and for each condition we used 2-5 biological replicates (Lines 831-832 & Line 1169).
Similarly, in Lines 129-132 we provided a quite detailed description of differences between STED and 3D-SIM, even though these techniques are not that rare as Raman spectroscopy in biology research.
Additional control is needed to report the resolution limit of Superresolution techniques-STED and 3D-SIM systems used by them.
We have already provided this information in our reply to comment #1 of this Reviewer (pages 6-7): In the revised version of the manuscript, we have specified the resolution of our systems, for STED in Lines 745-746: ”This system enables super-resolution imaging with 35 nm lateral and 130 nm axial resolution.” and for SIM in Lines 759-761: “Images were acquired over the majority of the cell volume in z-dimension with 15 raw images per plane (five phases, three angles), providing ~120-135 nm lateral and ~340-350 nm axial resolution for 488/568 nm lasers, respectively.” The resolution of our systems is routinely verified by the following methods: The resolution of our OMX (SIM-3D) system was tested using ARGO-SIM slide containing a pattern of 36 µm long lines with gradually increasing spacing ranging from (left to right) 0 to 390 nm, with a step of 30 nm (Fig. 1 below). Our SIM system was able to clearly resolve two lines separated by 120 nm.
Would be very helpful if the zonation was plotted for the FluoroUridine (FU) also to show that Zone1 (heterochromatin) is completely depleted of FU, and is present in other regions.
In the revised version of the manuscript, we performed the suggested analysis and in Supplementary Fig. 3a we now show that indeed FU is significantly less localized to Zone 1 (heterochromatin) and has the most abundant localization in Zones 3 and 4, similar to the localization of SATB1 protein, as demonstrated in Fig. 2b.
Scale bar needed figure 3d
In the revised version of the manuscript, we included scale bars which are both 0.5 µm (line 1213).
Perfectly rounded SATB1 foci- this does not mean LLPS. For LLPs measurement, protein condensate dynamics measurement by FRAP or fusion experiments is required. What is the size of condensates? and cellular concentration of SATB1? Will SATB1 undergo LLPS in vitro at similar concentrations? does SATB1 interact with DNA or RNA to undergo LLPS ?
We toned down this sentence which now reads: “Here we demonstrated its connection to transcription and found that it forms spherical speckles (Fig. 1g), markedly resembling phase separated transcriptional condensates. (Lines 200-202)”.
Moreover, as explained in earlier replies to comments of this Reviewer, we cannot perform FRAP on primary murine T cells without generating a new mouse line. We did, however, use FRAP and other in vitro approaches including visualization of droplet fusion in ex vivo experiments utilizing cell lines. Moreover, we are willing to demonstrate the LLPS properties of SATB1 on in vitro purified SATB1 protein as indicated in the suggested experiment of Point#4 (page 2).
After careful reading of the MS I conclude that the main conclusions of the paper are very preliminary and need much more detailed experiments. So does not qualify to get published at all at this stage.
**Reviewer #1 (Significance)**:
The present manuscript tries to connect the phase separation of SATB1 to understanding the mechanism of SATB1 function in cells. One of the major hallmarks of phase separation is dynamic, liquid-like behaviour and in absence of these measurements, it is very difficult to say that the current manuscript has made any contribution to showing that SATB1 can phase separate.
The presence of 2 isoforms of SATB1 is a novel finding and the paper could have focused more on this. E.g. elucidate expression of the isoform during thymocyte development and maturation.
As a reviewer my expertise are cell biology experiments, microscopy, in vitro reconstitution assays, RNA binding proteins, RNA and RBP condensate formation. And I feel that the reconstitution experiments are an important tool for understanding phase behaviour of proteins and also to gauge if this behaviour can occur or not in cellular concentration and conditions.
I do not have sufficient expertise in Raman microscopy and hence the information provided in the MS on this part was not enough to understand the experiment and conclusions drawn from it.
**Reviewer #2 (Evidence, reproducibility and clarity)**:
The authors have reported the existence of a 'long' SATB1 isoform which also undergoes LLPS. The authors tried to draw multiple comparisons and pointed out distinction between phase properties of SATB1 isoforms. The authors also touch upon two functional roles of SATB1. Although a wide array of assays are used, the data presented and hence the manuscript makes multiple transitions into disparate hypotheses without diving deep into a single hypothesis. As a result, the connections drawn are unclear, and do not converge at best. The authors have used number of techniques, however, the results do not support their conclusions and they appear hastily drawn. It is not clear why the authors jump from one context to the other, discussing LLPS first, then transcription, splicing, post-translational modification and finally cancer. The link between all of these isn't clear and not fully supported by data. It appears that the authors wish to focus on Satb1's physiological role in development, hence the data on breast cancer is confusing. Thus, this work suffers from multiple pitfalls. Specific comments are given below:
Major comments 1. Importantly, in Fig 1d, there is no statistics shown. There is no mention of number of replicates as well in the legends. Proper statistical evaluation is critical for interpreting this result.
Please note that Fig. 1d only serves as a control to the sequencing experiment in Fig. 1b. In Line 566, we now state that for the RNA-seq: “A biological triplicate was used for each genotype.” To validate these data, we further designed a RT-qPCR experiment which was performed on three technical replicates from a male and female mouse. We now state this in Line 636. For the low number of samples, statistical tests are not accurate but we still added t test into the figure Fig. 1d and specified it also in the figure legend in Line 1169-1170.
- Figure 1f presents one of the weakest evidences in the manuscript. There are a number of corrections needed. Firstly, being their major and only validation figure for their custom antibody, the immunoblot is not clean, bands are fuzzy. Importantly, as the authors claim that the antibody is highly specific to 'long' SATB1, after the IP there should be only a single band (like input) of Satb1 long. But that does not seem to be the case, rather an array of bands are visible below (lane 2 top panel). This could easily mean that the shorter isoforms or non-specific protein bands are also pulled down with the 'long' form specific antibody. Therefore, raising a critical concern regarding the specificity of the antibody.
• The long antibody was raised in mice inoculated with the extra peptide present in the long isoform only. Therefore, the capacity of this antibody precipitating the shorter isoforms, which do not express the sequence of the extra peptide (EP, Figure 1a) in not possible. • We have repeated the immunodepletion experiment and we now provide the results in Fig. 1f and Supplementary Fig. 1b. The western blot in Fig. 1f is now cleaner and supports quite convincingly the presence of a long SATB1 isoform. Given the lack of isoform-specific knockouts which we could utilize to immunoprecipitate or detect the different isoforms in a single cell (or cell population), the utilized approach of immunodepletion and subsequent western blotting is the approach we thought of implementing. • As shown in Fig. 1f and Supplementary Figure 1b, the long isoform SATB1 antibody has the capacity to recognize the long isoform in murine thymocyte protein extracts but not the short SATB1 isoform (please compare lane 3 in the two western blots utilizing either the antibody for the long isoform -top panel - or the antibody that detects both isoforms (lower panel). • We have performed Immunofluorescence experiments utilizing the antibody detecting the long SATB1 isoform in thymocytes isolated from either C57BL/6 or Satb1 cKO mice. The antibody is specific to the SATB1 protein since there is no signal in immunofluorescence experiments utilizing the knockout cells (Supplementary Figure 1c). • We have performed Immunofluorescence experiments utilizing thymocytes and the antibody detecting the long SATB1 or a commercially available antibody detecting all SATB1 isoforms. The pattern of SATB1 subnuclear localization is similar for both antibodies (Supplementary Figure 1e). • In our accompanying revised manuscript Zelenka et al., 2022 (https://doi.org/10.1101/2021.07.09.451769), we provide yet another piece of evidence, consisting of bacterially expressed short and long SATB1 protein isoforms detected by western blot using either the long isoform-specific or the non-selective all SATB1 isoforms antibodies. • Regarding the additional bands detected in the immunoprecipitation experiment presented in the original Supplementary Figure 1b (lane 2), it is not surprising that additional bands appear in a sample of protein extracts that is used for several hours for the immunoprecipitation experiments, while the “input” sample simply denotes protein extract that is frozen at -80oC right after the preparation of protein extracts until use. It is well-established that SATB1 is the target of proteases which might as well be active during the immunoprecipitation steps (2 consecutive immunoprecipitation steps take place). Therefore, the immunoprecipitated material cannot necessarily be a copy of the input material displaying a single protein band even if protease inhibitors are included in the buffers.
Taken together the experiments described here we showed that the antibody raised against the extra 31 aa long peptide, present only in the long SATB1 isoform, is specific for this isoform.
- Related to Fig. 2 a, the authors state on Pg 5, '....the euchromatin and interchromatin regions (zones 3 & 4, Fig. 2a, b).' Although the DAPI correlation seems clear, there is no mention on how they reached the above said correlation. They should at least show a parallel speckle staining for HP1 or signature modification such as H3K4me9 STEDs for making supporting such a claim. DAPI alone is not sufficient. The authors should rectify the text thoroughly for many such interpretations without validation/reference or provide relevant data.
This is a great suggestion we have again taken under consideration and we added the following experiments and the appropriate changes in the revised version of our manuscript. • We modified the text and added a reference to Miron et al., 2020 (https://doi.org/10.1126/sciadv.aba8811) supporting our claims regarding SATB1 localization in relation to DAPI staining. • We have also added new microscopy images for HP1, H3K4me3 and fibrillarin staining and quantified the localization of FU-stained sites of active transcription in nuclear zones, to further support our claims. • This whole modified part in Lines 139-167 then reads: “ “The quantification of SATB1 speckles in four nuclear zones, derived based on the relative intensity of DAPI staining, highlighted the localization of SATB1 mainly to the regions with medium to low DAPI staining (zones 3 & 4, Fig. 2a, b). A similar distribution of the SATB1 signal could also be seen from the fluorocytogram of the pixel-based colocalization analysis between the SATB1 and DAPI signals (Supplementary Fig. 2a). SATB1’s preference to localize outside heterochromatin regions was supported by its negative correlation with HP1β staining (Supplementary Fig. 2b). Localization of SATB1 speckles detected by antibodies targeting all SATB1 isoforms and/or only the long SATB1 isoform, revealed a significant difference in the heterochromatin areas (zone 1, Fig. 2b), where the long isoform was less frequently present (see also Fig. 2a and Fig. 3c). Although, this could indicate a potential difference in localization between the two isoforms, due to the inherent difficulty to distinguish the two based on antibody staining, we refrain to draw any conclusions. The prevailing localization of SATB1 corresponded with the localization of RNA-associated and nuclear scaffold factors, architectural proteins such as CTCF and cohesin, and generally features associated with euchromatin and active transcription32. This was also supported by colocalization of SATB1 with H3K4me3 histone mark (Supplementary Fig. 2c), which is known to be associated with transcriptionally active/poised chromatin. Given the localization of SATB1 to the nuclear zones with estimated transcriptional activity32 (Fig. 2b, zone 3), we investigated the potential association between SATB1 and transcription. We unraveled the localization of SATB1 isoforms and the sites of active transcription labeled with 5-fluorouridine. Sites of active transcription displayed a significant enrichment in the nuclear zones 3 & 4 (Supplementary Fig. 3a), similar to SATB1. As detected by fibrillarin staining, SATB1 also colocalized with nucleoli which are associated with active transcription and RNA presence (Supplementary Fig. 3b). Moreover, we found that the SATB1 signal was found in close proximity to nascent transcripts as detected by the STED microscopy (Fig. 2c). Similarly, the 3D-SIM approach indicated that even SATB1 speckles that appeared not to be in proximity with FU-labeled sites in one z-stack, were found in proximity in another z-stack (Supplementary Fig. 3c). Additionally, a pixel-based colocalization of SATB1 and sites of active transcription is quantified later in the text in Fig. 3g, supporting their colocalization.”
- The authors mention, '...of the different SATB1 isoforms, uncovered by the use of the two different antibodies, relied in the heterochromatin areas (zone 1), where the long isoform was less frequently...' There is no supporting figure number mentioned. The authors need to show a zone-by-zone comparison images for 'all iso' vs 'long' iso of SATB1. Just to reiterate, there is a need for a heterochromatin mark to unambiguously call out the distinction.
We should remind that there is an inherent difficulty to accurately compare localization of short and long SATB1 isoforms in primary cells, especially due to the lack of Satb1 isoform-specific knockout mice. There is no way to detect only the short isoform in these primary cells as there are only antibodies targeting the long or all SATB1 isoforms. Therefore, we cannot set up additional experiments probing these questions.
In line with this, in the revised version of the manuscript, we toned down our statements regarding the differential localization of the two isoforms in primary cells. We only refer to it as an indication and we support it by adding references to the relevant figures. This part now reads: “Localization of SATB1 speckles detected by antibodies targeting all SATB1 isoforms and/or only the long SATB1 isoform, revealed a significant difference in the heterochromatin areas (zone 1, Fig. 2b), where the long isoform was less frequently present (see also Fig. 2a and Fig. 3c). Although, this could indicate a potential difference in localization between the two isoforms, due to the inherent difficulty to distinguish the two based on antibody staining, we refrain to draw any conclusions. (Lines 145-150)”
- On the same lines, '....Given the localization of SATB1 to the nuclear zones with estimated transcriptional activity (Fig. 2b, zone 3)....' How was the region labelled as transcriptionally active? For the statistical analysis of speckle count for the two antibodies' staining, the claim posited is a bit bigger. This could simply be true for that cell. The authors thus need to statistically analyse the speckle counts for multiple cells. This needs to be done for all imaging statistics done in multiple figures throughout the manuscript.
As mentioned in our reply to the two previous comments of this Reviewer, transcriptional activity in relation to the nuclear zonation is well established in the literature. To make this clear, we have now added the reference to Miron et al., 2020 (https://doi.org/10.1126/sciadv.aba8811) supporting our claims and additionally we have also included HP1, H3K4me3 and fibrillarin staining and quantification of FU signal in the nuclear zones. Moreover, it is not clear to which particular cell the comment refers to. The presented dots in Fig. 2b represent individual cells and the relative proportions of speckles in each nuclear zone are plotted on the y axis. In the revised version of the manuscript, we added into the figure the number of cells scored and we adapted the figure legend so that it is absolutely clear that we have analyzed multiple cells:
“Nuclei of primary murine thymocytes were categorized into four zones based on the intensity of DAPI staining and SATB1 speckles in each zone were counted. Images used represented a middle z-stack from the 3D-SIM experiments. The graph depicts the differences between the long and all SATB1 isoforms’ zonal localization in nuclei of primary murine thymocytes. (Lines 1189-1193)”
- For figure 2c. the authors have used 5 Fluorouridine for nascent RNA speckles. 5FU is known to have a spread signal type (with strong association to nucleolus as well). This is not the case for the image presented 2c. The authors should resolve this by showing different sets of images.
Developing and naive T cells are very unique in terms of their metabolic features and thus they should not be directly compared with other cell types. Therefore, we would not expect to see such a spread FU pattern as previously shown for other cell types. Having said that, we could not find any reference publication that utilized super-resolution microscopy to detect localization of FU-stained sites of active transcription in developing primary T cells. However, we performed additional immunofluorescence experiments to demonstrate the colocalization or its lack between SATB1 and HP1 (Supplementary Fig. 2b), H3K4me3 (Supplementary Fig. 2c) and fibrillarin (Supplementary Fig. 3b). Moreover, we provide additional regions of SATB1 and FU staining in Supplementary Fig. 3c. The modified text reads:
“We unraveled the localization of SATB1 isoforms and the sites of active transcription labeled with 5-fluorouridine. Sites of active transcription displayed a significant enrichment in the nuclear zones 3 & 4 (Supplementary Fig. 3a), similar to SATB1. As detected by fibrillarin staining, SATB1 also colocalized with nucleoli which are associated with active transcription and RNA presence (Supplementary Fig. 3b). Moreover, we found that the SATB1 signal was found in close proximity to nascent transcripts as detected by the STED microscopy (Fig. 2c). Similarly, the 3D-SIM approach indicated that even SATB1 speckles that appeared not to be in proximity with FU-labeled sites in one z-stack, were found in proximity in another z-stack (Supplementary Fig. 3c). Additionally, a pixel-based colocalization of SATB1 and sites of active transcription is quantified later in the text in Fig. 3g, supporting their colocalization. (Lines 157-167)”
- Fig 2 d., the authors have suddenly jumped solely to 'all iso' Satb1 here for IP MS. Is there a reason for that? The authors either need to do this with 'long iso' antibody or remove the analysis from the manuscript as it does not add to their primary aim of the manuscript. Also, the authors have only selectively talked about two clusters? What about chromatin related proteins? It is quite intuitive to have highest enrichment of these given previous literature and even IP MS data by other groups. Thus, it is necessary to revise this thoroughly or remove it.
We appreciate the acknowledgment by the Reviewer that our IP-MS data identified anticipated factors. In the revised version of the manuscript we modified the underlying text to accommodate references to these former findings revealing interactions between SATB1 and chromatin modifying complexes: “Apart from subunits of chromatin modifying complexes that were also detected in previous reports25,33–36, unbiased k-means clustering of the significantly enriched SATB1 interactors revealed two major clusters consisting mostly of proteins involved in transcription (blue cluster 1; Fig. 2d and Supplementary Fig. 4c) and splicing (yellow cluster 2; Fig. 2d and Supplementary Fig. 4c). (Lines 170-174)”
Please note that many subunits of chromatin modifying and chromatin-related complexes are in fact characterized as transcription-related factors, therefore our statements are not in disagreement with the former findings. Note also that we provide Supplementary File 1 & 2 with comprehensive description of our IP-MS data for the readers’ convenience. Please also note that we are the first group to report on the existence of the long isoform. Therefore, we find it absolutely reasonable to perform IP-MS experiment for all SATB1 isoforms which can then be used for a comparison with other publicly available datasets. We believe that there is no contradiction in this experimental setup in relation to the rest of the manuscript. We discuss the two major clusters simply because they are the two major clusters identified as indicated in Fig. 2d. Additionally, in Supplementary Fig. 4c, we provide a comprehensive description of all significantly enriched interactors including their cluster annotation and thus anyone can investigate the data if needed.
- In relation to Fig. 2f, the authors have not mentioned any of the previously published work on Satb1 CD4 specific KO, not even the RNA seq studies the other groups have reported under the same condition. Only an unpublished reference of their own (preprint) is cited. It is imperative to show how much their data corroborates with other published studies. Additionally, what is the binding site status of dysregulated genes?
In the revised version of the manuscript, we have included the references to other studies using the same Satb1 conditional knockout. Moreover, we have clarified the relationship between SATB1 binding and gene transcription. The modified part in Lines 182-194 now reads: “Satb1 cKO animals display severely impaired T cell development associated with largely deregulated transcriptional programs as previously documented19,37,38. In our accompanying manuscript19, we have demonstrated that long SATB1 isoform specific binding sites (GSE17344619) were associated with increased chromatin accessibility compared to randomly shuffled binding sites (i.e. what expected by chance), with a visible drop in chromatin accessibility in Satb1 cKO. Moreover, the drop in chromatin accessibility was especially evident at the transcription start site of genes, suggesting that the long SATB1 isoform is directly involved in transcriptional regulation. Consistent with these findings and with SATB1’s nuclear localization at sites of active transcription, we identified a vast transcriptional deregulation in Satb1 cKO with 1,641 (922 down-regulated, 719 up-regulated) differentially expressed genes (Fig. 2f). Specific examples of transcriptionally deregulated genes underlying SATB1-dependent regulation are provided in our accompanying manuscript19. Additionally, there were 2,014 genes with altered splicing efficiency (Supplementary Fig. 4d-e; Supplementary File 3-4). We should also note that the extent of splicing deregulation was directly correlated with long SATB1 isoform binding (Supplementary Fig. 4d).”
- In context of Figure 3a and b, the authors write .'...The long SATB1 isoform speckles evinced such sensitivity as demonstrated by a titration series with increasing concentrations of 1,6-hexanediol treatment followed...' Whereas it is apparent from the image at least that overall numbers of individual speckles are instead increased at both 2 and 5%. There is although a clear spreading of restricted speckles compared to the controls. The authors should revise their figures to substantiate the associated text. Furthermore, there needs to be 'all iso' SATB1 3D SIM imaging and not just quantitation for comparison. This is also true for panel c in order to demonstrate the effect.
In the revised Fig. 3a we provide new images which better reflect the underlying data analysis. Moreover, in Fig. 3c and Fig. 3d we provide an additional comparison between SATB1 all isoforms and long isoform staining and their changes upon hexanediol treatment, detected by both the 3D-SIM and STED approaches. It is true that upon treatment, there tend to be more speckles, however these are much smaller as they are gradually being dissolved. Depending on the treatment duration, the cells are swollen which is reflected in increased spreading of speckles. Nevertheless, the nuclear size was considered in all the quantification analyses. We believe that the new images provide better evidence of SATB1’s sensitivity to hexanediol treatment.
- Fig. 3 d also does not clearly demonstrate what the authors have claimed '...hexanediol treatment highly decreased colocalization between...' The figure shows at best decreased signal intensity for both SATB1 and FU. We suggest that the authors should give a statistical analysis as well for the colocalization points between the two using multiple source images. Lastly, the two images shown (control and treated), there seems to be a clearly visible magnification difference. The authors should clarify this.
• In the revised version of the manuscript in Figure 3d, we have provided scale bars, which are both 0.5 µm (line 1213). The difference observed by this Reviewer is actually the main reason why we provided this image. Figure 3d demonstrates that upon hexanediol treatment, the speckles are mostly missing or significantly reduced in size, for both FU and SATB1 staining. • Moreover, the suggested statistical analysis is also provided – in Figure 3e. In Figure 3e, we performed pixel-based colocalization analysis which is a method that allows both quantification and statistical comparison of colocalization between two factors and between different conditions. Please note especially the decreased colocalization between long SATB1 isoform and FU-stained sites of active transcription in the left graph, which is in agreement with our claims in the manuscript. • Moreover, our data are compared to a negative control, i.e. 90 degrees rotated samples, which is a common method in colocalization experiments as described for example in Dunn et al., 2011 (https://doi.org/10.1152/ajpcell.00462.2010). • Additionally, we provide Costes’ P values which are based on randomly scrambling the blocks of pixels (instead of individual pixels, because each pixel’s intensity is correlated with its neighboring pixels) in one image, and then measuring the correlation of this image with the other (unscrambled) image. Please see Costes et al., 2004 (https://doi.org/10.1529%2Fbiophysj.103.038422) for more details.
- Figure 3f. The authors show the PC plot for Raman spectroscopy for phase behaviour due to Satb1. The experiment and its related text seems misinterpreted; the authors write...' ese bonds were probably enriched for weak interactions responsible for LLPS that are susceptible to hexanediol treatment. This shifted the cluster of WT treated cells towards the Satb1 cKO cells. However, the remaining covalent bonds differentiated the WT samples from Satb1 cKO cells......' whereas the clusters are clearly far away in 3D for both WT and KO while being closer to their respective treatments. Which is also intuitive given the sensitivity of Raman spectroscopy. Thus, it is more likely to be treatment effect and KO effect as separate. Treatment of WT leads to KO like spectra is far-fetched. Thus, the authors need to show separate PCs and modify their text thoroughly.
We do not present any 3D graph hence it is not clear what the Reviewer refers to. Please also note that as stated in Lines 817-818, we used a customized Raman Spectrometer. Therefore, this approach allowed us to measure Raman spectra at cellular and even sub-cellular levels. For example, solely by utilizing Raman spectroscopy, we can now distinguish euchromatin and heterochromatin, methylated and unmethylated DNA and RNA, etc. This, together with other reports, such as Kobayashi-Kirschvink et al., 2018 (https://doi.org/10.1016/j.cels.2018.05.015) and Kobayashi-Kirschvink et al., 2022 (https://doi.org/10.1101/2021.11.30.470655), indicate a potential use of Raman in biological research. In our manuscript, we used this method as a supplementary approach, however we do find it noteworthy. We should also emphasize that in the revised Raman spectroscopy Fig. 3h, each point represents measurements from an individual cell and for each condition we used 2-5 biological replicates (Lines 831-832 & Lines 1225-1226). We specifically refer to the principal component 1 (PC1) that differentiates the samples. Therefore, there are certain spectra (representing certain chemical bonding) that allowed us to differentiate between WT and Satb1 cKO. The same type of bonding was then affected when WT samples were treated with hexanediol and we also had controls to rule out the impact of hexanediol on the resulting spectra.
- In Fig 4. b, The authors have shown the propensity of SATB1 N terminus to phase separate using different optodroplet constructs. Although the imaging is clear, why are the regions selected not uniform when comparing various constructs?
We have selected images that would best represent each category. Please note that this was live cell imaging of photo-responsive constructs, thus there are many limitations regarding the area selection. Very often, even the brief time of bright light exposure to localize cells may trigger protein clustering. Upon disassembly, every new light exposure of the same cell then triggers much faster assembly which skews the overall results. It is therefore desired to work fast, while neglecting selection of equally sized cells. Moreover, it is not clear how would the proposed change improve the quality of our manuscript.
- Figure 5a, the disassembly should be shown for 'long' SATB1 as well. On pg 13, the authors write '....cytoplasmic protein aggregation has been previously described for proteins containing poly-Q domains and PrLDs..' no reference given.
• In the revised version of the manuscript, we present the assembly and disassembly for both short and long full length SATB1 optogenetic constructs. To increase clarity, we present the behavior of the short and long isoforms as two separate images in Figure 5a and Figure 5b, respectively. • Moreover, we provided references to the statement regarding aggregation of PrLD and poly-Q-containing proteins in Lines 305-309, which now reads: ”Since protein aggregation has been previously described for proteins containing poly-Q domains and PrLDs8,11,38,39, we next generated truncated SATB1 constructs encoding two of its IDR regions, the PrLD and poly-Q domain and in the case of the long SATB1 isoform also the extra peptide neighboring the poly-Q domain (Fig. 1a and 4a).”
- Fig. 5d, Is there an amino-acid specific reasoning to support the authors claim of the phase behaviour due to extra peptide? They need to show a proper control with equal extra (unrelated) peptide to show the specificity. Are the shorter isoform aggregates responsive to light?
• We have referred to the amino acid composition bias in Fig. 5c. In the revised version of the manuscript, we made this clear by showing the composition bias in the new revised Fig. 5e. The related part of the main text then reads: “Computational analysis, using the algorithm catGRANULE37, of the protein sequence for both murine SATB1 isoforms indicated a higher propensity of the long SATB1 isoform to undergo LLPS with a propensity score of 0.390, compared to 0.379 for the short isoform (Fig. 5d). This difference was dependent on the extra peptide of the long isoform. Out of the 31 amino acids comprising the murine extra peptide, there are six prolines, five serines and three glycines – all of which contribute to the low complexity of the peptide region3 (Fig. 5e).” (Lines 298-304) • Moreover, we should note that the low complexity extra peptide of the long SATB1 isoform directly extends the PrLD and IDR regions as indicated in Fig. 4a and which we now directly state in Lines 304-305: “Moreover, the extra peptide of the long SATB1 isoform directly extends the PrLD and IDR regions as indicated in the Fig. 4a.” • We show in Fig. 4, that the N terminus of SATB1 undergoes LLPS. Since this part of SATB1 is shared by both isoforms, it is reasonable to assume that both isoforms would undergo LLPS. This is also in line with the observed photo-responsiveness of both short and long full length SATB1 isoforms in CRY2 optogenetic constructs in revised Fig. 5a,b, and similar FRAP results for both short and long full length SATB1 isoform constructs transiently transfected in NIH-3T3 cells in the revised Supplementary Fig. 6f. However, the main reason why we think that the difference in LLPS propensity between the isoforms is important is because the long isoform is more prone to aggregate compared to the short isoform, as documented in Fig 5c,f,g and Supplementary Fig. 5f.
- Fig 6c., It is important that authors show the data for NLS+short iso data as well to prove their hypothesis.
As shown in original Figure 5d, the long SATB1 isoform undergoes cytoplasmic aggregation, unlike the short SATB1 isoform (as shown in the same Figure). Therefore, an image of the NLS + short isoform would not be related to our hypothesis. Actually, we wanted to reverse the long SATB1 isoform’s relocation, from the aggregated form in the cytoplasm into the nucleus. Nevertheless, to show the complete picture, in the revised version of the manuscript in Figure 6c, we now provide data for both short and long SATB1 isoforms.
- Fig 6d., The authors claim that mutating a specific P site changes the phase behaviour of the 'short iso'. Does it also increase for the long isoform? The authors need to confirm this in order to verify the effect of a single P site outside of oligomerization domain. ...' phosphorylation status; when phosphorylated it remains diffused, whereas unphosphorylated SATB1 is localized to PML bodies....' This being an important premise, thus should be moved to the results text.
In the revised version of the manuscript, we moved the part regarding PML in the results section, as suggested by the Reviewer. Moreover, we included additional experiments probing the impact of association between PML and two SATB1 full length isoforms on their dynamics. The modified section in Lines 357-368 now reads: “In relation to this, a functional association between SATB1 and PML bodies was already described in Jurkat cells64. We should note that PML bodies represent an example of phase separated nuclear bodies65 associated with SATB1. Targeting of SATB1 into PML bodies depends on its phosphorylation status; when phosphorylated it remains diffused, whereas unphosphorylated SATB1 is localized to PML bodies66. This is in line with the phase separation model as well as with our results from S635A mutated SATB1, which has a phosphorylation blockade promoting its phase transitions and inducing aggregation. To further test whether SATB1 dynamics are affected by its association with PML, we co-transfected short and long full length SATB1 isoforms with PML isoform IV. The dynamics of long SATB1 isoform was affected more dramatically by the association with PML than the short isoform (Supplementary Fig. 7e), which again supports a differential behavior of the two SATB1 isoforms.”
Moreover, given the localization of the discussed phosphorylation site in the DNA binding region of SATB1 we did test its impact on DNA binding as documented in the revised Supplementary Fig. 7d. Additionally, as we have noted in our answer in Major Comment C of this reviewer, to further support the effect of serine phosphorylation on the DNA binding capacity of SATB1 we have performed DNA affinity purification experiments utilizing primary thymocyte nuclear extracts treated with phosphatase (Supplementary Fig. 7b) We found that SATB1’s capacity to bind DNA (RHS6 hypersensitive site of the TH2 LCR) is lost upon treatment with phosphatase (Supplementary Fig. 7c).
- Pg 16,. The authors have tried to explain multiple things (concepts of self-regulation, accessibility) which is quite tangential. There is no inference to Fig 6f., which is showing the opposite to what the authors had postulated. This portion should either be removed or explained with a rationale. The writing also needs to be revised thoroughly in this section. Similarly, the discussion should also be modified.
The rationale for the original Fig. 6f (revised Fig. 6g) was described in great detail in Lines 330-343 of the original manuscript. It is not clear why the Reviewer assumes that it shows the opposite to our hypothesis. As we explained, the increased accessibility allows faster read-through by RNA polymerase, and thus the exon with higher accessibility is more likely to be skipped. The exact relationship is shown in the revised Fig. 6g where the increased accessibility is associated with the expression of the short isoform, whereas the long isoform expression needs lower chromatin accessibility which allows the splicing machinery to act on the specific exon to be included. We reason that these findings are important and relevant because: 1) we suggest a potential regulatory mechanism for the SATB1 isoforms production. This is highly relevant to this manuscript given the fact that this is the first report on the existence of the long SATB1 isoform, and 2) the differential production of the long/short SATB1 isoforms has a potential relevance to breast cancer prognosis. In the revised version of the manuscript we added Fig. 6f, which now indicates the differential chromatin accessibility in human breast cancer patients and accordingly the expression of the long SATB1 isoform are associated with worse patient prognosis as indicated in Fig. 6h and Supplementary Fig. 8a,b. In the revised version of the manuscript, we substantially modified the text in Lines 374-408, to make the relevance of all these conclusions clear. The modified text now reads: “Therefore, we reasoned that a more plausible hypothesis would be based on the regulation of alternative splicing. In our accompanying manuscript19, we have reported that the long SATB1 isoform DNA binding sites display increased chromatin accessibility than what expected by chance (Fig. 3b in 19), and chromatin accessibility at long SATB1 isoform binding sites is reduced in Satb1 cKO (Fig. 3c in 19), collectively indicating that long SATB1 isoform binding promotes increased chromatin accessibility. We identified a binding site specific to the long SATB1 isoform19 right at the extra exon of the long isoform (Fig. 6e). Moreover, the study of alternative splicing based on our RNA-seq analysis revealed a deregulation in the usage of the extra exon of the long Satb1 isoform (the only Satb1 exon affected) in Satb1 cKO cells (deltaPsi = 0.12, probability = 0.974; Supplementary File 4). These data suggest that SATB1 itself is able to control the levels of the short and long Satb1 isoforms. A possible mechanism controlling the alternative splicing of Satb1 gene is based on its kinetic coupling with transcription. Several studies indicated how histone acetylation and generally increased chromatin accessibility may lead to exon skipping, due to enhanced RNA polymerase II elongation48,49. Thus the increased chromatin accessibility promoted by long SATB1 isoform binding at the extra exon of the long isoform, would increase RNA polymerase II read-through leading to decreased time available to splice-in the extra exon and thus favoring the production of the short SATB1 isoform in a negative feedback loop manner. This potential regulatory mechanism of SATB1 isoform production is supported by the increased usage of the extra exon in the absence of SATB1 in Satb1 cKO (Supplementary File 4). To further address this, we utilized the TCGA breast cancer dataset (BRCA) as a cell type expressing SATB150. ATAC-seq experiments for a series of human patients with aggressive breast cancer51 revealed differences in chromatin accessibility at the extra exon of the SATB1 gene (Fig. 6f). In line with the “kinetic coupling” model of alternative splicing, the increased chromatin accessibility at the extra exon (allowing faster read-through by RNA polymerase) was positively correlated with the expression of the short SATB1 isoform and slightly negatively correlated with the expression of the long SATB1 isoform (Fig. 6f). Moreover, we investigated whether the differential expression of SATB1 isoforms was associated with poor disease prognosis. Worse pathological stages of breast cancer and expression of SATB1 isoforms displayed a positive correlation for the long isoform but not for the short isoform (Fig. 6g and Supplementary Fig. 6c). This was further supported by worse survival of patients with increased levels of long SATB1 isoform and low levels of estrogen receptor (Supplementary Fig. 6d). Overall, these observations not only supported the existence of the long SATB1 isoform in humans, but they also shed light at the potential link between the regulation of SATB1 isoforms production and their involvement in pathological conditions.”
- The authors should not draw conclusions based on any data which is not shown '....ed differences in chromatin accessibility at the extra exon of the SATB1 gene (data not shown), suggesting its potential involvement in alternative splicing regulation according to the "kinetic coupling" model...'. This has led to overspeculation and needs correction.
In the revised version of the manuscript, we included the ATAC-seq data from human breast cancer patients in the revised Fig. 6f. The legend of this figure now reads: “Human TCGA breast cancer (BRCA) patient-specific ATAC-seq peaks51 span the extra exon (EE: extra exon; labeled in green) of the long SATB1 isoform. Note the differential chromatin accessibility in seven selected patients, emphasizing the heterogeneity of SATB1 chromatin accessibility in cancer. Chromatin accessibility at the promoter of the housekeeping gene DNMT1 is shown as a control. (Lines 1281-1285)” Accordingly, we have also modified the main text: “ATAC-seq experiments for a series of human patients with aggressive breast cancer68 revealed differences in chromatin accessibility at the extra exon of the SATB1 gene (Fig. 6f). In line with the “kinetic coupling” model of alternative splicing, the increased chromatin accessibility at the extra exon (allowing faster read-through by RNA polymerase) was positively correlated with the expression of the short SATB1 isoform and slightly negatively correlated with expression of the long SATB1 isoform (Fig. 6g).” (Lines 395-339)”
Minor comments: 1. On pg 4, the authors state 'Here, we utilized primary murine T cells, in which we have identified two full-length SATB1 protein isoforms.' Whereas only one 'long' isoform is identified and the other is the canonical version. The authors should correct the statement.
In the revised version of the manuscript, we modified this statement as follows: ”In this work, we utilized primary developing murine T cells, in which we have identified a novel full-length long SATB1 isoform and compared it to the canonical “short” SATB1 isoform.” (Lines 64-66)”
- Fig. 1 a , Is there a specific reason to generate a custom-made antibody for 'all' SATB1, using similar regions that are already commercially available. This becomes redundant otherwise, because there is no apparent difference in detection compared to the commercial one (Suppl. Fig 1a). Antibody generation strategy (1a) should be moved to supplementary. Additionally, authors have obtained the custom antibodies from a commercial source, therefore, the text should reflect the same alongside relevant details.
The custom-made SATB1 antibody targeting the amino-terminal region of the protein has been developed in order to be utilized for detecting the native form of the protein. Unlike commercially available antibodies raised against either short peptides or denatured forms of the protein we have utilized the native form of the amino-terminal part of the protein for raising this antibody. To be honest, this antibody has been raised in order to be utilized in ChIP-seq experiments since no commercially available antibody is of high quality for this approach. Moreover, the original Figure 1a was utilized in order to provide an overview of the SATB1 protein structure which is highly relevant to understand its biophysical properties and not for presenting the strategy for raising a custom-made antibody for SATB1.
- Fig 3e: what is the control used here? In their Pearson correlation analysis, there seem to be significant reduction in control sets as well upon treatment. This needs to be clarified.
We used scans rotated by 90° which served as a negative control, as stated in Line 769: “SATB1 scans rotated by 90° served as a negative control for the colocalization with FU.” Note that this is a commonly used control in colocalization experiments as described for example in Dunn et al., 2011 (https://doi.org/10.1152/ajpcell.00462.2010).
Additionally, we provide Costes’ P values which are based on randomly scrambling the blocks of pixels (instead of individual pixels, because each pixel’s intensity is correlated with its neighboring pixels) in one image, and then measuring the correlation of this image with the other (unscrambled) image. Please see Costes et al., 2004 (https://doi.org/10.1529%2Fbiophysj.103.038422) for more details. Moreover, it was actually anticipated to see a decrease in colocalization upon hexanediol treatment even in the negative control, as hexanediol significantly reduces both SATB1 and FU speckles as established in Fig. 3a-d.
- Pg 10, the authors claim that '..., thus we reasoned that it may also be used to study phase separation...' But there have been numerous reports starting from 2018, which have utilized this technique in corelation to phase behaviour (albeit individual proteins). The authors should include proper citations as they are extending an idea from the same field to their specific need.
In the revised version of the manuscript, we included relevant citations to support the use of Raman spectroscopy in LLPS research: “Raman spectroscopy was already used in many biological studies, such as to predict global transcriptomic profiles from living cells42, and also in research of protein LLPS and aggregation43–47. Thus we reasoned that it may also be used to study phase separation in primary T cells.” (Lines 225-228)”
- For Fig 5b, there should be a comparative image for 'short' isoform.
In the revised Figure 5c we have included a comparative image for the short SATB1 isoform.
- In the context of Figure 5c, the authors claim ...' Note also the higher LLPS propensity of the human long SATB1 isoform compared to the murine SATB1...' Why suddenly human and mouse comparisons are drawn? This figure should be moved to supplementary.
The comparison between the human and mouse SATB1 isoforms has been implemented because it is relevant for our claims regarding the increased SATB1 aggregation in human cells in relation to the revised Fig. 6f,g,h and Supplementary Fig. 6c,d. This is also discussed in Lines 479-482, which read: “This is particularly important given the higher LLPS propensity of the human long SATB1 isoform compared to the murine SATB1 (Fig. 5d). Therefore, human cells could be more susceptible to the formation of aggregated SATB1 structures which could be associated with physiological defects.”
**Reviewer #3 (Evidence, reproducibility and clarity):**
Zelenka et al., focus on a T cell genome-organizing protein, SATB1, to show that SATB1 undergoes liquid liquid phase-separation (LLPS), and distinct isoforms confer different LLPS-related biophysical properties. They generate a long-isoform specific antibody and conduct several experiments to test for LLPS and compare LLPS properties between the long-isoform relative to the whole SATB1 protein population. Given that SATB1 plays important roles in T cell development and in cancer, interrogating SATB1 biophysical properties is an important question. However, there are multiple problems with the experimental setup and data that weaken their support of the conclusions. I will detail some of the major issues below:
Regarding phase-separation There are several assays to determine whether a protein undergoes LLPS. 1. One of the first the authors address is the spherocity or roundness. Indeed, formation of spherical droplets is one evidence of the liquid nature of a protein. However, the authors use fixed preparations (which can introduce artifacts), not free-floating protein, and determine roundness by showing a 2D image. Roundness should take into account the diffraction-limits of fluorescent imaging, as many structures can be imaged to appear round by the detector. There are quantifiable measurements that can be taken on 3D images to show roundness. This would best be shown using non-fixed protein.
• We thank this Reviewer for several insightful comments. Although, we agree with most of them, we should highlight the main goal of our manuscript, i.e. to investigate the SATB1 protein with an emphasis on its physiological roles in primary developing murine T cells. We highlight this already in the introduction in Line 64 “In this work, we utilized primary developing murine T cells,...” and mainly also in the respective part of the result section: “To probe differences in phase separation in mouse primary cells, without any intervention to SATB1 structure and expression, we first utilized 1,6-hexanediol treatment, which was previously shown to dissolve the liquid-like droplets34.(Lines 203-205)”
• We believe that this is a very important aspect of our study that should not be overlooked. The majority of proteins perhaps behave differently under physiological and in vitro conditions. However, due to the extensive post-translational modifications affecting the properties of SATB1, its completely different localization patterns between primary developing T cells and other cell types but especially cell lines and many other aspects, it was of utmost importance to focus our research on primary T cells. Unfortunately, this was accompanied with multiple difficulties, such as that we have to use fixed cells as this is the only way to visualize SATB1 in these cells. Alternatively, one could create a new mouse line expressing a fluorescently tagged SATB1 protein, but this is beyond the scope of our work.
• However, we should also note that many LLPS-related studies do not pay any focus on primary physiological functions of proteins and they simply focus on the investigation of protein’s artificial behavior in in vitro conditions. Having said that, we too extended our experiments in primary cells to the ex vivo studies in cell lines to further support our claims. In these experiments, we utilized live cell imaging in Fig. 4-6, quantified the spherocity in Supplementary Fig. 6, showed the ability of speckles to coalesce in Fig. 4c and also used FRAP in Fig. 4f and also in the revised version of the manuscript in Supplementary Figure 6f. Moreover, we should note that most of these experiments were designed and performed during 2017 and 2018 conforming with the standards. We are well aware of the progress in the field and impact of fixation on LLPS, as described in Irgen-Gioro et al., 2022 (https://doi.org/10.1101/2022.05.06.490956), but after over seven months of review process in another journal we also believe that these aspects should be considered not to delay further progress of the SATB1 field.
Regarding the isoform specificity of SATB1 biophysical properties 1. The authors generate a long isoform-specific antibody. However, the western blot is not convincing that this is indeed specific to the long isoform as there is a rather large smear. Can this be improved with antibody preabsorption? Since this is a key reagent for the manuscript, improvement in antibody quality is essential.
The custom-made antibody for the long isoform has been raised against the unique 31 amino acids long peptide present in the long SATB1 isoform. The polyclonal serum has undergone affinity chromatography utilizing the immobilized peptide (antigen) to purify the antibody. In the revised version of the manuscript we have included another immunodepletion experiment with cleaner bands (Fig. 1f). Moreover, please read our answer to Major comment #2 of Reviewer 1 that follows: • The long antibody was raised in mice inoculated with the extra peptide present in the long isoform only. Therefore, the capacity of this antibody precipitating the shorter isoforms, which do not express the sequence of the extra peptide (EP, Figure 1a) in not possible.
• We have repeated the immunodepletion experiment and we now provide the results in Fig. 1f and Supplementary Fig. 1b. The western blot in Fig. 1f is now cleaner and supports quite convincingly the presence of a long SATB1 isoform. Given the lack of isoform-specific knockouts which we could utilize to immunoprecipitate or detect the different isoforms in a single cell (or cell population), the utilized approach of immunodepletion and subsequent western blotting is the approach we thought of implementing.
• As shown in Fig. 1f and Supplementary Figure 1b, the long isoform SATB1 antibody has the capacity to recognize the long isoform in murine thymocyte protein extracts but not the short SATB1 isoform (please compare lane 3 in the two western blots utilizing either the antibody for the long isoform -top panel - or the antibody that detects both isoforms (lower panel).
• We have performed Immunofluorescence experiments utilizing the antibody detecting the long SATB1 isoform in thymocytes isolated from either C57BL/6 or Satb1 cKO mice. The antibody is specific to the SATB1 protein since there is no signal in immunofluorescence experiments utilizing the knockout cells (Supplementary Figure 1c).
• We have performed Immunofluorescence experiments utilizing thymocytes and the antibody detecting the long SATB1 or a commercially available antibody detecting all SATB1 isoforms. The pattern of SATB1 subnuclear localization is similar for both antibodies (Supplementary Figure 1e).
• In our accompanying revised manuscript Zelenka et al., 2022 (https://doi.org/10.1101/2021.07.09.451769), we provide yet another piece of evidence, consisting of bacterially expressed short and long SATB1 protein isoforms detected by western blot using either the long isoform-specific or the non-selective all SATB1 isoforms antibodies.
• Regarding the additional bands detected in the immunoprecipitation experiment presented in the original Supplementary Figure 1b (lane 2), it is not surprising that additional bands appear in a sample of protein extracts that is used for several hours for the immunoprecipitation experiments, while the “input” sample simply denotes protein extract that is frozen at -80oC right after the preparation of protein extracts until use. It is well-established that SATB1 is the target of proteases which might as well be active during the immunoprecipitation steps (2 consecutive immunoprecipitation steps take place). Therefore, the immunoprecipitated material cannot necessarily be a copy of the input material displaying a single protein band even if protease inhibitors are included in the buffers.
Taken together the experiments described here we showed that the antibody raised against the extra 31 aa long peptide, present only in the long SATB1 isoform, is specific for this isoform.
- Fig 4 Optodroplet experiment appears to show that the N-terminus of SATB1 can undergo LLPS. The results of this assay show that SATB1 has a domain that can undergo phase-separation in isolation, but it does not show that the protein itself is a phase-separating protein. The FRAP assay methods are not provided by the authors, but this is important, as continued light activation means proteins are continuously forming aggregates, and the bleaching for FRAP should be balanced with the levels of Cry2 activation. A very good description of the methods is described in the original Optodroplet paper: https://www.sciencedirect.com/science/article/pii/S009286741631666X?via%3Dihub#sec4
We should note that we did follow the FRAP protocol provided by the recommended study Shin et al., 2017 (https://doi.org/10.1016/j.cell.2016.11.054). Indeed, these experiments are very tricky to perform and interpret, as every cell expresses slightly different amounts of protein which is directly associated with the different speed of optoDroplet formation, and thus its propensity to aggregate upon overactivation. On the other hand, there need to be continuous activation during the FRAP experiment as the lack of activation laser would result in fast disassembly of the optoDroplets, counteracting the FRAP results. Moreover, the optoDroplets actively move around the cell in all dimensions which makes the accurate measurement of signal intensity really challenging, even with an adjusted pinhole. Therefore, we do not think that FRAP is the best approach to examine the behavior of optoDroplets.
Either way, we have now described the detailed FRAP protocol in Lines 889-898, which read: “For the FRAP experiments, cells were first globally activated by 488 nm Argon laser illumination (alongside with DPSS 561 nm laser illumination for mCherry detection) every 2 s for 180 s to reach a desirable supersaturation depth. Immediately after termination of the activation phase, light-induced clusters were bleached with a spot of ∼1.5 μm in diameter. The scanning speed was set to 1,000 Hz, bidirectionally (0.54 s / scan) and every time a selected point was photobleached for 300 ms. Fluorescence recovery was monitored in a series of 180 images while maintaining identical activation conditions used to induce clustering. Bleach point mean values were background subtracted and corrected for fluorescence loss using the intensity values from the entire cell. The data were then normalized to mean pre-bleach intensity and fitted with exponential recovery curve in Fiji or in frapplot package in R.”
- Description of analyses that authors prefer not to carry out
**Reviewer #1**:
Can they use the all and long isoform antibodies together, then subtract the signal from long isoform to conclude about the localization of the shorth isoform ?
We thank the Reviewer for the suggestion, though given the differential efficiency of antibodies and other limitations of imaging experiments, we do not find the suggested experiment to have a potential to improve the quality of our manuscript. However, we should note that we have performed a pixel-based colocalization experiment between the signal detected by all isoform and long isoform SATB1 antibodies. Fluorocytogram of the pixel-based colocalization, based on 3D-SIM data is provided on the left, with quantified colocalization on the right of the revised Supplementary Fig. 5a.
3) Lack of better staining with antibody against the long and short SATB1 isoforms after treatment with 1,6 Hexanediol. 1,6 Hexanediol treatment can change many other chromatin associated proteins to which SATB1 can be bound to indirectly. This experiment can
We do understand the controversy and difficulties of experiments using 1,6-hexanediol treatment. However, we have to note that there is no better approach available for the investigation of LLPS in our primary murine T cells. We did use alternative approaches in ex vivo experiments, utilizing cell lines to validate our hypothesis without the involvement of 1,6-hexanediol.
**Reviewer #2**:
- The authors mention, '...of the different SATB1 isoforms, uncovered by the use of the two different antibodies, relied in the heterochromatin areas (zone 1), where the long isoform was less frequently...' There is no supporting figure number mentioned. The authors need to show a zone-by-zone comparison images for 'all iso' vs 'long' iso of SATB1. Just to reiterate, there is a need for a heterochromatin mark to unambiguously call out the distinction.
We should remind that there is an inherent difficulty to accurately compare localization of short and long SATB1 isoforms in primary cells, especially due to the lack of Satb1 isoform-specific knockout mice. There is no way to detect only the short isoform in these primary cells as there are only antibodies targeting the long or all SATB1 isoforms. Therefore, we cannot set up additional experiments probing these questions.
In line with this, in the revised version of the manuscript, we toned down our statements regarding the differential localization of the two isoforms in primary cells. We only refer to it as an indication and we support it by adding references to the relevant figures. This part now reads: “Localization of SATB1 speckles detected by antibodies targeting all SATB1 isoforms and/or only the long SATB1 isoform, revealed a significant difference in the heterochromatin areas (zone 1, Fig. 2b), where the long isoform was less frequently present (see also Fig. 2a and Fig. 3c). Although, this could indicate a potential difference in localization between the two isoforms, due to the inherent difficulty to distinguish the two based on antibody staining, we refrain to draw any conclusions. (Lines 145-150)”
- Fig. 6a, The authors wished to see the effect of RNA on Satb1 nuclear localization. This is not related to the main theme of the paper, thus should be moved to supplementary (true for b as well). Importantly, the experiments should be performed with total cells to show the divergence of localization (like the paper the authors referred to) instead of matrix for clarity.
• We did not wish to see the effect of RNA on SATB1 localization. In fact, there is a long history of SATB1 research that is inherently linked with the concept of nuclear matrix, a putative nuclear structure which is highly associated with nuclear RNAs. SATB1 was described many times as a nuclear matrix protein (https://doi.org/10.1016/0092-8674(92)90432-c; https://doi.org/10.1128/mcb.14.3.1852-1860.1994; https://doi.org/10.1074/jbc.272.17.11463; https://doi.org/10.1128/mcb.17.9.5275; https://doi.org/10.1021/bi971444j; https://doi.org/10.1083/jcb.141.2.335; https://doi.org/10.1101/gad.14.5.521; https://doi.org/10.1038/ng1146).
• Moreover, our data discussed in comments 4-7 of this Reviewer, such as i. the localization of SATB1 to the nuclear zones associated with RNA and nuclear scaffold factors (Fig. 2b, Supplementary Fig. 1c), ii. colocalization of SATB1 with actively transcribed RNAs (Fig. 2c, Fig. 3g, Supplementary Fig. 2a, Supplementary Fig. 2c), iii. including its association with nucleoli (Supplementary Fig. 3b), and also iv. its computationally predicted interaction with Xist lncRNA (Agostini et al., 2013; https://doi.org/10.1093/nar/gks968) as a notable factor of nuclear matrix, all suggest that the interaction between RNA and SATB1 is plausible and potentially relevant for its function and/or at least its subnuclear localization. It is relevant even more so, when considering numerous reports on the ability of RNA-binding, poly-Q and PrLD-containing proteins to undergo LLPS https://doi.org/10.1016/j.molcel.2015.08.018; https://doi.org/10.1042/bcj20160499; https://doi.org/10.1016/j.cell.2018.03.002; https://doi.org/10.1016/j.cell.2018.06.006; https://doi.org/10.1093/nar/gkaa681), including RNAs specifically regulating LLPS behavior, especially for poly-Q and PrLD-containing proteins, such as SATB1 (https://doi.org/10.1126/science.aar7366; https://doi.org/10.1126/science.aar7432; https://doi.org/10.1016/j.ceb.2019.03.007; https://doi.org/10.1038/s41598-020-57994-9; https://doi.org/10.1016/j.molcel.2015.09.017; https://doi.org/10.1038/s41598-019-48883-x; https://doi.org/10.1038/s41467-019-11241-6).
• It should also be noted that SAF and various hnRNPs, as the most prominent proteins of nuclear matrix were many times reported to phase separate (https://doi.org/10.1016/j.molcel.2019.10.001; https://doi.org/10.1074/jbc.ra118.005120; https://doi.org/10.1016/j.celrep.2019.12.080; https://doi.org/10.1038/s41467-019-09902-7; https://doi.org/10.1016/j.molcel.2017.12.022; https://doi.org/10.1074/jbc.tm118.001189). All these aspects show that the relation between nuclear matrix, SATB1 and RNA are quite relevant to our manuscript.
• Moreover, in light of the aforementioned information, we believe that it is much clearer to follow the protocol we did – i.e. to remove soluble proteins by CSK treatment and then, upon RNase treatment, extract the released proteins using ammonium sulfate. In an experiment utilizing whole cells, one would need to microinject RNase A into the nucleus, which 1. is very challenging for primary T cells having a radius of 3-5 micrometers, 2. is of low throughput, 3. would not allow for released protein removal which would thus make the results hard to interpret. Please note that in the reference paper, the authors used cell lines overexpressing heterologous GFP-tagged proteins, which is not related to our setup.
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Reply to the Reviewers
I thank the Referees for their...
Referee #1
- The authors should provide more information when...
Responses + The typical domed appearance of a hydrocephalus-harboring skull is apparent as early as P4, as shown in a new side-by-side comparison of pups at that age (Fig. 1A). + Though this is not stated in the MS 2. Figure 6: Why has only...
Response: We expanded the comparison
Minor comments:
- The text contains several...
Response: We added...
Referee #2
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- May 2022
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Reply to the reviewers
Manuscript number: RC-2021-01219
Corresponding author(s): Rajan, Akhila
1) General Statements [optional]
This section is optional. Insert here any general statements you wish to make about the goal of the study or about the reviews.
The goal of this study is to:
- Define how prolonged exposure to a high-sugar diet (HSD) regime alters both the lipid landscape and feeding behavior.
- Determine how changes in lipid classes within the adipose tissue regulates feeding behavior. Key findings:
In this study, by taking an unbiased systems level and genetic approach, we reveal that phospholipid status of the fat tissue controls global satiety sensing.
Impact of Key findings:
By uncovering a critical role for adipose tissue phospholipid balance as a key regulator of organismal feeding, our work raises the possibility that the rate-limiting enzymes in phospholipid synthesis, including Pect, are potential targets for therapeutic interventions for obesity and feeding disorders.
Peer review comments:
This study has immensely benefited from the thoughtful peer-review of three reviewers. As per their recommendations, we have performed a major revision by performing additional experiments (see summary table below in next section) and strived to address the major concerns raised. Based on our reading, there were two major concerns that overlapped between all three reviewers raised. They are as follows:
- Does the genetic disruption of Pect in fly fat body alter phospholipid levels? Two reviewers (#2 and #3) recommended that we perform lipidomic analyses on adult flies with adipose tissue specific knockdown of For the revised version, we have completed this lipidomic experiment, and present results as a new main Figure 6, Supplemental S7 and S9.
- Is the dampened HSD induced hunger-driven feeding (HDF) behavior because of increased baseline feeding (#1 and #3)? In addition, reviewer #1, asked us whether HSD flies experience an energy-deficit? In other words, we were asked to uncouple whether what we observed was HSD-driven allostasis or indeed, as we had interpreted, that HSD dampened hunger-driven feeding response.
Hence, they recommended that we:
- Re-analyze our hunger-driven feeding datasets and present non-normalized data (also requested by Reviewer #3) and show baseline feeding behavior on HSD. To address this, we have completed this analysis and present our results in Figure 1B-D and S1.
- Determine whether the HSD fed flies display an energy deficit on starvation. To this end, we performed an assayed starvation-induced fat mobilization on HSD, results for this are now presented on Figure 1E-G and S2. Conclusions after the revision:
First, it is important to note here that the additional experiments have not caused a significant revision of the major conclusions of the original version of our study. In fact, we hope that the revised version provides clarity and further substantiation to our original arguments.
- The lipidomics experiments on Pect fat-specific knock-down flies show that reducing Pect in fat-body causes a significant reduction in certain PE lipid species (PE 36.2 specifically- Figure 6B). This is consistent with a prior report on lipidomics of the Pect null allele by Tom Clandinin’s group (PMID: 30737130). Furthermore, we note that when Pect is knocked down in the fat body, there is a significant increase in two other classes of phospholipids LPC and LPE (Figure 6A). Together, this suggests that an imbalance in phospholipid composition in the absence of Pect activity in fat.
- The starvation-induced fat mobilization experiments show that despite being fed a prolonged HSD, adult flies sense starvation and effectively mobilize fat stores, at a level comparable to Normal food (NF) fed adult flies, suggesting that even despite HSD exposure, adult flies experience an energy deficit on starvation.
- In our non-normalized data, we find that the baseline feeding events are not significantly altered between HSD and NF-fed flies (Figure 1D). This suggests that the effects we observe are not due to an increase in the “denominator”, but a dampening of hunger-driven feeding on HSD. With regard to our original version, all three peer-reviewers found that the study was interesting, significant, important, and novel – Reviewer #1: “The work is potentially novel and interesting”; #2 : “I find the study to be potentially very important - the authors combine a longitudinal study that would be difficult in any other model with the powerful genetic tools available in the fly. The conclusions are mostly convincing”; #3: “This manuscript demonstrates how fat body Pect levels affect HSD induced changes in hunger-driven feeding response. I agree with all the reviewers points; potentially very interesting”. But had requested that we provide further substantiation and clarification.
We sincerely hope that the peer-reviewers find that our revised version with additional new experimental datasets, improved data visualization, and the presentation of non-normalized raw data points, makes this study clear, compelling, and well-substantiated.
- Point-by-point description of the revisions This section is mandatory. *Please insert a point-by-point reply describing the revisions that were already carried out and included in the transferred manuscript. *
Below we summarize in Part A, the key experiments that were performed to address the major concerns. In Part B, we provide a point-point response to each reviewer with embedded datasets.
Part a:
We performed several new experiments, including:
- To address the primary concern of Reviewer #1 regarding whether the HSD flies have a similar energy deficit to Normal food (NF) fed flies, we performed analysis of stored neutral fat Triacylglycerol (TAG) reserves and how HSD fed flies mobilized fat stores on starvation. We present these results in Figure 1E-G, S2. These results show that HSD-flies despite accumulating more TAG (S2), breakdown a similar amount of fat reserves as NF-fed flies on starvation at any time-point (Figure 1E-G). This suggests that HSD-fed flies do sense and respond to energy deficit.
- To address concerns of reviewer #2 and #3 on whether Pect genetic manipulation affects specific phospholipid classes, we performed lipidomic analyses. The table below summarizes the new 3 new figures and 4 supplemental figures (blue text are all new figure numbers and figure panels) and three new Supplementary files as per reviewer’s request.
Figure #
Main point
New datasets in revision
Companion Supplement
1
HSD alters feeding behavior, but flies still breakdown TAG on starvation.
TAG storage and breakdown over longitudinal HSD shows that HSD and NF fed flies show similar levels of TAG breakdown on starvation, despite consistently elevated TAG on HSD. This supports the idea that flies do sense starvation even on HSD, but there is a uncoupling of the feeding behavior after Day 14. Revised the data representation of Figure 1 to show non-normalized data over time. S1 and S2 companions are new in the revision. Panels 1D to 1E are new for the revision.
S1- Raw data of feeding events plotted.
S2 Elevated TAG at all time points.
2
HSD causes insulin resistance
S3A added to show that insulin transcript levels remain the same in response to reviewer #3’s concerns.
S3
3
Phospholipid concentration raw data from lipidomic on Day 7 and Day 14 HSD suggest that PC, PE levels are increased on Day 14 HSD.
Figure 3 revamped to show new data visualization and non-normalized raw data to address Reviewer #2’s major concerns. S4A and S4B added. In addition Supplementary File 1 and 2 provided with raw lipidomics data as per reviewer #2’s request.
S4.
S4A- non normalized raw data of all other lipid classes on HSD.
S4B- fatty acid species data on Day 14 added as per request of rev.#2.
4
HSD regulate Apo-I levels in the IPCs and phenocopies Pect KD.
Added Figure 4A to show that HSD phenocopies Pect-KD in terms of delivery to brain
S5 showing the validation of the Apo-I antibody.
S6 validation of Pect KD and over-expression and Pect mRNA levels dysregulation on HSD.
5
Pect RNAi is insulin resistant
N/A
N/A
6
Pect knockdown shows significant increase in LPC and LPE, and a non-significant reduction in PC, PE levels. Specifically, the PE lipid class PE36.2 is downregulated.
Fig 6, S7, S9 are completely new based on reviewer #2 and #3 requests. In addition Supplementary File 3 provided with raw lipidomics data as per reviewer #2’s request
S7, S8, S9#.
S7- new Pect KD other classes
S8- new PE classes for day 14 and Pect associated classes.
S9- Pect OE lipidomics
7
Pisd and Pect activity in adipocytes are required for hunger-driven feeding behavior in normal diets
Pisd RNAi data was moved from supplement to main figure.
N/A
Note on revised text: We have revised text not only in the results section, but also as per reviewer #2’s recommendation, we have revamped our introduction and discussion as well. Since the manuscript has been significantly revised to include a main figure 6, fully altered Figure 1 and 3, multiple new supplemental figures, the changes in text are extensive. Hence, they are unmarked in the main text. Nonetheless, we hope that the reviewers will be able to evaluate these changes, as we have provided the specific locations in text and embed key figures in the point-point response below.
__Part B: __Point-Point responses to reviewer comments.
Reviewer #1 comments in Blue, author response in black.
Reviewer #1 (Evidence, reproducibility and clarity (Required)):
In this manuscript, Kelly et al. show that the difference between the feeding behavior of fed and starved flies (hunger-driven feeding; HDF) is absent in animals fed a high-sugar diet (HSD) for two weeks or more. The disappearance of HDF with HSD coincides with changes in phospholipid profiles caused by HSD. Furthermore, RNAi-mediated downregulation of Pect in the fat body-a key enzyme in the PE biosynthesis pathway-phenocopies physiological effects of HSD. Moreover, downregulation or overexpression in the fat body abolishes or induces HDF, respectively, abolishes or induces HDF, respectively, independent of HSD treatment.
Overall, the manuscript is well-written and the phenotypes are clear. However, I have major concerns regarding the authors' interpretation of the data and their conclusion. Most importantly, while it is clear that the authors' high-sugar dietary treatment affects feeding behavior and physiology, I am not convinced that the changes can be considered "hunger-driven"-which is central to the main point of the manuscript. Therefore, it is my recommendation that the authors substantially revise the manuscript by either showing additional/re-analyzed data that rule out alternative hypotheses, or rewriting the manuscript keeping alternative interpretations in mind.
We are thankful to this reviewer for their thoughtful critique, and constructive and specific suggestions on how we can redress these concerns. We have taken on board the concerns of this reviewer regarding our interpretation of whether the changes in feeding behavior can be considered hunger-driven or not. Based on their advice, we have made significant changes by addressing: i) does HSD increased baseline feeding- we now show non-normalized raw data and data supports conclusion that baseline feeding is not higher; ii) whether HSD- fed flies can sense an energy deficit at levels similar to NF fed flies- we show that HSD flies sense energy deficit. We have provided detailed response below, and we hope the reviewer finds the additional datasets and re-analyzed data are consistent with the interpretation that prolonged HSD dampens starvation induced feeding. In addition to this key concern this reviewer has made a many other salient points that we have addressed with additional data or by clarifying the text.
Major comments: 1) The data do not sufficiently show that the long-term HSD regime disrupts "hunger-sensing." The manuscript should address alternative hypotheses by showing raw instead of normalized data, rewriting the manuscript with a new central conclusion, or running additional experiments that actually show a defect in hunger-driven response. a. The main results that the authors rely on for the argument is that the ratio of feeding events that the starved and non-starved flies eat is different between the groups fed normal or HSD. However, because the authors only show normalized data (normalized to non-starved flies; Fig. 1), it is difficult to tell whether the change is due to a chronically increased feeding in non-starved HSD flies-maybe in perpetual hunger-like allostasis-or dampened starvation response. Indeed, the data shown in Fig S1 show that flies fed HSD for as short as 5 days show more frequent feeding events compared to age-matched controls fed normal food. It is possible that because the HSD-fed flies eat more than NF-fed flies, even without being starved, the ratio of starved/non-starved feeding is lower in the HSD-fed group-due to changes in the denominator, rather than the numerator.
We have taken onboard this concern regarding presenting only normalized data, and that clouded the interpretation and left open other possibilities. In the completely revised figure 1 and S1. We now show non-normalized data, as a function of time. First we note that HSD-fed flies, do not show higher baseline feeding that NF fed flies, except on Day 10 of HSD, when there is a modest but significant elevation (Figure 1D).
Nonetheless, on Day 10 HSD, flies still display increased hunger-driven feeding HDF (Figure 1C), it is only after Day 14 HSD that HSD dampens the starvation induced feeding.
- It is also possible that the HSD-fed flies are simply not in as big an energy deficit physiologically, due to the increased fat deposits they've accumulated (as the authors show later in the manuscript). It may take longer for the fat HSD flies to reach substantial energy deficiency than the NF flies, but they still may eventually be able to appropriately respond to hunger, just like NF flies. In such case, it would be a misnomer to call this behavioral change a 'defect in hunger-driven feeding behavior.' Maybe an experiment with a dose-response curve of "hunger driven feeding response" as a function of duration of starvation would help? Prompted by this reviewers question, we asked whether HSD fed flies, that have a higher baseline neutral fat store (Triacylglycerol-TAG) level, and if HSD-fed flies can sense energy deficit. For this, we revisited the longitudinal assays for neutral fat triacylglycerol (TAG) storage that our lab had generated, along with the HSD-HDF studies. We now present this evidence as Figure 1E-1G and Figure S2. Overall, our experiments point to the idea that adult flies fed HSD, are able to sense and mobilize TAG stores effectively throughout the 28-day time point that we analysed.
First as shown in Figure S2, flies fed HSD display an increase in TAG levels. But it is to be noted that while TAG stores increase, the increase is not linear with time. This suggests that adult flies exposed to HSD store excess energy as TAG, but the increased TAG stores stay within a certain range despite the length of HSD exposure. This suggests that adult flies on HSD still display TAG homeostasis.
Next, to directly address the reviewers point about HSD fed flies not sensing an energy deficit, we subject HSD-fed flies to an overnight starvation, same regime as used in the overnight feeding experiments, and asked whether they mobilize TAG. We noted that flies exposed to HSD breakdown TAG throughout the 28-day exposure at statistically significant levels for Day 3- Day 28, except on 14 and 21 days (Figure 1F). While there is TAG mobilization on Day 14 and 21, the difference is not statistically significant. Nonetheless, we note the same levels TAG breakdown for normal lab food (NF) fed flies on Day 14 and 21 (Figure 1E). Overall, HSD fed flies sense and display energy deficit, as measured by TAG store mobilization, throughout the 28 days of HSD exposure, at levels comparable to NF-fed flies (Figure 1G).
Taken together, these results suggest that while HSD-fed flies experience an energy deficit on starvation, at levels comparable to NF-fed flies, throughout the 28-day time point assayed. But, their starvation driven feeding-response is dampened by Day 14 and by Day 28, the HSD-fed flies display more feeding events than HSD starved flies. These results are consistent with the interpretation that in HSD-fed flies the starvation-induced feeding behavior becomes desynchronized from the starvation induced TAG-mobilization, suggesting that there is an absence of hunger-driven feeding.
2) How can you be sure that lower Dilp5 immunofluorescence is indicative of increased Dilp5 secretion? Wouldn't decreased production of dilp5 also have the same results?
It has been shown previously in HSD fed larvae are hyperinsulinemic, i.e., they have 55% increase in circulating Dilp2 ( PMID: 22567167). Additionally, we have shown that ectopic activation of the insulin-producing neurons by expressing TRPA1, an ion channel that activates neurons, reduces Dilp5 accumulation without a change in Dilp5 mRNA levels (PMID: 32976758), suggesting that reduced Dilp5 accumulation, without alterations to mRNA levels is a proxy for increased secretion. Now, in response to this concern, in the revised manuscript, we have added qPCR data of Dilp2 and 5 (Figure S3A), which show no difference in expression levels after 14 days on HSD. Therefore, there is no dip in Dilp5 mRNA production. Given that Dilp2 and Dilp5 mRNA levels remain the same, but we see reduced Dilp5 accumulation, we interpret this to mean that Dilp5 secretion is increased.
- Also, the authors should state in the main text that it is Dilp5, not just any Dilp. Thanks for this suggestion and we have fixed this and referred to Dilp5 specifically throughout the text in the results section.
3) Data presentation: a. Sometimes the data are normalized to NF (Fig 4B-C), sometimes not (ex. Fig 4A, S4C). Unless there is a specific rationale for the data transformation, it would be more appropriate to show untransformed data (ex. Fig 4A, S4C), especially as the authors use two-way ANOVA to determine significance. Only showing the differences implies comparison against a hypothetical mean (i.e. μ0=0), not between two group means.
We thank the reviewers for bringing this issue to our attention. We updated all the figures to show untransformed data in the revised manuscript.
- Some figures show both individual data points and summary statistics (mean, SD, ... ex. Fig 2A)-which I believe is ideal-but some show only one or the other (ex. Fig 2B, no summary statistics; Fig. 3, no data points. The manuscript would read more convincing if data visualization is consistent across figures. We thank the reviewers for their feedback. We have made changes to all the figures in the revised manuscript to improve visual consistency.
Minor comments: 1) High sugar diet: what is the actual sugar concentration in the NF v. HSD diets? The authors write that the HSD diet contains "30% more sugar" than the NF, but providing the final sugar concentrations-sucrose or others-would be informative for other scientists studying the effect of high sugar diets.
We thank the reviewer for their suggestion and now we have updated the methods to include this sentence. “After 7 days, flies were either maintained on normal diet or moved to a high sugar diet (HSD), composed of the same composition as normal diet but with an additional 300g of sucrose per liter”.
- Additionally, the definition of HSD is inconsistent. Main text (Page 5, line 17) states that their HSD is "60% more sugar than normal media," whereas the figure legend (Fig 1) and the Methods state that the HSD contains "30% more sugar." We apologize for this egregious typo in the figure legend! We have now fixed this to say 30% HSD. Only 30% HSD was used throughout this study.
2) Starvation medium: please provide justification for why the authors used 1% sucrose/agar for starvation medium, instead of plain agar/water that most labs use. At least clarify and provide a reference for the claim that the 1% sucrose/agar "is a minimal food media to elicit a starvation response."
We are very grateful for this reviewer identifying this this methods description error and bring it to our attention. We used 0% sucrose agar for overnight starvation in this study as most labs do. The error occurred because we were using another manuscript from the lab to help draft the methods section (PMID: 29017032). In that study, where we assayed the effect of chronic starvation our lab used: “1% sucrose agar for 5 days at 25C”. However, in this current study, because we are testing acute effects of overnight starvation, we are using 0% sucrose agar.
3) Pect mRNA level is higher with HSD. This is surprising because not only, as authors mention, is increased PC32.2 with HSD suggests lower Pect activity, but also because Pect RNAi phenocopies long-term HSD in HDF behavior, lipid morphology, FOXO accumulation in fat body. The authors speculate that the data "likely shown an upregulation in an attempt to mediate the Pect dysregulation occurring at the protein level." If that were true, a western blot may be informative. Zhao and Wang (2020, PLoS Genetics) generated a Pect antibody that seems compatible with western blot applications. That being said, I don't think such data is critical for the manuscript. I mention this simply as a suggestion for the authors. a. page 8, line 22-23, did you mean to write "Given how PC32.2 is elevated after 14 days of exposure to HSD, we assumed that Pect levels would be low for flies under HSD," not "high?" Otherwise the subsequent 2 sentences don't make sense.
We agree that the most confusing aspect of the study was that Pect mRNA levels being very high on Day 14 HSD, but nonetheless the effects of Pect-KD phenocopied HSD. To resolve this, we have now performed lipidomic analyses on whole adult flies, when Pect is knocked-down (KD) by RNAi in the fat tissue. We now present a new dataset in Figure 6. Two striking changes occur. They are:
- Pect-KD shows increase in the phospholipid classes LPC and LPE (Figure 6A). In contrast, LPE is significantly downregulated on HSD Day 14 (Figure 3).
- Pect-KD shows a significant reduction in specific class of PE 36.2 (Figure 6B). Our data regarding increase in PE 36.2 agree with a previous lipidomic analyses of Pect mutant retina (PMID: 30737130). In contrast, PE 36.2 trends upwards on 14 day HSD (Figure S7C) though not significantly. On 14-day HSD consistent with extreme upregulation of Pect mRNA fed flies (Figure S6A; Pect mRNA 200-250 fold), PE trends upwards on 14-day HSD (Figure 3) and PE 36.2 trends higher (Figure S7C). We note that on the surface of it PE and LPE per se are contrasting between 14-day HSD lipidome and fat-specifc Pect-KD. But there is a significant commonality that under both states there is an imbalance of phospholipids classes PE and LPE. Hence, we propose that maintaining the compositional balance of phospholipid classes PE and LPE is critical to hunger-driven feeding and insulin sensitivity. Hence, either increase or decrease, of these key phospholipid species, may lead to abnormal hunger-driven feeding.
We agree that a western blot would be informative as well, but we were unable to obtain the reagent from Dr. Wang’s group, precluding us from performing this request. See email snapshot.
To ensure that we appropriately discuss and clarify this issue, we have now included a section in the discussion - Page 14 Lines 26-34- under the subtitle “The implications of relationship between Pect levels and HSD”. We have pasted an excerpt from that subsection below for this reviewers assessment.
“Also, we note that over-expression of Pect cDNA in the fat-body does not alter phospholipid balance (Figure S9) and indeed improves HDF on HSD (Figure 7B). While this may appear inconsistent, it is critical to note that over-expression of Pect cDNA using UAS/Gal4 only increases Pect mRNA expression by 7-fold (Figure S6A), whereas HSD causes its upregulation by 250-fold (Figure S6B). Hence, we speculate that an increased ‘basal’ level of Pect such as by that provided by a cDNA over-expression in fat, may be protective to the negative effects of HSD (Figure 7B) without affecting overall phospholipid levels (Figure S9) , but extreme upregulation Pect on HSD affects the PE and LPE balance (Figure 3).”
Reviewer #1 (Significance (Required)):
The work is potentially novel and interesting, but at this stage it's difficult to interpret what the phenotype signifies. Although the manuscript could be revised simply by modifying the text, experimentally addressing the concerns would significantly improve the work.
In sum, we hope we have addressed the key concern for Reviewer #1 as to whether the behavior we report here is indeed a dampening of starvation-induced feeding, or an effect of increase in baseline feeding. We hope that by reviewing our non-normalized data, they can appreciate that it is the former. Also, we hope that Reviewer #1 appreciates that we have strived to address the concerns by additional experiments, to clarify our findings and improve the impact of the work.
Reviewer #2 (Evidence, reproducibility and clarity (Required)):
This intriguing manuscript by Kelly and colleagues uses the fruit fly Drosophila melanogaster as a model to understand how diet-induced obesity alters the feeding response over time. In particular, the authors findings indicate that chronic exposure to a high-sugar diet significantly alters the starvation-induced feeding response. These behavioral studies are complemented by a lipidomics approach that reveals how a chronic high sugar affects many lipid species, including phospholipids. The authors then pursue mechanistic studies that indicate phospholipid metabolism within the fat body appears to remotely affect insulin secretion from the insulin producing cells. Moreover, the changes in phospholipid abundance are associated with changes in insulin-signaling, including increased insulin secretion from the IPCs and elevated levels of FOXO within the nucleus.
I find the study to be potentially very important - the authors combine a longitudinal study that would be difficult in any other model with the powerful genetic tools available in the fly. The conclusions are mostly convincing, but a few follow-up experiments are required:
We are grateful for the reviewers constructive, detail-oriented, and balanced feedback, and their recognition of the value of this study. Now, we have performed additional experiments to address the key concerns raised by all reviewers. We hope that on reading the revised version of our study, that the reviewer continues to feel positive about the message of this study and its potential impact.
- The key conclusions from the manuscript assume that manipulation of Pect expression levels alters phosphatidylethanolamine (PE) levels. However, the authors make no attempt to verify that the genetic experiments described herein actually affect PE levels. At a minimum, changes in PE levels should be verified for the Pect knockdown and overexpression lines. Similarly, there is no evidence that manipulation of either EAS or Pcyt2 induces the expected metabolic effects. I'm not asking that the longitudinal feeding experiments be repeated, simply that the authors measure the relevant lipid species, preferably with a targeted LC-MS approach.
Prompted by this reviewer, we performed targeted LC-MS on whole adult flies, on normal diet, to assess lipid levels for fat-specific Pect-KD and overexpression. We decided to focus on Pect, as its knock-down even on normal diet causes a dampened hunger-driven feeding behavior (Figure 7A) and phenocopied a 14-day HSD feeding phenotype.
We now present a new dataset in Figure 6. Two striking changes occur:
They are:
Pect-KD shows a significant reduction in specific class of PE 36.2 (Figure 6B). Our data regarding decrease in PE 36.2 agree with a previous lipidomic analyses of Pect mutant retina (PMID: 30737130). It is to be noted that though overall levels of all PE species trend downwards, like the Clandinin lab study on Pect (PMID: 30737130), we did not find a significant change in the overall PC and PE levels.
- Pect-KD shows increase in the phospholipid classes LPC and LPE (Figure 6A). In contrast, LPE is significantly downregulated on HSD Day 14 (Figure 3). On 14-day HSD consistent with extreme upregulation of Pect mRNA fed flies (Figure S6A; Pect mRNA 200-250 fold), PE trends upwards on 14-day HSD (Figure 3) and PE 36.2 trends higher (Figure S7C). We note that on the surface of it PE and LPE per se are contrasting between 14-day HSD lipidome and fat-specifc Pect-KD. But there is a significant commonality that under both states there is an imbalance of phospholipids classes PE and LPE. Hence, we propose that maintaining the compositional balance of phospholipid classes PE and LPE is critical to hunger-driven feeding and insulin sensitivity. Hence, either increase or decrease, of these key phospholipid species, may lead to abnormal hunger-driven feeding.
Finally, fat-specific Pect-OE did not cause significant changes to lipid species (Figure S9). This could either be due to the fact that in fat-specific Pect-OE flies under normal food and that we were assaying whole body lipid levels and not fat-specific lipid changes. But to counter that, even a 60% reduction in Pect mRNA levels (Figure S6A), was sufficient to produce an effect on whole body phospholipid balance (Figure 6). Hence, we speculate that by maintaining a basally higher (7-fold higher Pect mRNA level Figure S6A), might allow 14-day HSD-fed flies to buffer the negative effects of HSD and we predict that it might take longer to disrupt the phospholipid balance and HDF response.
We have now included a section in the discussion - Page 14 Lines 26-34- under the subtitle “The implications of relationship between Pect levels and HSD”. We have pasted an excerpt from that subsection below for this reviewers assessment.
“Also, we note that over-expression of Pect cDNA in the fat-body does not alter phospholipid balance (Figure S9) and indeed improves HDF on HSD (Figure 7B). While this may appear inconsistent, it is critical to note that over-expression of Pect cDNA using UAS/Gal4 only increases Pect mRNA expression by 7-fold (Figure S6A), whereas HSD causes its upregulation by 250-fold (Figure S6B). Hence, we speculate that an increased ‘basal’ level of Pect such as by that provided by a cDNA over-expression in fat, may be protective to the negative effects of HSD (Figure 7B) without affecting overall phospholipid levels (Figure S9), but extreme upregulation Pect on HSD affects the PE and LPE balance (Figure 3).”
A central hypothesis in the study is that the HSD over a period of 14 days results in insulin resistant and that these changes are leading to changes in hunger dependent feeding. I would encourage the authors to determine if Foxo mutants are resistant to these HSD-induced effects on HFD.
We thank the reviewers for this suggestion. However, given that dFOXO nuclear localization rather than expression levels regulate insulin sensitivity, we feel that disrupting dFOXO levels via mutation or knockdown will produce a plethora of indirect effects including developmental abnormalities (PMID: 24778227, PMID: 16179433, PMID: 29180716, PMID: 12893776). Our data suggest that chronic HSD treatment and Pect affect insulin sensitivity in fat tissue. However, we feel that investigating whether insulin sensitivity/FOXO signaling in fat tissue regulates feeding behavior is outside the scope of our work.
- In lines 25-30, the authors draw the conclusion that an increase in unsaturated fatty acid species is associated with the HSD and that these changes results in a more fluid lipid environment. While I agree with the model, the manuscript contains no evidence to support such a model. Either test the hypothesis or move the last line of the section to the discussion.
We thank the reviewer for this important and insightful comment. We agree that the data we presented and discussed in the original version is at the moment speculative. Addressing the hypothesis that increase in unsaturated fatty acid species result in a more fluid lipid environment will require us to build tools and expertise. Hence, this hypothesis is better suited for exploration in a future study. Given this, we have moved this out of the results section into the Discussion section titled “HSD and fat-specific PECT-KD causes changes to phospholipid profile” (See excerpt below from page 13, lines 24-35).
“In addition to changes in phospholipid classes, we found that HSD caused an increase in the concentration of PE and PC species with double bonds (Figure S4C and S4D). Double bonds create kinks in the lipid bilayer, leading to increased lipid membrane fluidity which impacts vesicle budding, endocytosis, and molecular transport14,92. Hence it is possible that a mechanism by which HSD induces changes to signaling is by altering the membrane biophysical properties, such as by increased fluidity, which would have a significant impact on numerous biological processes including synaptic firing and inter-organ vesicle transport.”
Also, as per the reviewer’s guidance, given that we are speculating here, we have also shifted this dataset from Main figure 4 to supplement S4C and S4D.
In addition, lines 25-30 state that FFAs are increased after 14 days of a HSD. Figure 3A shows the exact opposite - FFAs are significantly decreased in 14 day fed animals despite being elevated in the 7 day fed animals. This is an interesting result that warrants discussion. Moreover, I would encourage to examine the lipidomic data more carefully to ensure that the text accurately portrays the lipid profiles.
We apologize for misstating that FFAs are decreased on 14-day HSD in the lines 25-30. It was an error and we have corrected this. We agree with the reviewer that the reduction of FFA on Day 14-HSD is an intriguing and unexpected observation that needs to be emphasized and further discussed. To this end, we have added figure S4B, wherein we have provided the difference in FFA concentration (by species) after days 7 and 14.
Furthermore, we have discussed what the potential meaning of reduced FFA at Day 14 implies in page 12, lines 19-27 of the Discussion section titled “HSD and fat-specific PECT-KD causes changes to phospholipid profile”. We have stated the following-
“We speculate that this reduction in FFA maybe due to their involvement in TAG biogenesis (PMID: 13843753). We were interested to see if the decrease in FFA correlated to a particular lipid species, as PE and PC are made from DAGs with specific fatty acid chains. However, further analysis of FFAs at the species level did not reveal any distinct patterns. The majority of FFA chains decreased in HSD, including 12.0, 16.0, 16.1, 18.0, 18.1, and 18.2 (Figure S4B). This data was more suggestive of a global decrease in FFA, likely being converted to TAG and DAG, rather than a specific fatty acid chain being depleted.”
The processed lipidomics data should also be included as supplementary data table so that they can be independently analyzed by the reader.
We thank the reviewer for this suggestion. As per the reviewers request, we have included the raw data as an attachment in our supplementary material (Supplementary Files 1-3.), so that interested readers can use the datasets generated in this study for future work and further analysis.
Beyond these experimental suggestions, the manuscript needs significant editing for clarity. While I won't provide a comprehensive list, the authors need to provide accurate descriptions and annotation of genotypes (including w[1118], which is written as W1118), typos, and formatting. I've listed a few examples below:
- Page 3, Line 1 and 2: "...have been shown to impact feeding behavior and metabolism that leads to..." This is an awkward and grammatically incorrect sentence.
- Page 3, Lines 7-32 is one very large paragraph but contains concepts that should be broken down over at least three paragraphs.
- Page 3, Line 25: A description of the reaction catalyzed by Pect would be helpful for a manuscript focused on Pecte activity.
- Page 4, Line 10: "previously characterized method of eliciting diet induced feeding behavior." As stated in the text, the method is previously described yet the manuscript characterizing the method isn't cited.
- Figure legend 3 contains a random assortment of capitalized lipid species. Also, the names of lipid species are inappropriately broken into multiple names. Please use correct nomenclature throughout the manuscript.
The list above is nowhere near comprehensive. The manuscript requires significant editing.
We are grateful to the reviewer for drawing our attention to these errors. We have made significant edits to the revised manuscript to address the above-mentioned concerns, as well as made additional textual changes throughout and copyedited it. We hope that the reviewer will find the manuscript reads better and the clarity and preciseness is significantly improved.
Reviewer #2 (Significance (Required)):
I find the study to be potentially very important - the authors combine a longitudinal study that would be difficult in any other model with the powerful genetic tools available in the fly. The findings will significantly advance our understanding of how lipid metabolism links dietary nutrition with feeding behavior.
Once again, we are grateful for this reviewer’s thoughtful critique and encouraging words regarding our work and its potential impact.
Reviewer #3 (Evidence, reproducibility and clarity (Required)):
Summary: This manuscript uses Drosophila to investigate how diet-induced obesity and the changes in the lipid metabolism of the fat boy modulate hunger-driven feeding (HDF) response. The authors first demonstrate that chronic exposure (14 days) of high sugar diet (HSD) suppresses HDF response. Through lipidome analysis, the authors identify a specific class of lipids to be elevated upon chronic HSD feeding. This coincided with the changes in expression of Pect, an enzyme that regulates the biosynthesis of these lipids. Modulating the expression of Pect specifically in the fat body affected HDF response.
We thank this reviewer for their rigorous and thoughtful critique and for identifying a key issue with our original study pertaining to a gap in how Pect mRNA levels on 14-day HSD are elevated but the Pect-KD phenocopies the HDF. Now by performing whole-body adult fly lipidomic on fat-specific Pect-KD we have resolved this issue and provided clarity on role of Pect in maintaining phospholipid homeostasis and thus subsequently impacts hunger-driven feeding. We hope the reviewer finds that the revised manuscript provides further clarity to the functional link between Pect’s role in fat-body and hunger-driven feeding.
Major comments: The author claim that the HDF response in HSD is distinct between early (5d, 7d) and chronic (day 14) HSD feeding. However, the data seem to indicate that HDF response is significantly decreased at all time points in HSD. For example, at day 5 HDF response was increased only 3-fold in HSD (Figure 1C) compared to around 50-fold increase in NF (Figure 1B). The scale of the Y-axis in Figure 1B and 1C is an order of magnitude different. Including the starved data (NFstv and HSDstv) in Figure S1, normalized to NF fed group, would better visualize the overall trends. Related to this, having the source data for the actual number of feeding events would be useful (e.g., to see the baseline changes in feeding in different time points in Figure 1 and the effect of genetic manipulations in Figure 7).
As per the reviewers request, we now have modified our graphs to show source data (Figure S1) and show the raw feeding events.
Then in the non-normalized graphs we plot, over a longitudinal time course, baseline and hunger-driven feeding events (Figure 1B-D). We also show that HSD fed flies do not display increased baseline feeding (Figure 1D) suggesting that the effect we see on HDF are no clouded by increased baseline feeding.
Yes, the reviewer makes an important point that HDF response on HSD fed flies is of a lower magnitude than NF fed flies. We think that is a biologically meaningful observation, as it suggests that flies have a remarkably fine-tuned ability to coordinate food-intake with nutrient store levels.
Now we have included a paragraph in the Discussion, Page 11 Lines 23-27, that say the following to ensure the readers appreciate this salient point raised by this reviewer.
*It is to be noted that the HDF response of HSD-fed flies (Figure 1C, Days 3-10) is of lower order of magnitude than the NF-fed flies. This suggests that that in addition to sensing an energy deficit and mobilizing fat stores (Figure 1F, 1G, S1), HSD fed flies calibrate their starvation-induced feeding to compensate only for the lost amount of fat. Overall, this suggests that flies have a remarkably fine-tuned ability to coordinate food-intake with nutrient store levels. *
The association between fat body Pect level and phospholipid levels is not clear. Day 14 of HSD feeding shows high expression of Pect in the fat body and elevated levels of PC32.0 and PC32.2. The authors assume the high expression of Pect in the fat body is due to the compensatory response, but there are no data indicating downregulation of Pect levels at the earlier time points of HSD feeding. A previous study demonstrated that Pect mutant flies have lower levels of PC32.0 but higher PC32.2 (PMID: 30737130).
We agree that one puzzling aspect of the original version of this study was that Pect mRNA levels being very high on Day 14 HSD, but nonetheless the effects of Pect-KD phenocopied HSD. To resolve this, prompted by Reviewer #2 and #3 concerns, for this revised version we have now performed lipidomic analyses on whole adult flies, when Pect is knocked down (KD) by RNAi in the fat tissue. We now present a new dataset in Figure 6. Two striking changes occu. They are:
- Pect-KD shows increase in the phospholipid classes LPC and LPE (Figure 6A). In contrast, LPE is significantly downregulated on HSD Day 14 (Figure 3).
- Pect-KD shows a significant reduction in specific class of PE 36.2 (Figure 6B). Our data regarding increase in PE 36.2 agree with a previous lipidomic analyses of Pect mutant retina (PMID: 30737130). In contrast, PE 36.2 trends upwards on 14 day HSD (Figure S7C) though not significantly. On 14-day HSD consistent with extreme upregulation of Pect mRNA fed flies (Figure S6A; Pect mRNA 200-250 fold), PE trends upwards on 14-day HSD (Figure 3) and PE 36.2 trends higher (Figure S7C). We note that on the surface of it PE and LPE per se are contrasting between 14-day HSD lipidome and fat-specifc Pect-KD. But there is a significant commonality that under both states there is an imbalance of phospholipids classes PE and LPE. Hence, we propose that maintaining the compositional balance of phospholipid classes PE and LPE is critical to hunger-driven feeding and insulin sensitivity. Hence, either increase or decrease, of these key phospholipid species, may lead to abnormal hunger-driven feeding.
On day 14, HDF response was increased 70-fold in w1118 flies in NF (Figure 1B; w1118), but only 2.5-fold in lpp>LucRNAi control flies in NF (Figure 7A). This suggests that lpp-gal4 driver lines have a significant effect on HDF response. Using a different fat-body specific Gal4 line would be necessary to validate conclusions.
Regards reduced HDF magnitude, in our experience using UAS-Gal4 reduces HDF response magnitude consistently and cannot be compared to w1118 which is more robust. To account for background differences, we use Uas-Gal4 with control RNAi. It clearly shows differences in HDF response on starvation, but Pect and Pisd RNAi does not (Figure 7A). Hence, given that this experiment internally controls for any changes in HDF response for UAS-Gal4>RNAi, we conclude that HDF response in disrupted in Pect and PISD KD (Figure 7).
We only presented the Lpp-driver in our study, as this driver is the only fat-specific driver that has no leaky expression in other tissues, and is specific to fat as apolpp promoter used to generate this Gal4 line is only expressed in fat tissue (Eaton and colleagues, PMID: 22844248). Other widely used fat-specific drivers, including the pumpless-Gal4 (ppl-Gal4) driver has leaky expression in gut or other tissues (See Table 2 of this detailed study by Dr. Drummond- Barbosa https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7642949/). If the reviewer is aware of a fat-specific Gal4 line, other than Lpp-Gal4, which has a highly specific expression in the fat tissue without leaky expression in other tissues, then we are happy to take onboard the reviewer’s suggestion and try that fat-specific Gal4 that they suggest.
HSD feeding promotes Pect expression (Figure S3C) and global changes in phospholipid levels (Figure 3, 4). Therefore, shouldn't Pect overexpression (not Pect RNAi) in a normal diet mimic HSD feeding state and promote loss of HDF response? Conversely shouldn't knockdown of Pect in HSD rescue loss of HDF response?
We agree that a puzzling aspect is that Pect mRNA levels are significantly elevated in HSD Day-14, but Pect-KD showed displays the inappropriate HDF response. As we have described in our response to this reviewer on Page 19, we believe that Pect-KD and HSD disrupt PE and LPE balance overall but in different ways. Whereas Pect-OE using cDNA expression in fat body does not cause a significant change to any lipid class (Figure S9), and our results suggest that basally higher level of PECT is likely to be protective on HSD with respect to HDF(Figure 7B).
To ensure that we appropriately discuss and clarify this issue, we have now included a section in the discussion - Page 14 Lines 26-33- under the subtitle “The implications of relationship between Pect levels and HSD”. We have pasted an excerpt from that subsection below for this reviewers assessment.
“Also, we note that over-expression of Pect cDNA in the fat-body does not alter phospholipid balance (Figure S9) and indeed improves HDF on HSD (Figure 7B). While this may appear inconsistent, it is critical to note that over-expression of Pect cDNA using UAS/Gal4 only increases Pect mRNA expression by 7-fold (Figure S6A), whereas HSD causes its upregulation by 250-fold (Figure S6B). Hence, we speculate that an increased ‘basal’ level of Pect such as by that provided by a cDNA over-expression in fat, may be protective to the negative effects of HSD (Figure 7B) without affecting overall phospholipid levels (Figure S9) , but extreme upregulation Pect on HSD affects the PE and LPE balance (Figure 3).”
We would have liked to test Pect protein expression on HSD, but since we were unable to access antibodies for Pect published in a prior study (PMID: 33064773) from Dr. Wang’s lab (see Page 10-11, of response to Reviewer #1). Hence, we were unable to test how the proteins levels of Pect correlate with the 250-fold increase mRNA expression.
In conclusion, we hope the reviewer appreciates that our results regarding Pect function are consistent with the main conclusion that achieving the right phospholipid balance between PE and LPE, is critical for an organism to display an appropriate HDF response.
Minor comments: All graphs should plot individual data points and showed as box and whisker plot as much as possible.
Thanks for this suggestion, we have added individual data points to the vast majority of figures in the paper. We have made exceptions to graphs such as seen in figure 1 and FigureS4B-D where we find individual data points add an unnecessary layer of complexity. We hope these changes provide additional clarity and strength to the claims made in this manuscript.
Data for day 14 missing in Figure S4A and S4B.
We have provided Day 14 for the PC composition and PE composition, due to changes in Figures, they are now S7A and S7B.
Reviewer #3 (Significance (Required)):
The interactions between diet-induced obesity, peripheral tissue homeostasis and feeding behavior is an interesting topic that can be addressed using Drosophila. This manuscript demonstrates how fat body Pect levels affect HSD induced changes in hunger-driven feeding response. However, at this point, the functional association between fat body Pect level, global phospholipid level, and loss of hunger-driven feeding response in chronic HSD feeding is not clear.
We hope the revised data, and discussion of the paper, provides well-substantiated functional association on the importance of maintaining phospholipid balance, driven by Pect enzyme, as a critical regulator of hunger-driven feeding behavior. As stated in the revised discussion, the key take home message of our manuscript is that on prolonged HSD exposure PC, PE and LPE levels are dysregulated, the loss of phospholipid homeostasis coincided with a loss of hunger-driven feeding. Following this lead on phospholipid imbalance, we then uncovered a critical requirement for the activity of the rate-limiting PE enzyme PECT within the fat tissue in controlling hunger-driven feeding.
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Referee #1
Evidence, reproducibility and clarity
Centriole duplication is a conserved pathway that need to be tightly regulated. The key enzyme of centriole assembly is Plk4 which is recruited to the centrioles and undergoes dynamic re-localization from a ring-like pattern around a centriole to a dot-like morphology at the daughter centriole assembly site. This event is central for inducing centriole biogenesis. Plk4 then phosphorylates Ana2/STIL which allows recruitment of Sas-6 to form the cartwheel structure for centriole assembly.
In the present study, Steinacker, Wong et al. monitor how cytoplasmic concentrations of the key proteins in centriole assembly, Plk4, Asl/Cep152, Ana2/STIL, Sas-6 and Sas-4/CPAP change during the centriole assembly process in the Drosophila embryo by using fluorescence correlation spectroscopy (FCS) and Peak Counting Spectroscopy (PeCoS). They find that their concentrations remain constant with exception of Ana2/STIL of which cytoplasmic diffusion rate increased at the end of S-phase and is dependent on phosphorylation by Cdk1/CyclinB. Phosphorylated Ana2/STIL blocks centriole duplication thus preventing premature initiation of centriole duplication in mitosis.
Major comments
The manuscript is interesting and very well written. Most of the experiments are carefully performed. However, there are some important aspects for improvements that are listed below
Additional experiments:
- Figure 3: the transgenic flies that were generated here, CC and STAN, still contain wild-type Ana2. So, the authors therefore need remove or dampen their claim that the change in Ana2's cytoplasmic diffusion does not depend on its interaction with Sas-6 (page 11).
- Figure 5A: is the observed reduced recruitment of Sas-6 by Ana2(12A) due to a decrease in binding affinity? This should also be shown by analyzing protein-protein interactions between Ana2(12A) and Sas-6 biochemically.
- The authors use an Ana2(12A) mutant which comprises putative Cdk1 phosphorylation sites that have been identified in Mc Lamarrah et al. JCB 2018. However, only three of them were phosphorylated by Cdk1/cyclin B in vitro (Fig. S6). Are all these 12 putative Cdk1 phosphorylation sites important in vivo? Did the authors generate the Ana2(3A) or the S284A/T301A mutants to see whether it can rescue the ana2-/- mutant phenotype similar to the 12A mutant? These might be sufficient to observe the phenotype.
- Figure 6: is the interaction between Plk4 and Ana2(12A) impaired? Similarly, Plk4 activity and phosphorylation of Ana2(12A) by Plk4
- Figure 7: Phosphomimetics, in this case 12 amino acid changes, have the disadvantage of introducing more negative charge than the phosphorylated residue. The Ana2/(12D/E)-mNG is not efficiently recruited to centrioles. Is effect also observed for the Ana2/(3D/E) mutant?
Minor comments
Figure S1: only mNG-tagged centriolar proteins are shown. An empty mNGtag or an mNG-tagged non-centriolar protein should be shown to exclude that the tag by itself shows centriolar localization or somehow affects the localization
S4C: Sas6-mNG CPM error bars are missing for the 10min time point
S5A: What are the expression levels of the Ana2(12A) mutant? The expression levels shown in this Figure are not similar.
Significance
Centriole duplication normally begins at the G1/S phase transition. An important question in the field is how premature centriole duplication in mitosis is prevented. The authors used fluorescence correlation spectroscopy (FCS) and Peak Counting Spectroscopy (PeCoS) to study the major conserved proteins in the centriole assembly pathwayq and found that only Ana2/STIL's cytoplasmic diffusion increases at the end of S-phase. It is known from the literature that Cdk1 prevent Plk4-STIL complex assembly in centriole biogenesis by directly competing with Plk4 for the CC domain of Ana2/STIL (Zitouni et al. Curr Biol 26, 1127-1137 (2016). However, Ana2/STIL can also bind to Plk4 via its conserved C-terminal region of STIL (Ohta et al., Cell Reports 11, 2018; McLamarrah et al., J Cell Biol 2018, 217, 1217-1231). The work by Steinacker, Wong et al. suggest that at least in fly embryos, growth of the daughter centriole is regulated though phosphorylation of Ana2 by Cdk1/CyclinB rather than binding. The findings described in this manuscript are interesting for a broad range of scientists from both the centrosome and mitosis fields
Expertise of the reviewer: centriole biogenesis, structural and numerical centrosomal aberrations in disease
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- Mar 2022
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- Oct 2020
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www.smithsonianmag.com www.smithsonianmag.com
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Why Are Finland’s Schools Successful? The country’s achievements in education have other nations, especially the United States, doing their homework <img src="https://thumbs-prod.si-cdn.com/thzZYTv2Evhq3x8iHdcaakihfVE=/800x600/filters:no_upscale()/https://public-media.si-cdn.com/filer/cd/ee/cdee1c82-f8e3-4de4-983e-8599d4485745/finland-smiles-wr.jpg" alt="Kirkkojarvi School" itemprop="image"> "This is what we do every day," says Kirkkojarvi Comprehensive School principal Kari Louhivuori, "prepare kids for life." (Stuart Conway) By LynNell Hancock Smithsonian Magazine | Subscribe September 2011 AddThis Sharing ButtonsShare to FacebookFacebookShare to TwitterTwitterShare to RedditReddit78Share to PinterestPinterest997Share to LinkedInLinkedInShare to FlipboardFlipboardShare to EmailEmailShare to PrintPrintShare to MoreAddThis934 It was the end of term at Kirkkojarvi Comprehensive School in Espoo, a sprawling suburb west of Helsinki, when Kari Louhivuori, a veteran teacher and the school’s principal, decided to try something extreme—by Finnish standards. One of his sixth-grade students, a Kosovo-Albanian boy, had drifted far off the learning grid, resisting his teacher’s best efforts. The school’s team of special educators—including a social worker, a nurse and a psychologist—convinced Louhivuori that laziness was not to blame. 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t="midroll".concat(e.midrollNumber);return r.adTagGenerator.generate(t,e.mediaId)}),f()(this,"generatePrerollTag",function(e,t){var n="preroll".concat(t);return r.adTagGenerator.generate(n,e)}),f()(this,"onAdTimeReached",function(){r.monetization.onMidrollAdOpportunity()}),f()(this,"onPreAdTimeReached",function(e){r.onPreMidrollAdOpportunity(e)}),f()(this,"onSeekToAdOpportunity",function(e){r.onPreMidrollAdOpportunity(e)}),f()(this,"isMidrollAlreadyRequested",function(e){return e.midrollNumber===r.lastRequestedMidroll.midrollNumber&&e.mediaId===r.lastRequestedMidroll.mediaId&&e.midrollTime===r.lastRequestedMidroll.midrollTime}),f()(this,"onPreMidrollAdOpportunity",function(e){if(Un(r.lastRequestedMidroll)||!r.isMidrollAlreadyRequested(e)){r.lastRequestedMidroll=e;var t=r.generateMidrollTag(e);r.monetization.onPreMidrollAdOpportunity(e,t)}}),f()(this,"onPrerollReached",function(e,t){var n=r.generatePrerollTag(e,t);r.monetization.onPrerollAdOpportunity(n)}),f()(this,"onSeekedWhileAdInProgress",function(){r.monetization.onMidrollAdOpportunity()});var i=t.getState;this.monetization=n,this.videoTimeSubscriber=new qi(t,this),this.videoSeekSubscriber=new zi(t,this),this.prerollScheduler=new Gi(t,this);var o=_i.adTagUrlTemplate(i());this.adTagGenerator=new Wi(o)},Yi=function(){function e(){Ai()(this,e)}return Vi()(e,null,[{key:"generateAdRequest",value:function(e,t,n){var r=new google.ima.AdsRequest;return r.adTagUrl=e,Fn()||r.setAdWillPlayMuted(t),r.vastLoadTimeout=n,r}}]),e}(),Zi=function(e){return function(t){t({type:"[MONETIZATION] change ad status",payload:e})}},Xi=function(e){return function(t){t({type:"[COMMON] set pending video status",payload:{pendingStatusObject:{type:e,value:""}}})}},Ji=function(e){return function(t){t({type:"[MONETIZATION] change loading ad status",payload:e})}},Qi=function(e){return function(t){t({type:"[MONETIZATION] update ad muted",payload:e})}},eo=function(e){return function(t){t({type:"[MONETIZATION] change ad volume",payload:e})}},to=function e(t,n,r,i,o){var a=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"IMAAdManager",void 0),f()(this,"adsLoader",void 0),f()(this,"adDisplayContainer",void 0),f()(this,"adVideoElement",void 0),f()(this,"videoPlayerElement",void 0),f()(this,"adContainerElement",void 0),f()(this,"anchorStatusStoreSubscriber",void 0),f()(this,"totalAdRequestMadeAmount",0),f()(this,"registerForWindowResize",function(){var e=zn(a.onResize.bind(a),80);window.addEventListener("resize",e)}),f()(this,"initMutationObserver",function(e){new MutationObserver(a.onResize).observe(e,{attributes:!0,childList:!1,subtree:!1})}),f()(this,"loadNewAd",function(e,t){var n=a.store.dispatch;a.clearOldAdManagerIfExist();var r=a.createAdRequest(e);try{a.validateAdRequestCorrectness(r),a.adsLoader.requestAds(r),function(e,t){return function(n){n({type:"[MONETIZATION] change ad 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google.ima.AdsLoader(t),a.adsLoader.getSettings().setDisableCustomPlaybackForIOS10Plus(!0),a.adsLoader.getSettings().setVpaidMode(google.ima.ImaSdkSettings.VpaidMode[n]),a.adsLoader.addEventListener(google.ima.AdsManagerLoadedEvent.Type.ADS_MANAGER_LOADED,a.onIMAAdsManagerLoaded.bind(a),!1,a),a.adsLoader.addEventListener(google.ima.AdErrorEvent.Type.AD_ERROR,a.onAdError.bind(a),!1,a)}),f()(this,"createAdRequest",function(e){var t=a.store.getState,n=gn.muted(t()),r=bi.adRequestTimeout(t());return Yi.generateAdRequest(e,n,r)}),f()(this,"validateAdRequestCorrectness",function(e){e&&e.adTagUrl&&decodeURIComponent(e.adTagUrl.replace(/\+/g," "))}),f()(this,"getLoadingError",function(e){var t=function(){return"bad ad request ".concat(JSON.stringify(e))};return{getError:function(){return{getMessage:t}}}}),f()(this,"getPlayAdError",function(e){var t=function(){return"play ad error: 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t=a.store,n=t.getState,r=t.dispatch,i=gn.volume(n());Bn()||gn.muted(n())?(e.setVolume(0),Qi(!0)(r)):(e.setVolume(gn.volume(n())),eo(i)(r),Qi(!1)(r))}),f()(this,"createIMAAdManager",function(t){a.IMAAdManager=t.getAdsManager(a.adVideoElement,e.getAdsRenderingSettings()),a.setAdVolume(a.IMAAdManager)}),f()(this,"registerToAdManagerEvents",function(){a.IMAAdManager.addEventListener(google.ima.AdErrorEvent.Type.AD_ERROR,a.onAdError),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.CONTENT_PAUSE_REQUESTED,a.onContentPauseRequested),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.CONTENT_RESUME_REQUESTED,a.onContentResumeRequested),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.STARTED,a.onAdStarted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.IMPRESSION,a.onAdImpression),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.SKIPPED,a.onAdSkipped),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.COMPLETE,a.onAdCompleted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.PAUSED,a.onAdPaused),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.RESUMED,a.onAdStarted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.AD_PROGRESS,a.onAdProgressChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.VOLUME_CHANGED,a.onVolumeChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.VOLUME_MUTED,a.onAdVolumeMutedChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.ALL_ADS_COMPLETED,a.onAdCompleted)}),f()(this,"onIMAAdsManagerLoaded",function(e){var t=a.store.dispatch;a.createIMAAdManager(e),a.registerToAdManagerEvents(),Zi("loaded")(t)}),f()(this,"onAdError",function(e){var t=a.store.dispatch;!function(e){return function(t){t({type:"[MONETIZATION] change ad error",payload:e})}}(e.getError().getMessage())(t),Ji(!1),a.continuePlayingContent()}),f()(this,"onAdImpression",function(e){var t=a.store.dispatch,n=!e.getAd().g.vpaid;a.setPodInfo(e),function(e){e({type:"[MONETIZATION] increase ad impression counter"})}(t),function(e){return function(t){t({type:"[MONETIZATION] update is vast ad",payload:e})}}(n)(t)}),f()(this,"onVolumeChanged",function(e){var t=a.store.dispatch;eo(e.target.getVolume())(t)}),f()(this,"onAdVolumeMutedChanged",function(e){var t=a.store.dispatch;0===e.target.getVolume()?Qi(!0)(t):Qi(!1)(t)}),f()(this,"continuePlayingContent",function(){var e=a.store,t=e.getState,n=e.dispatch,r=hn.videoTagStatus(t());Xi("idle"===r?"play":"resume")(n)}),f()(this,"stopPlayingContent",function(){var e=a.store.dispatch;Xi("pause")(e)}),f()(this,"onContentPauseRequested",function(){a.stopPlayingContent()}),f()(this,"onContentResumeRequested",function(){a.continuePlayingContent()}),f()(this,"onAdPaused",function(){var e=a.store.dispatch;Zi("paused")(e)}),f()(this,"setPodInfo",function(e){var t=e&&e.getAd()&&e.getAd().getAdPodInfo();if(!Un(t)){var n=a.store.dispatch;!function(e,t){return function(n){n({type:"[MONETIZATION] change pod info",payload:{slotNumber:e,podNumber:t}})}}(t.getAdPosition(),a.totalAdRequestMadeAmount)(n)}}),f()(this,"onAdStarted",function(){var e=a.store,t=e.dispatch,n=e.getState,r=gn.volume(n());Zi("playing")(t),0===a.IMAAdManager.getVolume()?a.IMAAdManager.setVolume(0):window.shouldPlayAdRule||a.IMAAdManager.setVolume(r),a.onResize()}),f()(this,"onAdCompleted",function(){var e=a.store.dispatch;Zi("completed")(e)}),f()(this,"onAdSkipped",function(){var e=a.store.dispatch;Zi("skipped")(e)}),f()(this,"onResize",function(){Un(a.IMAAdManager)||(a.IMAAdManager.resize(a.videoPlayerElement.clientWidth,a.videoPlayerElement.clientHeight,google.ima.ViewMode.NORMAL),a.adContainerElement.style.height="".concat(a.videoPlayerElement.clientHeight,"px"))}),f()(this,"onAdProgressChanged",function(e){var t,n,r=a.store,i=r.dispatch,o=r.getState,s=e.getAdData().currentTime,u=e.getAdData().duration,c=_i.adDuration(o());(t=s,function(e){e({type:"[MONETIZATION] change ad current time",payload:t})})(i),c!==u&&(n=u,function(e){e({type:"[MONETIZATION] change ad duration",payload:n})})(i)}),f()(this,"onAnchorStatusChanged",function(){var e=a.store.getState;"processing"!==Pr(e())&&a.onResize()}),f()(this,"changeAdVolume",function(e){Un(a.IMAAdManager)||a.IMAAdManager.setVolume(e)}),f()(this,"changeAdMuted",function(e,t){Un(a.IMAAdManager)||(t?a.IMAAdManager.setVolume(0):a.IMAAdManager.setVolume(e))}),f()(this,"changeAdStatus",function(e){Un(a.IMAAdManager)||("playing"===e&&a.IMAAdManager.resume(),"paused"===e&&a.IMAAdManager.pause())});var s=t.getState;this.store=t,this.adVideoElement=r,this.videoPlayerElement=i,this.adContainerElement=n,this.adDisplayContainer=new google.ima.AdDisplayContainer(n,r),this.createAdLoader(s(),this.adDisplayContainer),this.adDisplayContainer.initialize(),this.anchorStatusStoreSubscriber=new ji(t,e.getAnchorDependencies,this.onAnchorStatusChanged.bind(this)),this.registerForWindowResize(),this.initMutationObserver(o)};f()(to,"getAdsRenderingSettings",function(){var e=new google.ima.AdsRenderingSettings;return e.restoreCustomPlaybackStateOnAdBreakComplete=!0,e.enablePreloading=!1,e.uiElements=[],e.loadVideoTimeout=15e3,e}),f()(to,"getAnchorDependencies",function(e){return[Pr(e)]});var no=function e(t,n,r,i,o,a){var s=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"playerId",void 0),f()(this,"adScheduler",void 0),f()(this,"adHandler",void 0),f()(this,"imaLoadingStatusSubscriber",void 0),f()(this,"adStatusSubscriber",void 0),f()(this,"videoTagStatusSubscriber",void 0),f()(this,"adContainer",void 0),f()(this,"adVideoElement",void 0),f()(this,"videoPlayerElement",void 0),f()(this,"playerContainer",void 0),f()(this,"pendingMidrollAdPlay",!1),f()(this,"pendingPrerollAdPlay",!1),f()(this,"pendingPrerollAdTag",null),f()(this,"pendingMidrollNumber",null),f()(this,"pendingAdStatusStoreSubscriber",void 0),f()(this,"adMutedStoreSubscriber",void 0),f()(this,"adVolumeStoreSubscriber",void 0),f()(this,"onMidrollAdOpportunity",function(){var e=s.store,t=e.dispatch,n=e.getState,r=_i.adStatus(n()),i=bi.continuePlayingWhileWaitingForAd(n());"loaded"===r?s.playAd(!0):"requested"===r&&(s.pendingMidrollAdPlay=!0,i||(Xi("pause")(t),Ji(!0)(t))),function(e){e({type:"[MONETIZATION] increase ad Opportunity counter"})}(t)}),f()(this,"onPrerollAdOpportunity",function(e){var t=s.store,n=t.getState,r=t.dispatch,i=Fi.loadingImaStatus(n());Un(s.adHandler)?"loading"!==i&&""!==i||(Ji(!0)(r),s.pendingPrerollAdPlay=!0,s.pendingPrerollAdTag=e):(s.pendingPrerollAdPlay=!0,Ji(!0)(r),s.adHandler.loadNewAd(e,"preroll"))}),f()(this,"onPreMidrollAdOpportunity",function(e,t){Un(s.adHandler)||(e.currentTime>=e.midrollTime&&(s.pendingMidrollAdPlay=!0),s.pendingMidrollNumber=e.midrollNumber,s.adHandler.loadNewAd(t,"midroll"))}),f()(this,"hasPendingAd",function(){return s.hasPendingMidrollAdPlay()||s.hasPendingPrerollAdPlay()}),f()(this,"onAdStatusChanged",function(e){var t=s.store.dispatch,n=_i.adStatus(e);"completed"===n&&Ji(!1)(t);var r=bi.continuePlayingWhileWaitingForAd(e),i=_i.loadingAd(e);"playing"!==n&&"error"!==n||r||!i||Ji(!1)(t),s.hasPendingAd()&&"loaded"===n?s.playAd(s.hasPendingMidrollAdPlay()):s.hasPendingAd()&&"error"===n?(Ji(!1),s.clearPendingMidroll(),s.clearPendingPreroll()):Hi(n)||(Ji(!1),function(e){e({type:"[MONETIZATION] clear ad data"})}(t))}),f()(this,"clearPendingMidroll",function(){s.pendingMidrollNumber=null,s.pendingMidrollAdPlay=!1}),f()(this,"clearPendingPreroll",function(){s.pendingPrerollAdPlay=!1,s.pendingPrerollAdTag=null}),f()(this,"onVideoTagStatusChanged",function(e){"complete"===hn.videoTagStatus(e)&&function(e){e({type:"[MONETIZATION] clear played midrolls"})}(s.store.dispatch)}),f()(this,"hasPendingMidrollAdPlay",function(){return s.pendingMidrollAdPlay}),f()(this,"hasPendingPrerollAdPlay",function(){return s.pendingPrerollAdPlay}),f()(this,"playAd",function(e){var t,n=s.store.dispatch,r=s.adHandler.playAd();e?((t=s.pendingMidrollNumber,function(e){e({type:"[MONETIZATION] add 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Ki(t,this),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this)),this.videoTagStatusSubscriber=new ji(t,e.getVideoTagStatusDependencies,this.onVideoTagStatusChanged.bind(this)),e.canUseIMA(u())?this.adHandler=new to(t,r,i,o,a):this.imaLoadingStatusSubscriber=new ji(t,e.getIMALoadingStatusDependencies,this.onIMALoadingStatusChanged.bind(this)),this.pendingAdStatusStoreSubscriber=new ji(t,e.getPendingAdStatusDependencies,this.onPendingAdStatusChanged.bind(this)),this.adMutedStoreSubscriber=new ji(t,e.getAdMutedDependencies,this.onAdMutedChanged.bind(this)),this.adVolumeStoreSubscriber=new ji(t,e.getAdVolumeDependencies,this.onAdVolumeChanged.bind(this))};f()(no,"getAdStatusDependencies",function(e){return[_i.adStatus(e)]}),f()(no,"getVideoTagStatusDependencies",function(e){return[hn.videoTagStatus(e)]}),f()(no,"getIMALoadingStatusDependencies",function(e){return[Fi.loadingImaStatus(e)]}),f()(no,"canUseIMA",function(e){return"success"===Fi.loadingImaStatus(e)}),f()(no,"getPendingAdStatusDependencies",function(e){return[_i.pendingAdStatus(e)]}),f()(no,"getAdMutedDependencies",function(e){return[_i.adMuted(e)]}),f()(no,"getAdVolumeDependencies",function(e){return[_i.adVolume(e)]});var ro=function(e,t){!function(e,t){var n=document.getElementById(vn(t));B(b(Li,{store:e,playerId:t}),n)}(e,t);var n=function(e){var t=Ri(e);return document.getElementById(t)}(t),r=function(e){var t=Bn()?Di(e):En(e);return document.getElementById(t)}(t),i=function(e){var t=En(e);return document.getElementById(t)}(t),o=function(e){var t=bn(e);return document.getElementById(t)}(t);return new no(e,t,n,r,i,o)},io=n(4),oo=n.n(io),ao=n(7),so=n.n(ao),uo=function(){function e(){Ai()(this,e),f()(this,"duration",void 0),f()(this,"position",void 0),f()(this,"previousPosition",void 0),f()(this,"loadTime",void 0),f()(this,"adOrder",void 0),f()(this,"adType",void 0),f()(this,"adDuration",void 0),f()(this,"errorMessage",void 0),f()(this,"adPodNumber",void 0),f()(this,"adSlotNumber",void 0)}return Vi()(e,[{key:"setDuration",value:function(e){return this.duration=e,this}},{key:"setPosition",value:function(e){return this.position=e,this}},{key:"setPreviousPosition",value:function(e){return this.previousPosition=e,this}},{key:"setLoadTime",value:function(e){return this.loadTime=e,this}},{key:"setAdOrder",value:function(e){return this.adOrder=e,this}},{key:"setAdType",value:function(e){return this.adType=e,this}},{key:"setAdDuration",value:function(e){return this.adDuration=e,this}},{key:"setErrorMessage",value:function(e){return this.errorMessage=e,this}},{key:"setAdPodNumber",value:function(e){return this.adPodNumber=e,this}},{key:"setAdSlotNumber",value:function(e){return this.adSlotNumber=e,this}},{key:"build",value:function(){var e=[];return jn(this.position)||e.push("video current position=".concat(Hn(this.position),"sec")),jn(this.duration)||e.push("video duration time=".concat(Hn(this.duration),"sec")),jn(this.loadTime)||e.push("video load time=".concat(this.loadTime,"milliseconds")),jn(this.previousPosition)||e.push("previous position=".concat(Hn(this.previousPosition),"sec")),jn(this.adOrder)||e.push("ad order=".concat(this.adOrder)),jn(this.adType)||e.push("ad type=".concat(this.adType)),jn(this.adDuration)||e.push("ad duration=".concat(Hn(Number(this.adDuration)),"sec")),jn(this.adPodNumber)||e.push("pod number=".concat(this.adPodNumber)),jn(this.adSlotNumber)||e.push("slot number=".concat(this.adSlotNumber)),jn(this.errorMessage)||e.push("error message=".concat(this.errorMessage)),e.join(";")}}]),e}(),co="mmPlus GTM data ready to GA",lo="mmPlus GTM event to GA",po={EMBED:"vplayer video player embed",FIRST_PLAY:"vplayer video first play",COMPLETION_25_PERCENTAGE:"vplayer video 25% complete",COMPLETION_50_PERCENTAGE:"vplayer video 50% complete",COMPLETION_75_PERCENTAGE:"vplayer video 75% complete",COMPLETION_90_PERCENTAGE:"vplayer video 90% complete",AD_BLOCK:"vplayer video ad block",AD_REQUEST:"vplayer video ad request",AD_IMPRESSION:"vplayer video ad impression",AD_ERROR:"vplayer video ad error",AD_VIEWABLE_IMPRESSION:"vplayer video ad viewable impression",AD_COMPLETE:"vplayer video ad complete",AD_SKIP:"vplayer video ad skip",AD_PAUSE:"vplayer video ad pause",VIDEO_COMPLETE:"vplayer video complete",FULLSCREEN_ON:"vplayer video fullscreen on",FULLSCREEN_OFF:"vplayer video fullscreen off",SEEK:"vplayer video position seeked",VIDEO_MUTE:"vplayer video mute",VIDEO_UNMUTE:"vplayer video unmute",CONTROLS_MUTE_OR_UNMUTE:"controls 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t=gn.fullscreen(e),n=hn.currentVideoTimeFragment(e),i=(new uo).setPosition(n).build(),o=t?po.FULLSCREEN_ON:po.FULLSCREEN_OFF;r.analyticsEventsCallbacks.onEvent(o,i)}),this.store=t,this.analyticsEventsCallbacks=n,this.videoMuteSubscriber=new ji(t,e.getVideoMuteDependencies,this.onMuteStateChanged.bind(this)),this.videoFullscreenSubscriber=new ji(t,e.getVideoFullscreenDependencies,this.onFullsScreenStateChanged.bind(this))};f()(yo,"getVideoMuteDependencies",function(e){return[gn.muted(e)]}),f()(yo,"getVideoFullscreenDependencies",function(e){return[gn.fullscreen(e)]});var go=n(3),vo=n.n(go),mo=n(8),bo=n.n(mo),Oo=n(9),_o=n.n(Oo),So=n(5),Eo=n.n(So);n(20);var wo={root:null,threshold:.5,rootMargin:"0px"},Po=function(){function e(t,n,r){Ai()(this,e),f()(this,"store",void 0),f()(this,"observableElement",void 0),f()(this,"callback",void 0),f()(this,"isViewableTimeoutHandler",null),f()(this,"observer",void 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The initial state may not be undefined, but can be null.')})}(n)}catch(s){o=s}return function(e,t){if(void 0===e&&(e={}),o)throw o;for(var r=!1,i={},s=0;s<a.length;s++){var u=a[s],c=n[u],l=e[u],d=c(l,t);if("undefined"===typeof d){var p=mt(u,t);throw new Error(p)}i[u]=d,r=r||d!==l}return(r=r||a.length!==Object.keys(e).length)?i:e}}({dependenciesLoadingStatus:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:da,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] update hls status":return la(la({},e),{},{loadingHLSStatus:t.payload});case"[CORE] update ima status":return la(la({},e),{},{loadingImaStatus:t.payload});default:return e}},playerData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:ha,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":var n=t.payload;return fa({},function(e,t,n){var r=t.playback_method,i=t.player_id;return fa(fa({},e),{},{playbackMethod:Un(r)?e.playbackMethod:r,playerId:Un(i)?e.playerId:i,playerInstanceUniqId:n,playerMode:Fn()?"mobile":"desktop"})}(e,n.initiateParams,n.playerInstanceUniqId));case"[CORE] reset player data time params":return fa(fa({},e),{},{currentVideoTimeFragment:0,currentVideoBufferedTime:0,currentVideoDuration:0,currentVideoTime:0});case"[COMMON] set mute video":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{muted:t.payload})});case"[COMMON] set volume":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{volume:t.payload})});case"[COMMON] change selected settings category":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{selectedSettingsCategory:t.payload})});case"[COMMON] change settings speed":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{speed:t.payload})});case"[COMMON] change settings quality":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{quality:t.payload})});case"[COMMON] set fullscreen":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{fullscreen:fa(fa({},e.playerSettings.fullscreen),{},{isFullscreenOn:t.payload,pendingFullscreenRequest:""})})});case"[COMMON] set fullscreen request":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{fullscreen:fa(fa({},e.playerSettings.fullscreen),{},{pendingFullscreenRequest:t.payload})})});case"[COMMON] set pending video status":var r=t.payload.pendingStatusObject;return fa(fa({},e),{},{pendingVideoTagStatus:fa({},r)});case"[COMMON] set player mode":return fa(fa({},e),{},{playerMode:t.payload});case"[CORE] update video current fragment position":return fa(fa({},e),{},{currentVideoTimeFragment:t.payload});case"[CORE] update video current position":return fa(fa({},e),{},{currentVideoTime:t.payload});case"[CORE] update video current buffered time":return fa(fa({},e),{},{currentVideoBufferedTime:t.payload});case"[CORE] update video current duration":return fa(fa({},e),{},{currentVideoDuration:t.payload});case"[CORE] change video tag status":return fa(fa({},e),{},{videoTagStatus:t.payload});case"[CORE] update player visibility":return fa(fa({},e),{},{playerVisibility:t.payload});case"[CORE] update placeholder visibility":return fa(fa({},e),{},{playerPlaceholderVisibility:t.payload});case"[CORE] change loading player status":return fa(fa({},e),{},{loadingPlayer:t.payload});case"[COMMON] show black screen with loader":return fa(fa({},e),{},{loader:fa(fa({},e.loader),{},{showBlackScreen:t.payload})});case"[CORE] set player size":return fa(fa({},e),{},{playerSize:t.payload});case"[COMMON] set error message":return fa(fa({},e),{},{errorMessage:t.payload});default:return e}},brandingData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:va,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return ga({},function(e,t){var n=t.powered_by_strip,r=t.brand_logo,i=t.brand_logo_click_url,o=t.brand_color;return ga(ga({},e),{},{showVoltaxLogo:Un(n)?e.showVoltaxLogo:n,brandingLogoSrc:Un(r)?e.brandingLogoSrc:r,brandingLogoUrl:Un(i)?e.brandingLogoUrl:i,brandingColor:Un(o)?e.brandingColor:o})}(e,t.payload.initiateParams));default:return e}},anchorOptions:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Oa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return ba({},function(e,t){var n=t.anchor_options;if(!Un(n)){var r=n.anchoring_appearance,i=n.can_close,o=n.closable_ad,a=n.close_after,s=n.continue_streaming,u=n.orientation,c=n.margins,l=n.sticky_below_class_name,d=n.width,p=Un(c)?e.margins:{top:Number.isInteger(c.top)?c.top:e.margins.top,bottom:Number.isInteger(c.bottom)?c.bottom:e.margins.bottom,left:Number.isInteger(c.left)?c.left:e.margins.left,right:Number.isInteger(c.right)?c.right:e.margins.right};return ba(ba({},e),{},{anchoringAppearance:r||e.anchoringAppearance,canClose:Un(i)?e.canClose:i,orientation:Un(u)?e.orientation:u,closableAd:Un(o)?e.closableAd:o,closeAfter:Un(a)?e.closeAfter:a,continueStreaming:Un(s)?e.continueStreaming:s,stickyBelowClassName:Un(l)?e.stickyBelowClassName:l,width:Un(d)?e.width:d,margins:p,anchorData:ba(ba({},e.anchorData),{},{anchorEnabled:!0})})}return e}(e,t.payload.initiateParams));case"[COMMON] set anchor enable":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorEnabled:t.payload})});case"[ANCHOR] update is anchor status":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorStatus:t.payload})});case"[COMMON] set anchor disabled by user":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorDisabledByUser:t.payload})});default:return e}},monetization:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:wa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Sa({},function(e,t){var n=t.monetization;if(Un(n))return e;var r=n.ad_tag,i=n.ad_type,o=n.vpaid_mode,a=n.ad_request_timeout,s=n.continue_content_play_while_waiting_for_ad,u=n.midrolls,c=u&&u.on&&u.on.sort(Wn),l=Un(s)?e.continuePlayingWhileWaitingForAd:s,d=c?c.indexOf(0):-1,p=-1!==d&&!l;return p&&(c=c.splice(d,1)),Sa(Sa({},e),{},{midrolls:Sa(Sa({},e.midrolls),{},{every:u&&u.every,on:c}),prerollEnabled:p,adRequestTimeout:Un(a)?e.adRequestTimeout:parseInt(a,10),vpaidMode:Un(o)?e.vpaidMode:o,continuePlayingWhileWaitingForAd:l,adsData:Sa(Sa({},e.adsData),{},{adType:Un(i)?e.adsData.adType:i,adTagUrlTemplate:Un(r)?e.adsData.adTagUrlTemplate:r})})}(e,t.payload.initiateParams));case"[COMMON] set new ad tag url template":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adTagUrlTemplate:t.payload})});case"[MONETIZATION] change ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adStatus:t.payload,adErrorMessage:null})});case"[MONETIZATION] change ad tag":var n=t.payload,r=n.adUnit,i=n.adTag;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{currentAdTag:i,adUnit:r})});case"[MONETIZATION] change pending ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{pendingAdStatus:t.payload})});case"[MONETIZATION] change ad error":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adStatus:"error",adErrorMessage:t.payload})});case"[MONETIZATION] increase ad impression counter":var o=e.adsData.adImpression;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adImpression:o+1})});case"[MONETIZATION] increase ad Opportunity counter":var a=e.adsData.adOpportunity;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOpportunity:a+1})});case"[MONETIZATION] add played midroll number":var s=e.adsData.playedMidrolls,u=In()(s);return u.push(t.payload),Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOrder:t.payload,playedMidrolls:u})});case"[MONETIZATION] clear played midrolls":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{playedMidrolls:[]})});case"[MONETIZATION] clear ad data":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOrder:0,currentAdTag:null,adDuration:0,adUnit:""})});case"[MONETIZATION] change ad duration":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adDuration:t.payload})});case"[MONETIZATION] update is vast ad":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{isVastAd:t.payload})});case"[MONETIZATION] change ad current time":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adCurrentTime:t.payload})});case"[MONETIZATION] update ad muted":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adMuted:t.payload})});case"[MONETIZATION] change ad volume":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adVolume:t.payload})});case"[MONETIZATION] change pod info":var c=t.payload,l=c.podNumber,d=c.slotNumber;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{podNumber:l,slotNumber:d})});case"[MONETIZATION] change loading ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{loadingAd:t.payload})});default:return e}},mediaData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:ja,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Va({},function(e,t){var n=t.content_type,r=t.media_id,i=t.display_title;return Va(Va({},e),{},{mediaType:Un(n)?e.mediaType:n,mediaId:Un(r)?e.mediaId:r,videoData:Va(Va({},e.videoData),{},{showTitle:!!Un(i)||i})})}(e,t.payload.initiateParams));case"[CORE] load video request":return Va(Va({},e),{},{loadingMedia:!0});case"[CORE] load video request success":return Va(Va({},e),{},{loadingMedia:!1,videoList:t.payload});case"[CORE] set current video":var n=t.payload,r=n.index,i=n.videoData;return Va(Va({},e),{},{activeVideoIndex:r,videoData:i});case"[CORE] load video request error":return Va(Va({},e),{},{loadingMedia:!1,mediaLoadingError:t.payload});case"[COMMON] media request":var o=t.payload.mediaRequestObject;return Va(Va({},e),{},{mediaRequest:Va({},o)});default:return e}},semanticOptions:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Ba,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Fa({},function(e,t){var n=t.semantic_options;if(Un(n))return e;var r=n.minimum_date_factor,i=n.promoted_videos,o=n.scan_images_on_page,a=n.scanned_element,s=n.scanned_element_type,u=n.scoped_keywords,c=n.tags;return Fa(Fa({},e),{},{minimumDateFactor:Un(r)?e.minimumDateFactor:r,promotedVideos:Un(i)?e.promotedVideos:i,scanImagesOnPage:Un(o)?e.scanImagesOnPage:o,scannedElement:Un(a)?e.scannedElement:a,scannedElementType:Un(s)?e.scannedElementType:s,scopedKeywords:Un(u)?e.scopedKeywords:u,tags:Un(c)?e.tags:c})}(e,t.payload.initiateParams));default:return e}},userInteraction:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Wa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[USER INTERACTION] change user interaction":return qa(qa({},e),{},{userInteractionType:t.payload});default:return e}},splitView:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:$a,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Ga({},function(e,t){var n=t.anchor_options;if(!Un(n)){var r=n.split_view,i=n.split_view_ratio;return Ga(Ga({},e),{},{splitViewRatio:Un(r)||!r||Un(i)?e.splitViewRatio:i})}return e}(e,t.payload.initiateParams));default:return e}},discovery:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Za,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Ya({},function(e,t){var n=t.next_video;return Un(n)?e:Ya(Ya({},e),{},{nextVideo:Xa(n)})}(e,t.payload.initiateParams));case"[DISCOVERY] show up next":return Ya(Ya({},e),{},{showUpNext:t.payload});case"[DISCOVERY] show skippable content":return Ya(Ya({},e),{},{showSkippableContent:t.payload});default:return e}}}),Qa=[],es=!1,ts=function e(){return function(t){return function(n){if(es)return Qa.push(n),null;es=!0;var r=t(n);return es=!1,Qa.length>0&&e()(t)(Qa.shift()),r}}},ns=function(e){var t=[];if(function(e){return!Un(e)&&!Un(e.enable_redux_debugging)&&e.enable_redux_debugging}(e)){var n=window&&window.__REDUX_DEVTOOLS_EXTENSION__&&window.__REDUX_DEVTOOLS_EXTENSION__();"function"===typeof n&&t.push(n)}var r=Et.apply(void 0,[wt(ua,ts)].concat(t));return vt(Ja,r)},rs=function(){function e(t){Ai()(this,e),f()(this,"playerVisibilitySubscriber",void 0),f()(this,"videoTagStatusSubscriber",void 0),f()(this,"shouldPlayIfLazyplay",!0),f()(this,"shouldPlayIfAutoplayWhenViewable",!0),f()(this,"videoPausedByObserver",!1),this.store=t,this.playerVisibilitySubscriber=null,this.videoTagStatusSubscriber=null,this.playAccordingToPlaybackMethod()}return Vi()(e,[{key:"lazyplayHandler",value:function(e){hn.playerVisibility(e)>=.5&&(this.playVideo(),this.shouldPlayIfLazyplay=!1)}},{key:"autoplayWhenViewableHandler",value:function(e){hn.playerVisibility(e)>=.5?this.playVideo():this.pauseVideo()}},{key:"onPlayerVisibilityChanged",value:function(e){var t=hn.playbackMethod(e);"lazyplay"===t&&this.shouldPlayIfLazyplay&&this.lazyplayHandler(e),"autoplay_when_viewable"===t&&this.shouldPlayIfAutoplayWhenViewable&&this.autoplayWhenViewableHandler(e)}},{key:"onVideoTagStatusChanged",value:function(e){var t=hn.videoTagStatus(e);"paused"!==t||this.videoPausedByObserver||(this.shouldPlayIfAutoplayWhenViewable=!1),"playing"===t&&(this.shouldPlayIfAutoplayWhenViewable=!0,this.videoPausedByObserver=!1)}},{key:"initiatePlayerVisibilitySubscriber",value:function(){this.playerVisibilitySubscriber=new ji(this.store,e.getPlayerVisibilityDependencies,this.onPlayerVisibilityChanged.bind(this))}},{key:"initiateVideoTagStatusSubscriber",value:function(){this.videoTagStatusSubscriber=new ji(this.store,e.getVideoTagStatusDependencies,this.onVideoTagStatusChanged.bind(this))}},{key:"playVideo",value:function(){var e=this.store,t=e.dispatch,n=e.getState;"idle"===hn.videoTagStatus(n())?on("play")(t):on("resume")(t)}},{key:"pauseVideo",value:function(){var e=this.store,t=e.dispatch,n=e.getState;"paused"!==hn.videoTagStatus(n())&&(this.videoPausedByObserver=!0,on("pause")(t))}},{key:"playAccordingToPlaybackMethod",value:function(){var e=this.store,t=e.dispatch,n=(0,e.getState)();switch(hn.playbackMethod(n)){case"autoplay":this.playVideo();break;case"lazyplay":this.initiatePlayerVisibilitySubscriber();break;case"autoplay_when_viewable":this.initiatePlayerVisibilitySubscriber(),this.initiateVideoTagStatusSubscriber();break;case"none":an(!1)(t)}}}],[{key:"getPlayerVisibilityDependencies",value:function(e){return[hn.playerVisibility(e)]}},{key:"getVideoTagStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}}]),e}(),is=function(){function e(t,n,r,i){var o=this;Ai()(this,e),f()(this,"videoStatusSubscriber",void 0),f()(this,"videoListSubscriber",void 0),f()(this,"mediaRequestSubscriber",void 0),f()(this,"playerVisibilitySubscriber",void 0),f()(this,"playbackMethodManager",void 0),f()(this,"store",void 0),f()(this,"loadContent",function(e,t,n,r){o.loadMedia(t,n,r).then(function(){o.playbackMethodManager=new rs(e)})}),f()(this,"loadMedia",function(e,t,n){var r=o.store,i=r.dispatch,a=r.getState,s=Dn.showTitle(a());if("semantic"===e){var u=pn.semanticOptions(a());return Na(u,s,n)(i)}return ka(t,s,n)(i)}),this.store=t,this.videoStatusSubscriber=new ji(t,e.getVideoStatusDependencies,this.onVideoStatusChanged.bind(this)),this.videoListSubscriber=new ji(t,e.getVideoListDependencies,this.onVideoListChanged.bind(this)),this.mediaRequestSubscriber=new ji(t,e.getMediaRequestDependencies,this.onMediaRequestChanged.bind(this)),this.playerVisibilitySubscriber=null,this.loadContent(t,r,n,i)}return Vi()(e,null,[{key:"createInstance",value:function(t,n,r,i){return new e(t,n,r,i)}}]),Vi()(e,[{key:"playNextVideo",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e),r=Cn.activeVideoIndex(e)+1;n.length>1&&r>=n.length&&(r=0),r<n.length&&(!function(e){e({type:"[CORE] reset player data time params"})}(t),La(r,n[r])(t),on("play")(t))}},{key:"playPreviousVideo",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e),r=Cn.activeVideoIndex(e);if(r>0){var i=r-1;La(i,n[i])(t),on("play")(t)}}},{key:"onVideoStatusChanged",value:function(e){"complete"===hn.videoTagStatus(e)&&this.playNextVideo(e)}},{key:"onVideoListChanged",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e);!jn(n)&&n.length>0&&La(0,n[0])(t)}},{key:"onMediaRequestChanged",value:function(e){var t=Cn.mediaRequest(e);switch(t.type){case"playNewVideo":this.loadMedia("specific",t.value);break;case"playNextVideo":this.playNextVideo(e);break;case"playPreviousVideo":this.playPreviousVideo(e)}}}],[{key:"getVideoStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}},{key:"getVideoListDependencies",value:function(e){return[Cn.videoList(e)]}},{key:"getMediaRequestDependencies",value:function(e){return[Cn.mediaRequest(e)]}}]),e}(),os=function e(t){var n=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"onDependencyFailure",function(e,t){console.log("onDependencyFailure",e,t);var r=n.store,i=r.dispatch,o=r.getState;switch(e){case"ima":"blocked"!==Fi.loadingImaStatus(o())&&Qn("error")(i);break;case"hls":er("error")(i)}}),f()(this,"onDependencyReady",function(e){var t=n.store.dispatch;switch(e){case"ima":Qn("success")(t);break;case"hls":er("success")(t)}}),this.store=t},as=function(e){return function(t){t({type:"[COMMON] set fullscreen",payload:e})}},ss=function(){function e(t,n){var r=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"videoTag",void 0),f()(this,"pendingFullscreenSubscriber",void 0),f()(this,"adStatusSubscriber",void 0),f()(this,"playerUniqId",void 0),f()(this,"onAdStatusChanged",function(e){var t=_i.adStatus(e),n=r.videoTag.webkitDisplayingFullscreen;"playing"===t&&Bn()&&n&&r.exitFullscreen(r.videoTag)}),f()(this,"isPlayerInFullscreen",function(){var e=document,t=Bn()?En(r.playerUniqId):bn(r.playerUniqId);return Un(e.fullscreenElement)?!Un(e.webkitFullscreenElement)&&0===e.webkitFullscreenElement.id.localeCompare(t):0===e.fullscreenElement.id.localeCompare(t)}),f()(this,"changePlayerWidth",function(e){r.videoTag.style.width=e?"100%":"auto"}),f()(this,"onFullscreenChanged",function(){var e=r.store.dispatch,t=r.isPlayerInFullscreen();r.changePlayerWidth(t),as(t)(e)}),f()(this,"onFullscreenChangedIos",function(){var e=r.store.dispatch,t=r.videoTag.webkitDisplayingFullscreen;t||on("resume")(e),r.changePlayerWidth(t),as(t)(e)}),f()(this,"onPendingFullscreenRequestChanged",function(e){var t=gn.pendingFullscreenRequest(e);"enter"===t?r.enterFullscreen(r.videoTag):"exit"===t&&r.exitFullscreen(r.videoTag)}),f()(this,"getFullScreenElement",function(e,t){var n=document.getElementById(bn(r.playerUniqId));return Bn()?t:e?document:n}),f()(this,"enterFullscreen",function(e){var t=r.getFullScreenElement(!1,e);Bn()?t.webkitEnterFullscreen():document.webkitExitFullscreen?t.webkitRequestFullscreen():document.webkitCancelFullScreen?t.webkitRequestFullScreen():document.mozCancelFullScreen?t.mozRequestFullScreen():document.msExitFullscreen&&t.msRequestFullscreen()}),f()(this,"exitFullscreen",function(e){var t=r.getFullScreenElement(!0,e);document.webkitExitFullscreen||Bn()?t.webkitExitFullscreen():document.webkitCancelFullScreen?t.webkitCancelFullScreen():document.mozCancelFullScreen?t.mozCancelFullScreen():document.msExitFullscreen&&t.msExitFullscreen()}),this.store=t,this.videoTag=document.getElementById(En(n)),this.playerUniqId=n,document.addEventListener("fullscreenchange",this.onFullscreenChanged.bind(this)),document.addEventListener("webkitfullscreenchange",this.onFullscreenChanged.bind(this)),Bn()&&(this.videoTag.addEventListener("webkitendfullscreen",this.onFullscreenChangedIos.bind(this)),this.videoTag.addEventListener("webkitbeginfullscreen",this.onFullscreenChangedIos.bind(this))),this.pendingFullscreenSubscriber=new ji(t,e.getPendingFullscreenDependencies,this.onPendingFullscreenRequestChanged.bind(this)),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this))}return Vi()(e,null,[{key:"createInstance",value:function(t,n){return new e(t,n)}}]),Vi()(e,null,[{key:"getPendingFullscreenDependencies",value:function(e){return[gn.pendingFullscreenRequest(e)]}},{key:"getAdStatusDependencies",value:function(e){return[_i.adStatus(e)]}}]),e}();function us(e,t){var n=Object.keys(e);if(Object.getOwnPropertySymbols){var r=Object.getOwnPropertySymbols(e);t&&(r=r.filter(function(t){return Object.getOwnPropertyDescriptor(e,t).enumerable})),n.push.apply(n,r)}return n}function cs(e){for(var t=1;t<arguments.length;t++){var n=null!=arguments[t]?arguments[t]:{};t%2?us(Object(n),!0).forEach(function(t){f()(e,t,n[t])}):Object.getOwnPropertyDescriptors?Object.defineProperties(e,Object.getOwnPropertyDescriptors(n)):us(Object(n)).forEach(function(t){Object.defineProperty(e,t,Object.getOwnPropertyDescriptor(n,t))})}return e}var ls,ds=function(e){return function(e){return e&&window.monti.playerConfigs&&window.monti.playerConfigs[e]}(e)?function(e){return 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t=hn.pendingVideoTagStatus(e),n=Dn.sources(e),i=Fi.loadingHLSStatus(e),o="blocked"===Fi.loadingImaStatus(e);r.handlePendingVideoStatus(t,n,i,o)}),f()(this,"onVideoDataChanged",function(){r.newVideoDataLoaded=!0}),f()(this,"sendPrerollPlayRequest",function(){var e=r.store.dispatch;hs("playPreroll")(e)}),f()(this,"handlePlayRequest",function(e,t,n){var i=r.store.dispatch;if(e&&e.length>0){if(r.newVideoDataLoaded&&(r.loadVideoSource(r.videoTag,e,t),r.newVideoDataLoaded=!1,r.prerollEnabled&&!n))return void r.sendPrerollPlayRequest();r.videoTag.play().catch(function(e){return console.error("Error playing the video: ",e)})}else dn(Xn.VIDEO_ERROR)(i)}),f()(this,"handlePendingVideoStatus",function(e,t,n,i){switch(e.type){case"play":r.handlePlayRequest(t,n,i);break;case"resume":r.videoTag.play().catch(function(e){return console.error("Error resuming the video: ",e)});break;case"pause":r.videoTag.pause();break;case"replay":r.videoTag.currentTime=0,r.videoTag.play().catch(function(e){return console.error("Error replaying the video: ",e)});break;case"seekTo":r.videoTag.pause(),r.videoTag.currentTime=e.value}}),f()(this,"loadMp4Source",function(e,t,n){var r=Ra(t,ys);n.setAttribute("src",r),n.load()}),f()(this,"loadVideoSource",function(e,t,n){var i=r.store.dispatch,o=Ra(t,gs);switch(fs.suitableVideoSource(e,o,n)){case"mp4":r.loadMp4Source(n,t,e);break;case"m3u8 with hls":r.videoStreamingManager.hlsLibrarySetup(e,o,function(e){return un(e)(i)},function(e){return dn(e)(i)});break;case"m3u8 directly":fs.loadHlsVideoDirectly(e,o)}}),this.store=t;var i=t.getState;this.videoStreamingManager=new fs,this.videoTag=document.getElementById(En(n)),this.prerollEnabled=bi.prerollEnabled(i()),this.pendingVideoStatusSubscriber=new ji(t,e.getPendingVideoStatusDependencies,this.onPendingVideoStatusChanged.bind(this)),this.videoDataSubscriber=new ji(t,e.getVideoDataDependencies,this.onVideoDataChanged.bind(this)),this.hlsLoadingStatusSubscriber=new ji(t,e.getHLSLoadingStatusDependencies,this.onHlsLoadingStatusChanged.bind(this))}return Vi()(e,null,[{key:"createInstance",value:function(t,n){return new e(t,n)}}]),Vi()(e,null,[{key:"getHLSLoadingStatusDependencies",value:function(e){return[Fi.loadingHLSStatus(e)]}},{key:"getPendingVideoStatusDependencies",value:function(e){return[hn.pendingVideoTagStatus(e)]}},{key:"getVideoDataDependencies",value:function(e){return[Cn.videoData(e)]}}]),e}();function ms(e,t){var n=Object.keys(e);if(Object.getOwnPropertySymbols){var r=Object.getOwnPropertySymbols(e);t&&(r=r.filter(function(t){return Object.getOwnPropertyDescriptor(e,t).enumerable})),n.push.apply(n,r)}return n}function bs(e){for(var t=1;t<arguments.length;t++){var n=null!=arguments[t]?arguments[t]:{};t%2?ms(Object(n),!0).forEach(function(t){f()(e,t,n[t])}):Object.getOwnPropertyDescriptors?Object.defineProperties(e,Object.getOwnPropertyDescriptors(n)):ms(Object(n)).forEach(function(t){Object.defineProperty(e,t,Object.getOwnPropertyDescriptor(n,t))})}return e}var Os={READY_EVENT:"ready",PLAY_EVENT:"play",PAUSE_EVENT:"pause",TIME_EVENT:"time",SEEK_EVENT:"seek",COMPLETE_EVENT:"complete",VOLUME_EVENT:"volume",MUTE_EVENT:"mute"},_s=Object.values(Os),Ss={FULLSCREEN_EVENT:"fullscreen",ANCHOR_STATUS_EVENT:"anchorStatusChanged",ANCHOR_CLOSED_EVENT:"anchorClosed"},Es={AD_PLAY_EVENT:"adPlay",AD_PAUSE_EVENT:"adPause",AD_RESUME_EVENT:"adResume",AD_COMPLETE_EVENT:"adComplete",AD_TIME_EVENT:"adTime",AD_MUTE_EVENT:"adMute",AD_SKIPPED_EVENT:"adSkipped",AD_ERROR_EVENT:"adError",AD_BLOCK_EVENT:"adBlock",AD_REQUEST_EVENT:"adRequest",AD_OPPORTUNITY_EVENT:"adOpportunity",AD_IMPRESSION_EVENT:"adImpression"},ws=Object.values(Es),Ps=Object.values(bs(bs(bs({},Os),Es),Ss)),Ts=function(){function e(t,n){var r=this;Ai()(this,e),f()(this,"eventsCallbacksHandler",void 0),f()(this,"store",void 0),f()(this,"videoStatusSubscriber",void 0),f()(this,"videoMuteSubscriber",void 0),f()(this,"videoVolumeSubscriber",void 0),f()(this,"videoTimeFragmentSubscriber",void 0),f()(this,"videoListStoreSubscriber",void 0),f()(this,"previousVideoTagStatus",void 0),f()(this,"startSeekTime",0),f()(this,"canHandleReady",function(e,t,n){if(t===Os.READY_EVENT){var r=Cn.videoList(e);if(Array.isArray(r)&&r.length>0)return n(),!0}return!1}),f()(this,"canBeHandled",function(e,t){var n=r.store.getState;return r.canHandleReady(n(),e,t)}),f()(this,"reportSeekEnd",function(e){var t={position:hn.currentVideoTimeFragment(e),offset:r.startSeekTime};r.eventsCallbacksHandler.onEvent(Os.SEEK_EVENT,t)}),f()(this,"onMuteStateChanged",function(e){var t=gn.muted(e);r.eventsCallbacksHandler.onEvent(Os.MUTE_EVENT,{state:t})}),f()(this,"onVolumeChanged",function(e){var t=gn.muted(e),n=gn.volume(e);r.eventsCallbacksHandler.onEvent(Os.VOLUME_EVENT,{level:t?0:n})}),f()(this,"onVideoTimeFragmentChanged",function(e){var t=hn.currentVideoTimeFragment(e),n=hn.currentVideoDuration(e);r.eventsCallbacksHandler.onEvent(Os.TIME_EVENT,{duration:n,position:t})}),f()(this,"onVideoListChanged",function(){r.eventsCallbacksHandler.onEvent(Os.READY_EVENT)}),this.store=t,this.eventsCallbacksHandler=n,this.videoStatusSubscriber=new ji(t,e.getVideoStatusDependencies,this.onVideoStatusChanged.bind(this)),this.videoMuteSubscriber=new ji(t,e.getVideoMuteDependencies,this.onMuteStateChanged.bind(this)),this.videoVolumeSubscriber=new ji(t,e.getVolumeDependencies,this.onVolumeChanged.bind(this)),this.videoTimeFragmentSubscriber=new ji(t,e.getVideoTimeDependencies,this.onVideoTimeFragmentChanged.bind(this)),this.videoListStoreSubscriber=new ji(t,e.getVideoListDependencies,this.onVideoListChanged.bind(this)),this.previousVideoTagStatus=hn.videoTagStatus(t.getState())}return Vi()(e,[{key:"onVideoStatusChanged",value:function(e){var t=hn.videoTagStatus(e);switch("seeking"===this.previousVideoTagStatus&&this.reportSeekEnd(e),t){case"paused":this.eventsCallbacksHandler.onEvent(Os.PAUSE_EVENT);break;case"seeking":this.startSeekTime=hn.currentVideoTimeFragment(e);break;case"complete":this.eventsCallbacksHandler.onEvent(Os.COMPLETE_EVENT);break;case"playing":this.eventsCallbacksHandler.onEvent(Os.PLAY_EVENT)}this.previousVideoTagStatus=t}}],[{key:"getVideoStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}}]),e}();f()(Ts,"getVideoMuteDependencies",function(e){return[gn.muted(e)]}),f()(Ts,"getVolumeDependencies",function(e){return[gn.volume(e)]}),f()(Ts,"getVideoTimeDependencies",function(e){return[hn.currentVideoTimeFragment(e)]}),f()(Ts,"getVideoListDependencies",function(e){return[Cn.videoList(e)]}),f()(Ts,"isContentEvent",function(e){return _s.some(function(t){return t===e})});var As=function e(t,n){var r=this;Ai()(this,e),f()(this,"eventsCallbacksHandler",void 0),f()(this,"store",void 0),f()(this,"fullscreenSubscriber",void 0),f()(this,"anchorStatusSubscriber",void 0),f()(this,"anchorDisabledByUserSubscriber",void 0),f()(this,"onFullscreenChanged",function(e){var t=gn.isFullscreenOn(e);r.eventsCallbacksHandler.onEvent(Ss.FULLSCREEN_EVENT,{state:t})}),f()(this,"onAnchorStatusChanged",function(e){var t="active"===Pr(e)?"activated":"deactivated";r.eventsCallbacksHandler.onEvent(Ss.ANCHOR_STATUS_EVENT,{state:t})}),f()(this,"onAnchorDisabledByUser",function(e){if(wr(e)){var t=hn.currentVideoTimeFragment(e);r.eventsCallbacksHandler.onEvent(Ss.ANCHOR_CLOSED_EVENT,{position:t})}}),this.store=t,this.eventsCallbacksHandler=n,this.fullscreenSubscriber=new ji(t,e.getFullscreenDependencies,this.onFullscreenChanged.bind(this)),this.anchorStatusSubscriber=new ji(t,e.getAnchorStatusDependencies,this.onAnchorStatusChanged.bind(this)),this.anchorDisabledByUserSubscriber=new 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t=_i.adStatus(e),n=_i.currentAdTag(e);switch(t){case"requested":r.eventsCallbacksHandler.onEvent(Es.AD_REQUEST_EVENT,{tag:n});break;case"paused":r.eventsCallbacksHandler.onEvent(Es.AD_PAUSE_EVENT,{tag:n});break;case"completed":r.eventsCallbacksHandler.onEvent(Es.AD_COMPLETE_EVENT,{tag:n});break;case"skipped":r.eventsCallbacksHandler.onEvent(Es.AD_SKIPPED_EVENT,{tag:n});break;case"playing":"paused"===r.previousAdStatus?r.eventsCallbacksHandler.onEvent(Es.AD_RESUME_EVENT,{tag:n}):r.eventsCallbacksHandler.onEvent(Es.AD_PLAY_EVENT,{tag:n});break;case"error":var i=_i.adErrorMessage(e);r.eventsCallbacksHandler.onEvent(Es.AD_ERROR_EVENT,{tag:n,message:i})}r.previousAdStatus=t}),f()(this,"onAtTimeChanged",function(e){var t=_i.adCurrentTime(e),n=_i.currentAdTag(e),i=_i.adDuration(e);r.eventsCallbacksHandler.onEvent(Es.AD_TIME_EVENT,{position:t,tag:n,duration:i})}),f()(this,"onAdMuteChanged",function(e){var t=_i.adMuted(e);r.eventsCallbacksHandler.onEvent(Es.AD_MUTE_EVENT,{state:t})}),f()(this,"onAdProviderLoadingChanged",function(e){"blocked"===Fi.loadingImaStatus(e)&&r.eventsCallbacksHandler.onEvent(Es.AD_BLOCK_EVENT)}),f()(this,"onAdImpressionChanged",function(e){var t=_i.currentAdTag(e);r.eventsCallbacksHandler.onEvent(Es.AD_IMPRESSION_EVENT,{tag:t})}),f()(this,"onAdOpportunityChanged",function(e){var t=_i.currentAdTag(e);r.eventsCallbacksHandler.onEvent(Es.AD_OPPORTUNITY_EVENT,{tag:t})}),this.store=t,this.eventsCallbacksHandler=n,this.previousAdStatus=_i.adStatus(t.getState()),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this)),this.adTimeSubscriber=new ji(t,e.getAdTimeDependencies,this.onAtTimeChanged.bind(this)),this.adMuteSubscriber=new ji(t,e.getAdMuteDependencies,this.onAdMuteChanged.bind(this)),this.adImpressionSubscriber=new ji(t,e.getAdImpressionDependencies,this.onAdImpressionChanged.bind(this)),this.adOpportunitySubscriber=new 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{"is_conflicting_with_other_jw_players":false,"programmatic_play_with_sound_on_desktop":false,"referrer_id":"af93e181-b289-0560-a2bf-808e93bb05bc","width":"100","comscore_publisher_id":"18120612","monetization":{"ad_type":"static_tag","continue_content_play_while_waiting_for_ad":false,"strategy":"on_player_load","ad_request_timeout":"10000","midrolls":{"on":[0]},"vpaid_mode":"ENABLED","ad_tag":"https://pubads.g.doubleclick.net/gampad/ads?sz=400x300|640x480|480x270|640x360&iu=/175840252/MMPlus/smithsonianmag/Video&impl=s&gdfp_req=1&env=vp&output=vast&unviewed_position_start=1&url=##REFERRER_URL_UNESC##&description_url=##DESCRIPTION_URL_UNESC##&correlator=##CACHEBUSTER##&cust_params=mm_midroll%3D##MIDROLL_ORDER##%26video_ID%3D##VIDEO_ID##"},"sponsorship":false,"player_identifier":"mplayer","recommendation_id":null,"brand_color":"#FF9900","powered_by_strip":true,"platform":"buffy","type":"video","config_name":"MM+ | Smithsonianmag | Podding","player_id":"3v9g2u2f","playlist_id":"fSkmeWKF","playback_method":"autoplay","anchor_viewability_method":"none","player_version":"v4","playlist_type":"semantic","semantic_options":{"scan_images_on_page":true,"scanned_element":"","tags":"geogrophy,nature,animals,habitat,outdoors,science,history","minimum_date_factor":30,"scanned_element_type":"tag","scoped_keywords":"mentalfloss","promoted_videos":[]},"script_destination":"mm","publisher_contribution":"floor8","general_script_description":"","brand_logo":"","brand_logo_click_url":"","next_video":"none","uniq_key":"af93e181-b289-0560-a2bf-808e93bb05bc","content_id":"fSkmeWKF","content_type":"semantic"})); Finland has vastly improved in reading, math and science literacy over the past decade in large part because its teachers are trusted to do whatever it takes to turn young lives around. This 13-year-old, Besart Kabashi, received something akin to royal tutoring. “I took Besart on that year as my private student,” Louhivuori told me in his office, which boasted a Beatles “Yellow Submarine” poster on the wall and an electric guitar in the closet. When Besart was not studying science, geography and math, he was parked next to Louhivuori’s desk at the front of his class of 9- and 10-year- olds, cracking open books from a tall stack, slowly reading one, then another, then devouring them by the dozens. By the end of the year, the son of Kosovo war refugees had conquered his adopted country’s vowel-rich language and arrived at the realization that he could, in fact, learn. Years later, a 20-year-old Besart showed up at Kirkkojarvi’s Christmas party with a bottle of Cognac and a big grin. “You helped me,” he told his former teacher. Besart had opened his own car repair firm and a cleaning company. “No big fuss,” Louhivuori told me. “This is what we do every day, prepare kids for life.” This tale of a single rescued child hints at some of the reasons for the tiny Nordic nation’s staggering record of education success, a phenomenon that has inspired, baffled and even irked many of America’s parents and educators. Finnish schooling became an unlikely hot topic after the 2010 documentary film Waiting for “Superman” contrasted it with America’s troubled public schools. “Whatever it takes” is an attitude that drives not just Kirkkojarvi’s 30 teachers, but most of Finland’s 62,000 educators in 3,500 schools from Lapland to Turku—professionals selected from the top 10 percent of the nation’s graduates to earn a required master’s degree in education. Many schools are small enough so that teachers know every student. If one method fails, teachers consult with colleagues to try something else. They seem to relish the challenges. Nearly 30 percent of Finland’s children receive some kind of special help during their first nine years of school. The school where Louhivuori teaches served 240 first through ninth graders last year; and in contrast with Finland’s reputation for ethnic homogeneity, more than half of its 150 elementary-level students are immigrants—from Somalia, Iraq, Russia, Bangladesh, Estonia and Ethiopia, among other nations. “Children from wealthy families with lots of education can be taught by stupid teachers,” Louhivuori said, smiling. “We try to catch the weak students. It’s deep in our thinking.” Advertisement scroll for more The transformation of the Finns’ education system began some 40 years ago as the key propellent of the country’s economic recovery plan. Educators had little idea it was so successful until 2000, when the first results from the Programme for International Student Assessment (PISA), a standardized test given to 15-year-olds in more than 40 global venues, revealed Finnish youth to be the best young readers in the world. Three years later, they led in math. By 2006, Finland was first out of 57 countries (and a few cities) in science. In the 2009 PISA scores released last year, the nation came in second in science, third in reading and sixth in math among nearly half a million students worldwide. “I’m still surprised,” said Arjariita Heikkinen, principal of a Helsinki comprehensive school. “I didn’t realize we were that good.” In the United States, which has muddled along in the middle for the past decade, government officials have attempted to introduce marketplace competition into public schools. In recent years, a group of Wall Street financiers and philanthropists such as Bill Gates have put money behind private-sector ideas, such as vouchers, data-driven curriculum and charter schools, which have doubled in number in the past decade. President Obama, too, has apparently bet on competition. His Race to the Top initiative invites states to compete for federal dollars using tests and other methods to measure teachers, a philosophy that would not fly in Finland. “I think, in fact, teachers would tear off their shirts,” said Timo Heikkinen, a Helsinki principal with 24 years of teaching experience. “If you only measure the statistics, you miss the human aspect.”
The facts show that America has it all wrong in putting to much emphasis on national "data-driven" competition. These approaches take away from the unique aspects of each child.
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t was the end of term at Kirkkojarvi Comprehensive School in Espoo, a sprawling suburb west of Helsinki, when Kari Louhivuori, a veteran teacher and the school’s principal, decided to try something extreme—by Finnish standards. One of his sixth-grade students, a Kosovo-Albanian boy, had drifted far off the learning grid, resisting his teacher’s best efforts. The school’s team of special educators—including a social worker, a nurse and a psychologist—convinced Louhivuori that laziness was not to blame. 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n=r.generatePrerollTag(e,t);r.monetization.onPrerollAdOpportunity(n)}),f()(this,"onSeekedWhileAdInProgress",function(){r.monetization.onMidrollAdOpportunity()});var i=t.getState;this.monetization=n,this.videoTimeSubscriber=new qi(t,this),this.videoSeekSubscriber=new zi(t,this),this.prerollScheduler=new Gi(t,this);var o=_i.adTagUrlTemplate(i());this.adTagGenerator=new Wi(o)},Yi=function(){function e(){Ai()(this,e)}return Vi()(e,null,[{key:"generateAdRequest",value:function(e,t,n){var r=new google.ima.AdsRequest;return r.adTagUrl=e,Fn()||r.setAdWillPlayMuted(t),r.vastLoadTimeout=n,r}}]),e}(),Zi=function(e){return function(t){t({type:"[MONETIZATION] change ad status",payload:e})}},Xi=function(e){return function(t){t({type:"[COMMON] set pending video status",payload:{pendingStatusObject:{type:e,value:""}}})}},Ji=function(e){return function(t){t({type:"[MONETIZATION] change loading ad status",payload:e})}},Qi=function(e){return function(t){t({type:"[MONETIZATION] update ad 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t=a.store,n=t.getState,r=t.dispatch,i=gn.volume(n());Bn()||gn.muted(n())?(e.setVolume(0),Qi(!0)(r)):(e.setVolume(gn.volume(n())),eo(i)(r),Qi(!1)(r))}),f()(this,"createIMAAdManager",function(t){a.IMAAdManager=t.getAdsManager(a.adVideoElement,e.getAdsRenderingSettings()),a.setAdVolume(a.IMAAdManager)}),f()(this,"registerToAdManagerEvents",function(){a.IMAAdManager.addEventListener(google.ima.AdErrorEvent.Type.AD_ERROR,a.onAdError),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.CONTENT_PAUSE_REQUESTED,a.onContentPauseRequested),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.CONTENT_RESUME_REQUESTED,a.onContentResumeRequested),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.STARTED,a.onAdStarted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.IMPRESSION,a.onAdImpression),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.SKIPPED,a.onAdSkipped),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.COMPLETE,a.onAdCompleted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.PAUSED,a.onAdPaused),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.RESUMED,a.onAdStarted),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.AD_PROGRESS,a.onAdProgressChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.VOLUME_CHANGED,a.onVolumeChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.VOLUME_MUTED,a.onAdVolumeMutedChanged),a.IMAAdManager.addEventListener(google.ima.AdEvent.Type.ALL_ADS_COMPLETED,a.onAdCompleted)}),f()(this,"onIMAAdsManagerLoaded",function(e){var t=a.store.dispatch;a.createIMAAdManager(e),a.registerToAdManagerEvents(),Zi("loaded")(t)}),f()(this,"onAdError",function(e){var t=a.store.dispatch;!function(e){return function(t){t({type:"[MONETIZATION] change ad error",payload:e})}}(e.getError().getMessage())(t),Ji(!1),a.continuePlayingContent()}),f()(this,"onAdImpression",function(e){var t=a.store.dispatch,n=!e.getAd().g.vpaid;a.setPodInfo(e),function(e){e({type:"[MONETIZATION] increase ad impression counter"})}(t),function(e){return function(t){t({type:"[MONETIZATION] update is vast ad",payload:e})}}(n)(t)}),f()(this,"onVolumeChanged",function(e){var t=a.store.dispatch;eo(e.target.getVolume())(t)}),f()(this,"onAdVolumeMutedChanged",function(e){var t=a.store.dispatch;0===e.target.getVolume()?Qi(!0)(t):Qi(!1)(t)}),f()(this,"continuePlayingContent",function(){var e=a.store,t=e.getState,n=e.dispatch,r=hn.videoTagStatus(t());Xi("idle"===r?"play":"resume")(n)}),f()(this,"stopPlayingContent",function(){var 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e=a.store.dispatch;Zi("skipped")(e)}),f()(this,"onResize",function(){Un(a.IMAAdManager)||(a.IMAAdManager.resize(a.videoPlayerElement.clientWidth,a.videoPlayerElement.clientHeight,google.ima.ViewMode.NORMAL),a.adContainerElement.style.height="".concat(a.videoPlayerElement.clientHeight,"px"))}),f()(this,"onAdProgressChanged",function(e){var t,n,r=a.store,i=r.dispatch,o=r.getState,s=e.getAdData().currentTime,u=e.getAdData().duration,c=_i.adDuration(o());(t=s,function(e){e({type:"[MONETIZATION] change ad current time",payload:t})})(i),c!==u&&(n=u,function(e){e({type:"[MONETIZATION] change ad duration",payload:n})})(i)}),f()(this,"onAnchorStatusChanged",function(){var e=a.store.getState;"processing"!==Pr(e())&&a.onResize()}),f()(this,"changeAdVolume",function(e){Un(a.IMAAdManager)||a.IMAAdManager.setVolume(e)}),f()(this,"changeAdMuted",function(e,t){Un(a.IMAAdManager)||(t?a.IMAAdManager.setVolume(0):a.IMAAdManager.setVolume(e))}),f()(this,"changeAdStatus",function(e){Un(a.IMAAdManager)||("playing"===e&&a.IMAAdManager.resume(),"paused"===e&&a.IMAAdManager.pause())});var s=t.getState;this.store=t,this.adVideoElement=r,this.videoPlayerElement=i,this.adContainerElement=n,this.adDisplayContainer=new google.ima.AdDisplayContainer(n,r),this.createAdLoader(s(),this.adDisplayContainer),this.adDisplayContainer.initialize(),this.anchorStatusStoreSubscriber=new ji(t,e.getAnchorDependencies,this.onAnchorStatusChanged.bind(this)),this.registerForWindowResize(),this.initMutationObserver(o)};f()(to,"getAdsRenderingSettings",function(){var e=new google.ima.AdsRenderingSettings;return 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e=s.store,t=e.dispatch,n=e.getState,r=_i.adStatus(n()),i=bi.continuePlayingWhileWaitingForAd(n());"loaded"===r?s.playAd(!0):"requested"===r&&(s.pendingMidrollAdPlay=!0,i||(Xi("pause")(t),Ji(!0)(t))),function(e){e({type:"[MONETIZATION] increase ad Opportunity counter"})}(t)}),f()(this,"onPrerollAdOpportunity",function(e){var t=s.store,n=t.getState,r=t.dispatch,i=Fi.loadingImaStatus(n());Un(s.adHandler)?"loading"!==i&&""!==i||(Ji(!0)(r),s.pendingPrerollAdPlay=!0,s.pendingPrerollAdTag=e):(s.pendingPrerollAdPlay=!0,Ji(!0)(r),s.adHandler.loadNewAd(e,"preroll"))}),f()(this,"onPreMidrollAdOpportunity",function(e,t){Un(s.adHandler)||(e.currentTime>=e.midrollTime&&(s.pendingMidrollAdPlay=!0),s.pendingMidrollNumber=e.midrollNumber,s.adHandler.loadNewAd(t,"midroll"))}),f()(this,"hasPendingAd",function(){return s.hasPendingMidrollAdPlay()||s.hasPendingPrerollAdPlay()}),f()(this,"onAdStatusChanged",function(e){var t=s.store.dispatch,n=_i.adStatus(e);"completed"===n&&Ji(!1)(t);var r=bi.continuePlayingWhileWaitingForAd(e),i=_i.loadingAd(e);"playing"!==n&&"error"!==n||r||!i||Ji(!1)(t),s.hasPendingAd()&&"loaded"===n?s.playAd(s.hasPendingMidrollAdPlay()):s.hasPendingAd()&&"error"===n?(Ji(!1),s.clearPendingMidroll(),s.clearPendingPreroll()):Hi(n)||(Ji(!1),function(e){e({type:"[MONETIZATION] clear ad data"})}(t))}),f()(this,"clearPendingMidroll",function(){s.pendingMidrollNumber=null,s.pendingMidrollAdPlay=!1}),f()(this,"clearPendingPreroll",function(){s.pendingPrerollAdPlay=!1,s.pendingPrerollAdTag=null}),f()(this,"onVideoTagStatusChanged",function(e){"complete"===hn.videoTagStatus(e)&&function(e){e({type:"[MONETIZATION] clear played midrolls"})}(s.store.dispatch)}),f()(this,"hasPendingMidrollAdPlay",function(){return s.pendingMidrollAdPlay}),f()(this,"hasPendingPrerollAdPlay",function(){return s.pendingPrerollAdPlay}),f()(this,"playAd",function(e){var t,n=s.store.dispatch,r=s.adHandler.playAd();e?((t=s.pendingMidrollNumber,function(e){e({type:"[MONETIZATION] add 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Ki(t,this),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this)),this.videoTagStatusSubscriber=new ji(t,e.getVideoTagStatusDependencies,this.onVideoTagStatusChanged.bind(this)),e.canUseIMA(u())?this.adHandler=new to(t,r,i,o,a):this.imaLoadingStatusSubscriber=new ji(t,e.getIMALoadingStatusDependencies,this.onIMALoadingStatusChanged.bind(this)),this.pendingAdStatusStoreSubscriber=new ji(t,e.getPendingAdStatusDependencies,this.onPendingAdStatusChanged.bind(this)),this.adMutedStoreSubscriber=new ji(t,e.getAdMutedDependencies,this.onAdMutedChanged.bind(this)),this.adVolumeStoreSubscriber=new ji(t,e.getAdVolumeDependencies,this.onAdVolumeChanged.bind(this))};f()(no,"getAdStatusDependencies",function(e){return[_i.adStatus(e)]}),f()(no,"getVideoTagStatusDependencies",function(e){return[hn.videoTagStatus(e)]}),f()(no,"getIMALoadingStatusDependencies",function(e){return[Fi.loadingImaStatus(e)]}),f()(no,"canUseIMA",function(e){return"success"===Fi.loadingImaStatus(e)}),f()(no,"getPendingAdStatusDependencies",function(e){return[_i.pendingAdStatus(e)]}),f()(no,"getAdMutedDependencies",function(e){return[_i.adMuted(e)]}),f()(no,"getAdVolumeDependencies",function(e){return[_i.adVolume(e)]});var ro=function(e,t){!function(e,t){var n=document.getElementById(vn(t));B(b(Li,{store:e,playerId:t}),n)}(e,t);var n=function(e){var t=Ri(e);return document.getElementById(t)}(t),r=function(e){var t=Bn()?Di(e):En(e);return document.getElementById(t)}(t),i=function(e){var t=En(e);return document.getElementById(t)}(t),o=function(e){var t=bn(e);return document.getElementById(t)}(t);return new 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this.errorMessage=e,this}},{key:"setAdPodNumber",value:function(e){return this.adPodNumber=e,this}},{key:"setAdSlotNumber",value:function(e){return this.adSlotNumber=e,this}},{key:"build",value:function(){var e=[];return jn(this.position)||e.push("video current position=".concat(Hn(this.position),"sec")),jn(this.duration)||e.push("video duration time=".concat(Hn(this.duration),"sec")),jn(this.loadTime)||e.push("video load time=".concat(this.loadTime,"milliseconds")),jn(this.previousPosition)||e.push("previous position=".concat(Hn(this.previousPosition),"sec")),jn(this.adOrder)||e.push("ad order=".concat(this.adOrder)),jn(this.adType)||e.push("ad type=".concat(this.adType)),jn(this.adDuration)||e.push("ad duration=".concat(Hn(Number(this.adDuration)),"sec")),jn(this.adPodNumber)||e.push("pod number=".concat(this.adPodNumber)),jn(this.adSlotNumber)||e.push("slot number=".concat(this.adSlotNumber)),jn(this.errorMessage)||e.push("error 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The initial state may not be undefined, but can be null.')})}(n)}catch(s){o=s}return function(e,t){if(void 0===e&&(e={}),o)throw o;for(var r=!1,i={},s=0;s<a.length;s++){var u=a[s],c=n[u],l=e[u],d=c(l,t);if("undefined"===typeof d){var p=mt(u,t);throw new Error(p)}i[u]=d,r=r||d!==l}return(r=r||a.length!==Object.keys(e).length)?i:e}}({dependenciesLoadingStatus:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:da,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] update hls status":return la(la({},e),{},{loadingHLSStatus:t.payload});case"[CORE] update ima status":return la(la({},e),{},{loadingImaStatus:t.payload});default:return e}},playerData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:ha,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":var n=t.payload;return fa({},function(e,t,n){var r=t.playback_method,i=t.player_id;return fa(fa({},e),{},{playbackMethod:Un(r)?e.playbackMethod:r,playerId:Un(i)?e.playerId:i,playerInstanceUniqId:n,playerMode:Fn()?"mobile":"desktop"})}(e,n.initiateParams,n.playerInstanceUniqId));case"[CORE] reset player data time params":return fa(fa({},e),{},{currentVideoTimeFragment:0,currentVideoBufferedTime:0,currentVideoDuration:0,currentVideoTime:0});case"[COMMON] set mute video":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{muted:t.payload})});case"[COMMON] set volume":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{volume:t.payload})});case"[COMMON] change selected settings category":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{selectedSettingsCategory:t.payload})});case"[COMMON] change settings speed":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{speed:t.payload})});case"[COMMON] change settings quality":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{quality:t.payload})});case"[COMMON] set fullscreen":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{fullscreen:fa(fa({},e.playerSettings.fullscreen),{},{isFullscreenOn:t.payload,pendingFullscreenRequest:""})})});case"[COMMON] set fullscreen request":return fa(fa({},e),{},{playerSettings:fa(fa({},e.playerSettings),{},{fullscreen:fa(fa({},e.playerSettings.fullscreen),{},{pendingFullscreenRequest:t.payload})})});case"[COMMON] set pending video status":var r=t.payload.pendingStatusObject;return fa(fa({},e),{},{pendingVideoTagStatus:fa({},r)});case"[COMMON] set player mode":return fa(fa({},e),{},{playerMode:t.payload});case"[CORE] update video current fragment position":return fa(fa({},e),{},{currentVideoTimeFragment:t.payload});case"[CORE] update video current position":return fa(fa({},e),{},{currentVideoTime:t.payload});case"[CORE] update video current buffered time":return fa(fa({},e),{},{currentVideoBufferedTime:t.payload});case"[CORE] update video current duration":return fa(fa({},e),{},{currentVideoDuration:t.payload});case"[CORE] change video tag status":return fa(fa({},e),{},{videoTagStatus:t.payload});case"[CORE] update player visibility":return fa(fa({},e),{},{playerVisibility:t.payload});case"[CORE] update placeholder visibility":return fa(fa({},e),{},{playerPlaceholderVisibility:t.payload});case"[CORE] change loading player status":return fa(fa({},e),{},{loadingPlayer:t.payload});case"[COMMON] show black screen with loader":return fa(fa({},e),{},{loader:fa(fa({},e.loader),{},{showBlackScreen:t.payload})});case"[CORE] set player size":return fa(fa({},e),{},{playerSize:t.payload});case"[COMMON] set error message":return fa(fa({},e),{},{errorMessage:t.payload});default:return e}},brandingData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:va,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return ga({},function(e,t){var n=t.powered_by_strip,r=t.brand_logo,i=t.brand_logo_click_url,o=t.brand_color;return ga(ga({},e),{},{showVoltaxLogo:Un(n)?e.showVoltaxLogo:n,brandingLogoSrc:Un(r)?e.brandingLogoSrc:r,brandingLogoUrl:Un(i)?e.brandingLogoUrl:i,brandingColor:Un(o)?e.brandingColor:o})}(e,t.payload.initiateParams));default:return e}},anchorOptions:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Oa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return ba({},function(e,t){var n=t.anchor_options;if(!Un(n)){var r=n.anchoring_appearance,i=n.can_close,o=n.closable_ad,a=n.close_after,s=n.continue_streaming,u=n.orientation,c=n.margins,l=n.sticky_below_class_name,d=n.width,p=Un(c)?e.margins:{top:Number.isInteger(c.top)?c.top:e.margins.top,bottom:Number.isInteger(c.bottom)?c.bottom:e.margins.bottom,left:Number.isInteger(c.left)?c.left:e.margins.left,right:Number.isInteger(c.right)?c.right:e.margins.right};return ba(ba({},e),{},{anchoringAppearance:r||e.anchoringAppearance,canClose:Un(i)?e.canClose:i,orientation:Un(u)?e.orientation:u,closableAd:Un(o)?e.closableAd:o,closeAfter:Un(a)?e.closeAfter:a,continueStreaming:Un(s)?e.continueStreaming:s,stickyBelowClassName:Un(l)?e.stickyBelowClassName:l,width:Un(d)?e.width:d,margins:p,anchorData:ba(ba({},e.anchorData),{},{anchorEnabled:!0})})}return e}(e,t.payload.initiateParams));case"[COMMON] set anchor enable":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorEnabled:t.payload})});case"[ANCHOR] update is anchor status":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorStatus:t.payload})});case"[COMMON] set anchor disabled by user":return ba(ba({},e),{},{anchorData:ba(ba({},e.anchorData),{},{anchorDisabledByUser:t.payload})});default:return e}},monetization:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:wa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Sa({},function(e,t){var n=t.monetization;if(Un(n))return e;var r=n.ad_tag,i=n.ad_type,o=n.vpaid_mode,a=n.ad_request_timeout,s=n.continue_content_play_while_waiting_for_ad,u=n.midrolls,c=u&&u.on&&u.on.sort(Wn),l=Un(s)?e.continuePlayingWhileWaitingForAd:s,d=c?c.indexOf(0):-1,p=-1!==d&&!l;return p&&(c=c.splice(d,1)),Sa(Sa({},e),{},{midrolls:Sa(Sa({},e.midrolls),{},{every:u&&u.every,on:c}),prerollEnabled:p,adRequestTimeout:Un(a)?e.adRequestTimeout:parseInt(a,10),vpaidMode:Un(o)?e.vpaidMode:o,continuePlayingWhileWaitingForAd:l,adsData:Sa(Sa({},e.adsData),{},{adType:Un(i)?e.adsData.adType:i,adTagUrlTemplate:Un(r)?e.adsData.adTagUrlTemplate:r})})}(e,t.payload.initiateParams));case"[COMMON] set new ad tag url template":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adTagUrlTemplate:t.payload})});case"[MONETIZATION] change ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adStatus:t.payload,adErrorMessage:null})});case"[MONETIZATION] change ad tag":var n=t.payload,r=n.adUnit,i=n.adTag;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{currentAdTag:i,adUnit:r})});case"[MONETIZATION] change pending ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{pendingAdStatus:t.payload})});case"[MONETIZATION] change ad error":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adStatus:"error",adErrorMessage:t.payload})});case"[MONETIZATION] increase ad impression counter":var o=e.adsData.adImpression;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adImpression:o+1})});case"[MONETIZATION] increase ad Opportunity counter":var a=e.adsData.adOpportunity;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOpportunity:a+1})});case"[MONETIZATION] add played midroll number":var s=e.adsData.playedMidrolls,u=In()(s);return u.push(t.payload),Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOrder:t.payload,playedMidrolls:u})});case"[MONETIZATION] clear played midrolls":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{playedMidrolls:[]})});case"[MONETIZATION] clear ad data":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adOrder:0,currentAdTag:null,adDuration:0,adUnit:""})});case"[MONETIZATION] change ad duration":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adDuration:t.payload})});case"[MONETIZATION] update is vast ad":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{isVastAd:t.payload})});case"[MONETIZATION] change ad current time":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adCurrentTime:t.payload})});case"[MONETIZATION] update ad muted":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adMuted:t.payload})});case"[MONETIZATION] change ad volume":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{adVolume:t.payload})});case"[MONETIZATION] change pod info":var c=t.payload,l=c.podNumber,d=c.slotNumber;return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{podNumber:l,slotNumber:d})});case"[MONETIZATION] change loading ad status":return Sa(Sa({},e),{},{adsData:Sa(Sa({},e.adsData),{},{loadingAd:t.payload})});default:return e}},mediaData:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:ja,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Va({},function(e,t){var n=t.content_type,r=t.media_id,i=t.display_title;return Va(Va({},e),{},{mediaType:Un(n)?e.mediaType:n,mediaId:Un(r)?e.mediaId:r,videoData:Va(Va({},e.videoData),{},{showTitle:!!Un(i)||i})})}(e,t.payload.initiateParams));case"[CORE] load video request":return Va(Va({},e),{},{loadingMedia:!0});case"[CORE] load video request success":return Va(Va({},e),{},{loadingMedia:!1,videoList:t.payload});case"[CORE] set current video":var n=t.payload,r=n.index,i=n.videoData;return Va(Va({},e),{},{activeVideoIndex:r,videoData:i});case"[CORE] load video request error":return Va(Va({},e),{},{loadingMedia:!1,mediaLoadingError:t.payload});case"[COMMON] media request":var o=t.payload.mediaRequestObject;return Va(Va({},e),{},{mediaRequest:Va({},o)});default:return e}},semanticOptions:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Ba,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Fa({},function(e,t){var n=t.semantic_options;if(Un(n))return e;var r=n.minimum_date_factor,i=n.promoted_videos,o=n.scan_images_on_page,a=n.scanned_element,s=n.scanned_element_type,u=n.scoped_keywords,c=n.tags;return Fa(Fa({},e),{},{minimumDateFactor:Un(r)?e.minimumDateFactor:r,promotedVideos:Un(i)?e.promotedVideos:i,scanImagesOnPage:Un(o)?e.scanImagesOnPage:o,scannedElement:Un(a)?e.scannedElement:a,scannedElementType:Un(s)?e.scannedElementType:s,scopedKeywords:Un(u)?e.scopedKeywords:u,tags:Un(c)?e.tags:c})}(e,t.payload.initiateParams));default:return e}},userInteraction:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Wa,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[USER INTERACTION] change user interaction":return qa(qa({},e),{},{userInteractionType:t.payload});default:return e}},splitView:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:$a,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Ga({},function(e,t){var n=t.anchor_options;if(!Un(n)){var r=n.split_view,i=n.split_view_ratio;return Ga(Ga({},e),{},{splitViewRatio:Un(r)||!r||Un(i)?e.splitViewRatio:i})}return e}(e,t.payload.initiateParams));default:return e}},discovery:function(){var e=arguments.length>0&&void 0!==arguments[0]?arguments[0]:Za,t=arguments.length>1?arguments[1]:void 0;switch(t.type){case"[CORE] initiate store":return Ya({},function(e,t){var n=t.next_video;return Un(n)?e:Ya(Ya({},e),{},{nextVideo:Xa(n)})}(e,t.payload.initiateParams));case"[DISCOVERY] show up next":return Ya(Ya({},e),{},{showUpNext:t.payload});case"[DISCOVERY] show skippable content":return Ya(Ya({},e),{},{showSkippableContent:t.payload});default:return e}}}),Qa=[],es=!1,ts=function e(){return function(t){return function(n){if(es)return Qa.push(n),null;es=!0;var r=t(n);return es=!1,Qa.length>0&&e()(t)(Qa.shift()),r}}},ns=function(e){var t=[];if(function(e){return!Un(e)&&!Un(e.enable_redux_debugging)&&e.enable_redux_debugging}(e)){var n=window&&window.__REDUX_DEVTOOLS_EXTENSION__&&window.__REDUX_DEVTOOLS_EXTENSION__();"function"===typeof n&&t.push(n)}var r=Et.apply(void 0,[wt(ua,ts)].concat(t));return vt(Ja,r)},rs=function(){function e(t){Ai()(this,e),f()(this,"playerVisibilitySubscriber",void 0),f()(this,"videoTagStatusSubscriber",void 0),f()(this,"shouldPlayIfLazyplay",!0),f()(this,"shouldPlayIfAutoplayWhenViewable",!0),f()(this,"videoPausedByObserver",!1),this.store=t,this.playerVisibilitySubscriber=null,this.videoTagStatusSubscriber=null,this.playAccordingToPlaybackMethod()}return Vi()(e,[{key:"lazyplayHandler",value:function(e){hn.playerVisibility(e)>=.5&&(this.playVideo(),this.shouldPlayIfLazyplay=!1)}},{key:"autoplayWhenViewableHandler",value:function(e){hn.playerVisibility(e)>=.5?this.playVideo():this.pauseVideo()}},{key:"onPlayerVisibilityChanged",value:function(e){var t=hn.playbackMethod(e);"lazyplay"===t&&this.shouldPlayIfLazyplay&&this.lazyplayHandler(e),"autoplay_when_viewable"===t&&this.shouldPlayIfAutoplayWhenViewable&&this.autoplayWhenViewableHandler(e)}},{key:"onVideoTagStatusChanged",value:function(e){var t=hn.videoTagStatus(e);"paused"!==t||this.videoPausedByObserver||(this.shouldPlayIfAutoplayWhenViewable=!1),"playing"===t&&(this.shouldPlayIfAutoplayWhenViewable=!0,this.videoPausedByObserver=!1)}},{key:"initiatePlayerVisibilitySubscriber",value:function(){this.playerVisibilitySubscriber=new ji(this.store,e.getPlayerVisibilityDependencies,this.onPlayerVisibilityChanged.bind(this))}},{key:"initiateVideoTagStatusSubscriber",value:function(){this.videoTagStatusSubscriber=new ji(this.store,e.getVideoTagStatusDependencies,this.onVideoTagStatusChanged.bind(this))}},{key:"playVideo",value:function(){var e=this.store,t=e.dispatch,n=e.getState;"idle"===hn.videoTagStatus(n())?on("play")(t):on("resume")(t)}},{key:"pauseVideo",value:function(){var e=this.store,t=e.dispatch,n=e.getState;"paused"!==hn.videoTagStatus(n())&&(this.videoPausedByObserver=!0,on("pause")(t))}},{key:"playAccordingToPlaybackMethod",value:function(){var e=this.store,t=e.dispatch,n=(0,e.getState)();switch(hn.playbackMethod(n)){case"autoplay":this.playVideo();break;case"lazyplay":this.initiatePlayerVisibilitySubscriber();break;case"autoplay_when_viewable":this.initiatePlayerVisibilitySubscriber(),this.initiateVideoTagStatusSubscriber();break;case"none":an(!1)(t)}}}],[{key:"getPlayerVisibilityDependencies",value:function(e){return[hn.playerVisibility(e)]}},{key:"getVideoTagStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}}]),e}(),is=function(){function e(t,n,r,i){var o=this;Ai()(this,e),f()(this,"videoStatusSubscriber",void 0),f()(this,"videoListSubscriber",void 0),f()(this,"mediaRequestSubscriber",void 0),f()(this,"playerVisibilitySubscriber",void 0),f()(this,"playbackMethodManager",void 0),f()(this,"store",void 0),f()(this,"loadContent",function(e,t,n,r){o.loadMedia(t,n,r).then(function(){o.playbackMethodManager=new rs(e)})}),f()(this,"loadMedia",function(e,t,n){var r=o.store,i=r.dispatch,a=r.getState,s=Dn.showTitle(a());if("semantic"===e){var u=pn.semanticOptions(a());return Na(u,s,n)(i)}return ka(t,s,n)(i)}),this.store=t,this.videoStatusSubscriber=new ji(t,e.getVideoStatusDependencies,this.onVideoStatusChanged.bind(this)),this.videoListSubscriber=new ji(t,e.getVideoListDependencies,this.onVideoListChanged.bind(this)),this.mediaRequestSubscriber=new ji(t,e.getMediaRequestDependencies,this.onMediaRequestChanged.bind(this)),this.playerVisibilitySubscriber=null,this.loadContent(t,r,n,i)}return Vi()(e,null,[{key:"createInstance",value:function(t,n,r,i){return new e(t,n,r,i)}}]),Vi()(e,[{key:"playNextVideo",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e),r=Cn.activeVideoIndex(e)+1;n.length>1&&r>=n.length&&(r=0),r<n.length&&(!function(e){e({type:"[CORE] reset player data time params"})}(t),La(r,n[r])(t),on("play")(t))}},{key:"playPreviousVideo",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e),r=Cn.activeVideoIndex(e);if(r>0){var i=r-1;La(i,n[i])(t),on("play")(t)}}},{key:"onVideoStatusChanged",value:function(e){"complete"===hn.videoTagStatus(e)&&this.playNextVideo(e)}},{key:"onVideoListChanged",value:function(e){var t=this.store.dispatch,n=Cn.videoList(e);!jn(n)&&n.length>0&&La(0,n[0])(t)}},{key:"onMediaRequestChanged",value:function(e){var t=Cn.mediaRequest(e);switch(t.type){case"playNewVideo":this.loadMedia("specific",t.value);break;case"playNextVideo":this.playNextVideo(e);break;case"playPreviousVideo":this.playPreviousVideo(e)}}}],[{key:"getVideoStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}},{key:"getVideoListDependencies",value:function(e){return[Cn.videoList(e)]}},{key:"getMediaRequestDependencies",value:function(e){return[Cn.mediaRequest(e)]}}]),e}(),os=function e(t){var n=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"onDependencyFailure",function(e,t){console.log("onDependencyFailure",e,t);var r=n.store,i=r.dispatch,o=r.getState;switch(e){case"ima":"blocked"!==Fi.loadingImaStatus(o())&&Qn("error")(i);break;case"hls":er("error")(i)}}),f()(this,"onDependencyReady",function(e){var t=n.store.dispatch;switch(e){case"ima":Qn("success")(t);break;case"hls":er("success")(t)}}),this.store=t},as=function(e){return function(t){t({type:"[COMMON] set fullscreen",payload:e})}},ss=function(){function e(t,n){var r=this;Ai()(this,e),f()(this,"store",void 0),f()(this,"videoTag",void 0),f()(this,"pendingFullscreenSubscriber",void 0),f()(this,"adStatusSubscriber",void 0),f()(this,"playerUniqId",void 0),f()(this,"onAdStatusChanged",function(e){var t=_i.adStatus(e),n=r.videoTag.webkitDisplayingFullscreen;"playing"===t&&Bn()&&n&&r.exitFullscreen(r.videoTag)}),f()(this,"isPlayerInFullscreen",function(){var e=document,t=Bn()?En(r.playerUniqId):bn(r.playerUniqId);return Un(e.fullscreenElement)?!Un(e.webkitFullscreenElement)&&0===e.webkitFullscreenElement.id.localeCompare(t):0===e.fullscreenElement.id.localeCompare(t)}),f()(this,"changePlayerWidth",function(e){r.videoTag.style.width=e?"100%":"auto"}),f()(this,"onFullscreenChanged",function(){var e=r.store.dispatch,t=r.isPlayerInFullscreen();r.changePlayerWidth(t),as(t)(e)}),f()(this,"onFullscreenChangedIos",function(){var e=r.store.dispatch,t=r.videoTag.webkitDisplayingFullscreen;t||on("resume")(e),r.changePlayerWidth(t),as(t)(e)}),f()(this,"onPendingFullscreenRequestChanged",function(e){var t=gn.pendingFullscreenRequest(e);"enter"===t?r.enterFullscreen(r.videoTag):"exit"===t&&r.exitFullscreen(r.videoTag)}),f()(this,"getFullScreenElement",function(e,t){var n=document.getElementById(bn(r.playerUniqId));return Bn()?t:e?document:n}),f()(this,"enterFullscreen",function(e){var t=r.getFullScreenElement(!1,e);Bn()?t.webkitEnterFullscreen():document.webkitExitFullscreen?t.webkitRequestFullscreen():document.webkitCancelFullScreen?t.webkitRequestFullScreen():document.mozCancelFullScreen?t.mozRequestFullScreen():document.msExitFullscreen&&t.msRequestFullscreen()}),f()(this,"exitFullscreen",function(e){var t=r.getFullScreenElement(!0,e);document.webkitExitFullscreen||Bn()?t.webkitExitFullscreen():document.webkitCancelFullScreen?t.webkitCancelFullScreen():document.mozCancelFullScreen?t.mozCancelFullScreen():document.msExitFullscreen&&t.msExitFullscreen()}),this.store=t,this.videoTag=document.getElementById(En(n)),this.playerUniqId=n,document.addEventListener("fullscreenchange",this.onFullscreenChanged.bind(this)),document.addEventListener("webkitfullscreenchange",this.onFullscreenChanged.bind(this)),Bn()&&(this.videoTag.addEventListener("webkitendfullscreen",this.onFullscreenChangedIos.bind(this)),this.videoTag.addEventListener("webkitbeginfullscreen",this.onFullscreenChangedIos.bind(this))),this.pendingFullscreenSubscriber=new ji(t,e.getPendingFullscreenDependencies,this.onPendingFullscreenRequestChanged.bind(this)),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this))}return Vi()(e,null,[{key:"createInstance",value:function(t,n){return new e(t,n)}}]),Vi()(e,null,[{key:"getPendingFullscreenDependencies",value:function(e){return[gn.pendingFullscreenRequest(e)]}},{key:"getAdStatusDependencies",value:function(e){return[_i.adStatus(e)]}}]),e}();function us(e,t){var n=Object.keys(e);if(Object.getOwnPropertySymbols){var r=Object.getOwnPropertySymbols(e);t&&(r=r.filter(function(t){return Object.getOwnPropertyDescriptor(e,t).enumerable})),n.push.apply(n,r)}return n}function cs(e){for(var t=1;t<arguments.length;t++){var n=null!=arguments[t]?arguments[t]:{};t%2?us(Object(n),!0).forEach(function(t){f()(e,t,n[t])}):Object.getOwnPropertyDescriptors?Object.defineProperties(e,Object.getOwnPropertyDescriptors(n)):us(Object(n)).forEach(function(t){Object.defineProperty(e,t,Object.getOwnPropertyDescriptor(n,t))})}return e}var ls,ds=function(e){return function(e){return e&&window.monti.playerConfigs&&window.monti.playerConfigs[e]}(e)?function(e){return 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n=null!=arguments[t]?arguments[t]:{};t%2?ms(Object(n),!0).forEach(function(t){f()(e,t,n[t])}):Object.getOwnPropertyDescriptors?Object.defineProperties(e,Object.getOwnPropertyDescriptors(n)):ms(Object(n)).forEach(function(t){Object.defineProperty(e,t,Object.getOwnPropertyDescriptor(n,t))})}return e}var Os={READY_EVENT:"ready",PLAY_EVENT:"play",PAUSE_EVENT:"pause",TIME_EVENT:"time",SEEK_EVENT:"seek",COMPLETE_EVENT:"complete",VOLUME_EVENT:"volume",MUTE_EVENT:"mute"},_s=Object.values(Os),Ss={FULLSCREEN_EVENT:"fullscreen",ANCHOR_STATUS_EVENT:"anchorStatusChanged",ANCHOR_CLOSED_EVENT:"anchorClosed"},Es={AD_PLAY_EVENT:"adPlay",AD_PAUSE_EVENT:"adPause",AD_RESUME_EVENT:"adResume",AD_COMPLETE_EVENT:"adComplete",AD_TIME_EVENT:"adTime",AD_MUTE_EVENT:"adMute",AD_SKIPPED_EVENT:"adSkipped",AD_ERROR_EVENT:"adError",AD_BLOCK_EVENT:"adBlock",AD_REQUEST_EVENT:"adRequest",AD_OPPORTUNITY_EVENT:"adOpportunity",AD_IMPRESSION_EVENT:"adImpression"},ws=Object.values(Es),Ps=Object.values(bs(bs(bs({},Os),Es),Ss)),Ts=function(){function e(t,n){var r=this;Ai()(this,e),f()(this,"eventsCallbacksHandler",void 0),f()(this,"store",void 0),f()(this,"videoStatusSubscriber",void 0),f()(this,"videoMuteSubscriber",void 0),f()(this,"videoVolumeSubscriber",void 0),f()(this,"videoTimeFragmentSubscriber",void 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t=hn.videoTagStatus(e);switch("seeking"===this.previousVideoTagStatus&&this.reportSeekEnd(e),t){case"paused":this.eventsCallbacksHandler.onEvent(Os.PAUSE_EVENT);break;case"seeking":this.startSeekTime=hn.currentVideoTimeFragment(e);break;case"complete":this.eventsCallbacksHandler.onEvent(Os.COMPLETE_EVENT);break;case"playing":this.eventsCallbacksHandler.onEvent(Os.PLAY_EVENT)}this.previousVideoTagStatus=t}}],[{key:"getVideoStatusDependencies",value:function(e){return[hn.videoTagStatus(e)]}}]),e}();f()(Ts,"getVideoMuteDependencies",function(e){return[gn.muted(e)]}),f()(Ts,"getVolumeDependencies",function(e){return[gn.volume(e)]}),f()(Ts,"getVideoTimeDependencies",function(e){return[hn.currentVideoTimeFragment(e)]}),f()(Ts,"getVideoListDependencies",function(e){return[Cn.videoList(e)]}),f()(Ts,"isContentEvent",function(e){return _s.some(function(t){return t===e})});var As=function e(t,n){var r=this;Ai()(this,e),f()(this,"eventsCallbacksHandler",void 0),f()(this,"store",void 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t=_i.adMuted(e);r.eventsCallbacksHandler.onEvent(Es.AD_MUTE_EVENT,{state:t})}),f()(this,"onAdProviderLoadingChanged",function(e){"blocked"===Fi.loadingImaStatus(e)&&r.eventsCallbacksHandler.onEvent(Es.AD_BLOCK_EVENT)}),f()(this,"onAdImpressionChanged",function(e){var t=_i.currentAdTag(e);r.eventsCallbacksHandler.onEvent(Es.AD_IMPRESSION_EVENT,{tag:t})}),f()(this,"onAdOpportunityChanged",function(e){var t=_i.currentAdTag(e);r.eventsCallbacksHandler.onEvent(Es.AD_OPPORTUNITY_EVENT,{tag:t})}),this.store=t,this.eventsCallbacksHandler=n,this.previousAdStatus=_i.adStatus(t.getState()),this.adStatusSubscriber=new ji(t,e.getAdStatusDependencies,this.onAdStatusChanged.bind(this)),this.adTimeSubscriber=new ji(t,e.getAdTimeDependencies,this.onAtTimeChanged.bind(this)),this.adMuteSubscriber=new ji(t,e.getAdMuteDependencies,this.onAdMuteChanged.bind(this)),this.adImpressionSubscriber=new ji(t,e.getAdImpressionDependencies,this.onAdImpressionChanged.bind(this)),this.adOpportunitySubscriber=new 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Vi()(e,[{key:"on",value:function(e,t){this.eventsHandler.onRegisterToEvent(e,t,!1)}},{key:"once",value:function(e,t){this.eventsHandler.onRegisterToEvent(e,t,!0)}}]),e}();function Ms(e,t){var n=Object.keys(e);if(Object.getOwnPropertySymbols){var r=Object.getOwnPropertySymbols(e);t&&(r=r.filter(function(t){return Object.getOwnPropertyDescriptor(e,t).enumerable})),n.push.apply(n,r)}return n}function Is(e){for(var t=1;t<arguments.length;t++){var n=null!=arguments[t]?arguments[t]:{};t%2?Ms(Object(n),!0).forEach(function(t){f()(e,t,n[t])}):Object.getOwnPropertyDescriptors?Object.defineProperties(e,Object.getOwnPropertyDescriptors(n)):Ms(Object(n)).forEach(function(t){Object.defineProperty(e,t,Object.getOwnPropertyDescriptor(n,t))})}return e}var ks=function(){var e=window.monti.dataset;return jn(e)?(e={players:{},preact:Is(Is({},r),i),store:{},plugins:{}},window.monti.dataset=e,e):e},Ns=function(e){var t=function(){var e=(new 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os(e);Ci.getInstance().addDependenciesCallback(n)}}(n),function(e,t){ks().players[t]=new Ds(e)}(n,t),t},Ls=function(e){return console.log("player initiation start",e),new Promise(function(t,n){try{var r=function(e){var t=e.player_pos||document.currentScript.parentElement,n=e.media_id||e.content_id;return cs(cs({},e),{},{player_pos:t,media_id:n})}(function(e){var t=e.player_id,n=ds(t);return null===n?e:cs(cs({},e),n)}(e)),i=Ns(r);!function(e){var t=new CustomEvent("montiConfigLoaded",{detail:{playerKey:e}});window.dispatchEvent(t)}(i),t(i)}catch(o){console.error("Player initiation error",o),n(o)}})},xs=function(){return{initiate:Ls}};window.monti=xs,Ci.getInstance().loadExternalDependencies()}]); window.monti().initiate(Object.assign({player_pos: document.currentScript.parentElement}, {"is_conflicting_with_other_jw_players":false,"programmatic_play_with_sound_on_desktop":false,"referrer_id":"af93e181-b289-0560-a2bf-808e93bb05bc","width":"100","comscore_publisher_id":"18120612","monetization":{"ad_type":"static_tag","continue_content_play_while_waiting_for_ad":false,"strategy":"on_player_load","ad_request_timeout":"10000","midrolls":{"on":[0]},"vpaid_mode":"ENABLED","ad_tag":"https://pubads.g.doubleclick.net/gampad/ads?sz=400x300|640x480|480x270|640x360&iu=/175840252/MMPlus/smithsonianmag/Video&impl=s&gdfp_req=1&env=vp&output=vast&unviewed_position_start=1&url=##REFERRER_URL_UNESC##&description_url=##DESCRIPTION_URL_UNESC##&correlator=##CACHEBUSTER##&cust_params=mm_midroll%3D##MIDROLL_ORDER##%26video_ID%3D##VIDEO_ID##"},"sponsorship":false,"player_identifier":"mplayer","recommendation_id":null,"brand_color":"#FF9900","powered_by_strip":true,"platform":"buffy","type":"video","config_name":"MM+ | Smithsonianmag | Podding","player_id":"3v9g2u2f","playlist_id":"fSkmeWKF","playback_method":"autoplay","anchor_viewability_method":"none","player_version":"v4","playlist_type":"semantic","semantic_options":{"scan_images_on_page":true,"scanned_element":"","tags":"geogrophy,nature,animals,habitat,outdoors,science,history","minimum_date_factor":30,"scanned_element_type":"tag","scoped_keywords":"mentalfloss","promoted_videos":[]},"script_destination":"mm","publisher_contribution":"floor8","general_script_description":"","brand_logo":"","brand_logo_click_url":"","next_video":"none","uniq_key":"af93e181-b289-0560-a2bf-808e93bb05bc","content_id":"fSkmeWKF","content_type":"semantic"})); Finland has vastly improved in reading, math and science literacy over the past decade in large part because its teachers are trusted to do whatever it takes to turn young lives around. This 13-year-old, Besart Kabashi, received something akin to royal tutoring.
Kari Louhiuori, a principal at a Finnish school made a mostly unheaard of and uncanny decision to hold back an immigrant student from 6th grader named Besart because he hadnʻt felt that this young man was falling behind due to laziness but to a lack of comprehension. After a year of "royal tutoring," by allowing the boy to read at his own pace, it worked!
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- Jul 2020
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www.biorxiv.org www.biorxiv.org
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Note: This rebuttal was posted by the corresponding author to Review Commons. Content has not been altered except for formatting.
Learn more at Review Commons
Reply to the reviewers
We would like to thank Reviewer #1 and #2 for the evaluation of our research and comments to our manuscript. Their comments are highly appreciated and addressed as described below.
Reviewer #1 (Evidence, reproducibility and clarity (Required)):
**Summary:**
*Provide a short summary of the findings and key conclusions (including methodology and model system(s) where appropriate).*
Here Ha et al. has further developed their Pumilio RNA tagging methodology for the isolation of UV-crosslinked proteins that are suggested to associate with Xist RNA in mouse embryonic stem cells (mESCs). Within this study the authors claim to have found the Lupus antigen RNA binding protein (La) as a novel Xist interacting partner that influences the efficacy of X-chromosome inactivation (XCI). The authors use a number of different techniques such as qPCR, fluorescent imaging, ATAC-SEQ and SHAPE to show aberration of XCI upon La shRNA knockdown. However, this study has significant flaws in the efficient isolation and validation of Xist associated proteins using their FLAG-out methodology. Furthermore, later experiments predominantly focus on cell death/survival assays, which is somewhat troubling given the essential roles La plays in processes such as cell differentiation and proliferation, ribosome biogenesis, transcriptional control and tRNA maturation. I feel the authors need to robustly address the potential effects La knockdown may be having on their mESCs.
Reviewer #1 did not fully understand the basic designs of the experimental systems (FLAG-out and iXist), and completely rejected these experimental systems. Reviewer #1 also ignored the majority of the functional analysis on the candidate protein, Ssb. These issues cannot be addressed by additional experiments
**Major comments:**
*-Are the key conclusions convincing?*
My major concern is in their Xist RNA purification.
First of all, I couldn't find any data on proving the enrichment of Xist RNA itself in their Pumilio pull-down experiment. It would have been useful to show Xist RNA enrichment before benzonase step. Secondly, it is hard to imagine the protocol would successfully isolated Xist RNA-protein complexes from the cell. An earlier report by Clemson et al., (J Cell Biol., 1996) has shown that majority of Xist RNA is still stuck in the nucleus after nuclear matrix prep protocol using detergent, which is not so different from the authors' protocol. Moreover, the authors used UV crosslink, which would have made even harder to purify Xist RNA without sonication. Thirdly, as the tag is located on 5' of Xist RNA, it is rather surprising to see that Spen is not detected in their pulldown. Spen is one of the main functional interactors with Xist, robustly detected by several previous reports. Similarly, other high-affinity binders of Xist such as hnRNP-K and Ciz1 were also lacking from this screen. Finally, the peptides found associated with FLAG-out Xist are extremely low in comparison with other data using glutaraldehyde or formaldehyde crosslinking. For example, HnRNP-M found in Chu et al 2015 has 1120 peptide counts in differentiated cells. The authors here use HnRNP-M as a baseline for specific interactions and show a total of 6 peptide counts in Xist expressing cells and 5 in i-Empty cells (Supplementary excel sheet 1). Similarly, the La protein of interest in this study has 8 counts in i-FLAG-Xist and 6 counts in i-Empty. I struggle to see how this result indicate specific Xist binding. Worryingly this is the starting rationale for the rest of their experiments, it is hard to therefore accept the rest of their conclusions either.
We have detected Xist RNA after Pumilio pull-down, and added the data in the revised manuscript (Figure S1). The enrichment of Xist RNA by Pumilio pull-down is about 75-fold, comparable to the enrichment reported by Minajigi et al.
Two out of three previous studies used similar protocols to prep cell lysates for co-IP, including UV cross-linking and detergent (McHugh et al. 2015 and Minajigi et al. 2015). The major difference between their protocols and ours is the co-IP step. They used antisense oligos to pull-down Xist RNA-protein complex, while we take advantage of the specific interaction between PUF and PBS to pull-down Xist RNA-protein complex. With the data in Figure S1, we are confident that our strategy is successful in isolating Xist RNA
For systematic identification of Xist binding proteins, each method has its own strength and weakness. As we described in the introduction, only 4 proteins were commonly identified by all three studies to systematically identify Xist binding proteins. There is no doubt that our method also missed some authentic Xist binding proteins (false negative) and identified some false positive candidates. Thus, we have to be careful in balancing between the false negative and false positive calls. The reason that we applied the ranking gain to identify Xist binding protein candidates, is to minimize the false negative rate. Meanwhile, we compared our Xist binding protein candidate list with previous identified Xist-binding proteins to enhance the confidence in our candidate lists.
Regardless the strength and weakness of our method, Ssb is also an Xist-binding protein identified by another study (Chu et al. 2015). More importantly, we have provided experimental validation to confirm Ssb’s involvement in XCI and extensive functional analysis to reveal the protein’s mechanistic role in XCI.
The other key conclusion the authors make is from the use of numerous cell death/survival assays for both male and female cell lines. This is extremely troubling in the context of assessing their target protein La. La is involved in multiple RNA maturation events of rRNAs, tRNAs and other polIII transcripts. Furthermore, La has been implicated in binding to the mRNA for Cyclin D1 in both human cells and mouse fibroblasts (NIH/3T3 - male) which show a significant effect on cell proliferation upon siRNA knockdown https://www.nature.com/articles/onc2010425. This, along with the observation that La knock-out blastocysts fail to develop any mice or ES cell lines (male or female) show the effect observed in the authors results is most likely not X-linked cell death https://mcb.asm.org/content/mcb/26/4/1445.full.pdf. The authors need to show that their shRNA KD isn't affecting the proliferation and general fitness of their mESC lines.
The cell death/survival assay was specially designed for analyzing the defect of XCI. The cell death of iXist ESCs upon adding Dox is due to the induction of Xist, which consequently initiates the silencing of the only X chromosome in male cells. Knockdown of genes involved in XCI compromises XCI, thus allowing cell survival. Given the diverse functions of Ssb in cell differentiation and proliferation, ribosome biogenesis, transcriptional control and tRNA maturation, one would expect slow growth and/or cell death of Ssb knockdown cells. Indeed, the result is consistent with our expectation (Figure 2C, without Dox). Nevertheless, more Ssb knockdown cells survive in the presence of Dox, compared with control cells (Figure 2C-E, with Dox), suggesting that Ssb plays an important role in XCI.
*- Should the authors qualify some of their claims as preliminary or speculative, or remove them altogether?*
As discussed above, I feel the authors have not clearly demonstrated Xist specific protein enrichment and haven't proven X-linked cell death. Due to the lack of necessary control experiments as discussed below, I feel the notion that La is involved directly in XCI as an RNA chaperone is currently preliminary/speculative.
The FLAG-out experiment just provided an initial point for the study. We have demonstrated the interaction between Xist and Ssb by RIP. And, Ssb knockdown antagonizes the lethal effect of induced XCI in male cells, allowing more cell to survive. This is contradictory to the diverse house-keeping functions of Ssb, which should lead to slow proliferation or cell death. Therefore, the data here (Figure 2C-E) should suggest a role of Ssb in XCI. In addition, we showed that knockdown of Ssb compromises the silencing of X-linked genes (Figure 2F, 2G, and 3E), the compaction of X chromosome (Figure 3D), Xist cloud formation (Figure 4), epigenetic modifications on Xi (Figure 5), Xist RNA folding (Figure 6F-I), and Xist RNA stability (Figure 7C and D). All these data indicate that Ssb is involved in XCI by regulating Xist RNA folding.
*- Would additional experiments be essential to support the claims of the paper? Request additional experiments only where necessary for the paper as it is, and do not ask authors to open new lines of experimentation.*
I would suggest them to show RT-qPCR results of Xist RNA enrichment from the sample after flagIP before benzonase treatment.
We have the data, and added it to Figure S1.
Also, it would have been more convincing if their negative control construct (i-Empty) would contain 25 copies of PBSb RNA at least.
This is a good alternative design of the negative control. Using i-Empty expressing 25 copies of PBSb RNA will allow us subtract the background causing by proteins binding to PBSb RNA. Yet, as discussed above, regardless how we improve the experimental setting, we cannot completely avoid the issue of false positive and false negative. Our goal of the FLAG-out experiment is to generate a list of Xist binding protein candidates, and their binding to Xist and their functions in XCI should be validated by additional experiments. With our current experimental setting, a list of Xist binding protein candidates has been generated, and we have validated the role of Ssb in XCI with subsequent experiments.
In Fig1b, the total amount of proteins loaded on the gel is not equivalent between two lanes. The gel should show equivalent amounts of proteins on the gel. It looks like if the negative control sample had been loaded at the same amount as the one with Xist, the band pattern wouldn't be distinguishable between the two samples. Furthermore, as these samples were used in the following mass spectrometry screen it may suggest that the minimal increase in peptide counts observed in the iXist FLAG-out were due to an increased amount of sample being loaded? No controls are conducted to account for this.
IP samples of i-Empty and i-FLAG-Xist were loaded in the gel in Figure 1b. It is expected that IP sample of i-FLAG-Xist should pull down more proteins than IP samples of i-Empty. The FLAG-PUFb bands (the strongest band in each lane) are about the same amount in two samples, indicating roughly equal amount of loading. After normalization of gel loading according to the FLAG-PUFb bands, the upper part of the i-FLAG-Xist lane showed some unique bands.
For mass spectrometry analysis, the loading of two samples are independent, therefore, to compare the absolute amount of each protein between the two samples does not always provide valuable information. Yet, the relative amount of different proteins within one sample is not affected by the loading amount, thus, more informative. Therefore, we used the ranking information to estimate the relative amount of different proteins in each sample and used the ranking gain to further identify protein candidates.
The authors quantify cell death in figures 2C - E. It seems clear that shSsb 1 and 2 have an effect on cell count even in the absence of Dox. The rescue effect seen upon Dox addition is minimal when compared to Empty + Dox 2D. The authors ∆A-iXist line with and without Ssb KD/Dox would be an informative control on whether the increase in cell survival that they see is X-linked.
As the reviewer pointed out earlier, Ssb plays multiple roles in cellular processes. Inevitably, KD of Ssb leads to slow growth and/or cell death with or without Dox. Thus, it is less meaningful to compare the surviving cell counts in Figure 2D. Rather, the survival rate (Figure 2E) reflects the rescuing effect more precisely. Shown in Figure 2E, both shSsb 1 and 2 increase the survival rate significantly, compared with Empty control.
Moreover, the data in Figure 3B and C demonstrated that Ssb KD compromises the survival of female differentiating cells, but not the survival of male differentiating cells, also indicating a role of Ssb in XCI. With these experiments, it should be sufficient to conclude that Ssb KD affects X-linked cell death/survival in both iXist male ESCs and WT female differentiating cells
The qPCR results used to validate silencing defects show minor changes in expression and also don't show significant silencing of X-linked genes sufficient for cell death. Could this be because only ~ 50 - 60% of Male iXist cells seem to be expressing in the movies and that this will have an effect on the observed qPCR results? Furthermore, it seems counterintuitive that expression in the Empty male cells increases in 48h compared to 14h. Is this due to cell death and positive selection of cells less able to silence their X-chromosome? How would these data look in the female XX line? How would the data look in a ∆A-iXist line in the presence and absence of shSsb/Dox?
First, high-quality live-cell imaging can only be carried out for 2 hours with 2-min time interval. The movies are meant to show the onset of Xist RNA signals. Therefore, they were taken one hour after Dox treatment (figure legend of Figure 4B-D). After overnight Dox treatment, Xist clouds can be seen in majority of cells.
Second, in Fig. 2F-G, we did not include uninduced iXist male ESCs. Therefore, it is impossible to judge whether induction of Xist in this male ESC line results in Xist-dependent silencing at 14 and 48 hr. However, in our previous publication (Li et al., JMB, 2018, 430: 2734-2746), it has been shown that Gpc4, Hprt, Mecp2, G418, and TomatoRed are silenced (4- to 16-fold reduction) at 24 and 48 hours after Dox induction.
Third, the qRT-PCR results in 14 h and in 48 h are not normalized to the same internal control. Thus, they are not directly comparable.
Confusingly, the male line in Fig 3C shows a drop in live cell count at day 6 of differentiation? Surely given their previous results in Fig 2 the Ssb KD should increase cell viability with +Dox? Ssb KD seems to have an adverse effect on ES cells during extended differentiation protocols. In Figure S1 the authors show ~ 8 - 10% survival of male lines during differentiation. Could the recombination of the Xist sequence around the loxP sites enable the cells to outcompete the dead cells? How would iEmpty and ∆A-iXist cells compare here? Have the differentiated cells been tested for their expression of Xist? Additionally, how are there similar live cell counts for male vs female lines when ~90% of male cells die during differentiation? Were more cells plated at day 4? If so, this would bias the competition of male cell survival and therefore make the male line an inappropriate control.
Given the essential role of La during development a control is needed to prove that this death is X-linked in the female 3F1 line. For example, an XO cell line retaining the Cast allele and shSsb expression could show the amount of death caused from shSsb alone independent of X-linked cell death.
The reviewer completely misunderstood the experiment. The severe cell death specifically observed in female differentiating ESCs is a strong evidence showing Ssb is involved in XCI (Figure 3).
The male ESCs in Figure 3C is a WT ESC line without the inducible Xist transgene, in which no XCI occurs upon differentiation. It is completely different from iXist male ESCs with Dox, in which forced Xist induction leads to XCI. Thus, the diverse functions of Ssb might contribute to the slight decrease in live cell count of wild type male cells at day 6 of differentiation.
Figure S2 shows the differentiation of iXist male ESCs with or without Dox. As explained above, forced Xist induction silences the only X chromosome in male cells, resulting in cell death. In addition, XCI occurs more efficiently in differentiation condition (Figure S2) than in pluripotent status (Figure 2C)
During differentiation, female ESCs silence one X chromosome, and the other X chromosome remains active. KD of Ssb compromises XCI, and two X chromosomes in some female differentiating cells maintain active, leading to cell death. The reviewer is correct that we need a control to rule out that the essential role of Ssb during development affects cell survival and death. An XO cell line can be used as a control. Similarly, a male cell line (XY) is also a good control. We already included a male cell line as a control in Figure 3B and 3C.
If I understood correctly, the RNA FISH used dsDNA probes ("Sx9") against 40 kb of the X-inactivation centre (Xic). Surely Tsix or other Xic transcripts will also be visible? Can the authors use their RNA FISH to determine the XX or XO status of their cells? In Figure S5 a number of cells appear to show a single pinpoint of transcription. This could either be low levels of Xist transcripts or Xic transcription from an XO line in which the 129 chromosome is missing. It would be best to solely quantify cells which have two x chromosomes and if a significant amount of X chromosomes have been kicked out, this should be discussed and controlled for.
This is a valid concern, but this concern can be adequately addressed with the available data in the manuscript.
First, if the female Ssb KD cell line is an “XO” cell line, in which the X129 allele is “kicked out”, the RNA allelotyping results should show an absolute “silencing” of the X129 allele. However, in complete contrast to this notion, RNA allelotyping detected “more” RNA transcripts from X129, showing the chromosome-wide XCI defects (Figure 3D).
Second, overexpression of Ssb in Ssb KD female cells restores the Xist clouds and the polycomb marks (Figure S8), suggesting that the Ssb KD female cells are XX, but not XO.
Third, the severe cell death specifically occurred in female Ssb KD lines is also against the “XO” argument (Figure 3B&C).
In Fig6, the authors generated a number of Ssb constructs for a rescue assay. However, these results complicate the matter and raise more questions than they address. It seems odd that the ∆RRM1 does not rescue based on comparison with their putative negative control, ∆NLS. However, the ∆RRM1 + 2 and ∆LAM do rescue the phenotype better than the full length Ssb? This makes no logical sense and highlights the inherent variation in cell viability these generated cell lines seem to show.
Following on from this, figure S7 quantifies the GFP tag mRNA levels, depicting all ∆RRM mutants with expression below ~30%? How can ∆RRM1 or 2 be rescuing in this scenario? Have these lines been tested for their XX or XO status? The loss of an X chromosome would lead to a rescue of the cell death phenotype, which is a process known to occur in XX lines that have been cultured for extended periods of time. Could it also be that the cell lines derived are more or less sensitive to exogenous shRNA expression? Also, further validation is needed to assess the efficiency of KD in these lines as theoretically most of these constructs will be targeted by shRNA? What is the endogenous Ssb expression level in these lines? Where in the mRNA sequence are the shRNAs targeted to? Does this make sense on the relative expression levels of ∆RRM1/2 for example? Further testing of GFP expression could also be assessed by quantitative western blot of GFP or even visualised in their RNA FISH/IF samples (Figure S8), currently neither are shown. In addition, some kind of information of stability of each Ssb protein constructs has not been demonstrated.
Our shRNA targets the LAM domain, so the expression of ∆LAM is not affected by the shRNA. The reviewer is correct that the detected GFP expression levels of ∆RRM1 and ∆RRM2 are too low to be conclusive. We have removed the data point of ∆RRM1 and ∆RRM2. Meanwhile, it is clear that ∆RRM1&2 has a better rescuing effect than ∆NLS, when ∆RRM1&2 and ∆NLS are expressed at similar levels. Ssb is a well known RNA chaperone/RNA helicase. Identifying Ssb is an Xist-binding protein already suggests the functional role of Ssb in XCI. The data of the plasmid rescue experiments further suggests that Ssb is involved in XCI as a RNA chaperone/RNA helicase.
As for the Western blot and GFP fluorescence (IF), we have tried both. Neither of them detected GFP signal, reflecting the low expression level of these GFP fusion proteins. As the reviewers pointed out that the shSsb is not targeting the 5’ or 3’-UTR region, therefore, interfering the exogenous Ssb as well. This might be a reason for the low expression of these GFP fusion proteins.
For the data shown in Figure 7A and B the authors quantify the % of cells with Xist signal. The authors have already shown a defect in Xist visualisation in Ssb KD. Surely it is plausible to assume a faster loss of Xist signal below background in weaker expressing cells. A more appropriate quantification would be the % loss of Xist signal per cell over time.
With Figure 7C and D, the samples have been treated with actinomycin D which globally affects the transcription of cells even the PolIII associated genes Ssb is needed to mature. This treatment could have an added effect on cell mortality and function. Data confirming that actinomycin D doesn't affect the cells disproportionately is needed. The difference in half-life could be attributed to such a treatment.
We agree with the reviewer that monitoring Xist signal loss per cell would be a better way to analyze the data. However, in Xist signal loss experiment, snapshot images were taken at four time points (1h, 2h, 3h and 4h). This is not a time-lapse imaging. High-quality time-lapse imaging can only be done within a 2-hour time period with 2-min time interval. Therefore, cell-tracking cannot be done in this experiment. In addition, even though Ssb KD slows down the formation of Xist cloud within the early phase (3 hours) of Xist induction (Figure 4), prolonged (overnight) Xist induction leads to Xist cloud formation in a significant fraction of Ssb KD cells, and the Xist cloud signals are about the same in WT and Ssb KD cells (Figure 7A, 0 h). Similarly, qRT-PCR also revealed that Xist RNA are at the same level in WT and Ssb KD cells (Figure 7C, 0 h). These data argue against that a faster loss of Xist signal in Ssb KD cells is due to weaker initial Xist signal.
Actinomycin D was added at the last 11 hours of the experiment. During this period, no obvious adverse effects on cells were observed.
In summarising the authors claim that La binds Xist to facilitate folding and appropriate spreading of Xist along the X-chromosome. No direct interaction has been shown, CLIP-seq data would resolve this, however I do understand this is a challenging technique. The authors have instead opted for RIP followed by qPCR (Figure S2). However, this process has a greater potential for non-specific recovery of RNAs via indirect binding. Furthermore, qPCR may also amplify the relative abundance of the RNA detected. As multiple nucleolar proteins came down in the mass spec screen and FLAG-Ssb is being over expressed, it is plausible to assume some transient Xist interactions may arise from nucleolar association at which La will be in high abundance. Positive and negative nuclear RNA controls (e.g. 7SK and U1 snRNA respectively) could be used so to determine the amount of non-specific Protein-RNA interactions in their RIP pull downs. Cytoplasmic actin is not an appropriate control as it is cytosolic.
We have to clarify one point that the mass spec screen analyzed samples pulled down by FLAG-PUFb, but not FLAG-Ssb.
We did not intend to distinguish whether Ssb directly binds Xist or is just associated with Xist. RIP followed by qPCR is sufficient to prove the association between Ssb and Xist RNA.
We can include nuclear RNA as controls, if the reviewer regards RIP as a valid method to show protein and RNA association
Other than this the authors may want to probe (via IF) for the presence of La accumulation on the X? Many other know factors such as Ciz1, hnrnpK and PRC1/2 complexes show clear accumulation on the X. If I understand correctly, there are many La antibodies on the market and endogenous levels on the X could be assessed. These antibodies may be useful in IP's and pull downs also.
Many XCI factors play extensive roles in the cell and are not clearly enriched on Xi, including Spen (Moindrot et al. 2015). We have tried the immunostaining and did not detect Ssb’s enrichment on Xi. Ssb shows a general distribution in the nucleus without a clear enrichment on Xi (data not shown).
*-Are the suggested experiments realistic in terms of time and resources? It would help if you could add an estimated cost and time investment for substantial experiments.*
The experiments suggested above are centrally focussed on the cell lines that are currently in the authors possession with maybe exceptions with the ∆A-iXist-shSsb line suggested. However, this should be reasonably quick to obtain given their previous work for this paper. Most experiments suggested will focus on the validation of karyotype, Xist expression, rescue construct expression, further RNA FISH classification and repeating more appropriate positive and negative controls for a number of experiments. In theory this can be obtained relatively simply and quickly from current resources. But with the sheer volume of further experiments that are required here, this may take a significant amount of time.
One vital improvement needed is the replication of mass spec data and the validation of Xist specific recovery and protein enrichment. As it stands this manuscript seems to not have any replicates of the FLAG-out methodology and mass spec data. This is troubling given the poor recovery and specificity of the protein samples obtained. Repeating these experiments would be costly in time and also financially. As it stands, I feel this is essential to conclusively validate their target of interest.
*- Are the data and the methods presented in such a way that they can be reproduced?*
The data is presented relatively well, however, it would be beneficial if deailed methods were in the main text and not in a supplementary file. Similarly, more information about the process of differentiation and how cell death/survival was quantified and validated is needed.
The reviewer rejected the basic design of the experimental system and ignored the majority of the functional analysis data. No additional experiment can address these issues
We can include more information in the main text, regarding Ssb. However, there is limited space for the main text, various depending on the journals. Meanwhile, the current citation on Ssb is adequate to emphasize that Ssb is a versatile RNA binding protein involved in a variety of fundamental RNA processing events in the cell.
*- Are the experiments adequately replicated and statistical analysis adequate?*
In the most part yes, however there seems to be no replicates of the FLAG-out mass spec screen which is worrying given the minimal specificity observed in the current data.
As we mentioned above, the FLAG-out experiment only serves as a starting point to generate a list of Xist binding protein candidates. Rather than repeating the FLAG-out experiment, we compared the result of FLAG-out to previously published lists of Xist binding protein candidates. More importantly, additional experiments are carried out to validate the Xist binding proteins identified by FLAG-out.
**Minor comments:**
*- Specific experimental issues that are easily addressable.*
Unfortunately, the majority of experimental issues need to be addressed with more robust data which are highlighted above. However, some image analysis, quantification and classification can be amended relatively easily. For example, the live-cell imaging data should be quantified as loss of signal as discussed and RNA FISH should be used to classify XX positive cells and the XO cells can be discarded from analysis.
We have addressed these issue in the previous sections of this rebuttal.
*- Are prior studies referenced appropriately?*
Most papers regarding Xist pull down and biology are discussed and referenced appropriately. However, the role in which La plays during development and its aberrant affects upon KD are seemingly downplayed. I would like to see more discussion of potential defects that could be caused due to globally altering cellular RNA folding.
We have tried to cite key references about Ssb in development and RNA folding. Due to length limitation, we cannot cite all references in the topic. If necessary, we could discuss the possibility of indirect effect of Ssb KD on XCI through globally altering cellular RNA folding.
*- Are the text and figures clear and accurate?*
For the most part, lots of the figures are clear and accurate. Apart from these exceptions.
1.The Y-axis of Figure 2D is confusing. What does 0.3 as a "sum of area" equate to? 30% of the area was ES cells? This doesn't look to be the case from Fig 2C. Also, how does the intensity of the signal compare? The area may not be a good quantification due to ES cells growing in colonies.
We have revised the Y-axis labelling of Figure 2D to “sum of area cm2”. Thus, “0.3” means that the area of ESCs is 0.3 cm2. ALPP is highly expressed on ES cell surface. ALPP stain usually produce saturated stains on ES cell colonies. Thoroughly stained ES cell colonies, big and small, show similar signal intensity levels. To analyze the “total signal intensity” will be not much different from “sum of area”.
2.In the Movies S1-7 there are boxes around certain cells and marked with "Figure 5a - c". This seems to be incorrect as figure 5 is currently the IF staining of polycomb marks. I assume this is in relation to Figure 4b-d?
We have corrected the labelling mistakes.
3.Similarly, in Movies S1-7, the intensities of Xist foci seem by eye to be similar. In the paper it is claimed that the Xist clouds that do form are lower in intensity. Are the Movies depicting the same range of pixel intensities? If not, this should be amended. Similarly, figure 7 seems to show relatively equivalent RNA signal at 0 h?
All the images were collected using a fixed standard of the microscope and camera setting, and these movies depict the same range of pixel intensities. Movies S1-S3 are WT control, and Movies S4-S7 are Ssb KD cells. The Xist cloud signals are weaker in Movie S4-S7 (also quantified in Figure 4E). For the Xist cloud signal, not only the intensity, but also the area of Xist cloud, have to be taken into account.
The 0 h in Figure 7 is after overnight Dox treatment, and different from the time point in Movies S1-7 (maximum 3 hour Dox treatment, figure legend of Figure 4B-D). The discrepancy can be explained by that knockdown of Ssb only slows down the formation of Xist clouds. After overnight forced expression, the Xist RNA still shows an accumulation in the cells. Figure 7 shows the forced accumulation of Xist RNA after prolonged Dox treatment disappears faster after Dox withdraw.
4.In figure 4A the data is from female XX cells, this should be highlighted to limit confusion with the male iXist data shown below in 4B-E. It would also be helpful to have the male/female icons (as in figure 3B), for each figure that has images of cells. Currently Figure 4, 5, 7, S5 and S8 are lacking these icons.
We have revised the labelling on Figure 3, 4, 5, 7 S6 and S9 (S5 and S8 before revision).
5.No explanation of the Flag-Ssb expression is given for figure S2. Furthermore, is it really necessary to express Flag-Ssb? There are reasonably good antibodies out there for Ssb as this was how it was originally found in Systemic Lupus patients. Also, no data showing the amount of Ssb being overexpressed is shown. This may have big implication to the validity of the RIP-qPCR analysis.
We could perform qRT-PCR to quantify the overexpression level of Flag-Ssb. If required, we could use Ssb antibody to do Western blot to show the amount of Flag-Ssb protein.
*- Do you have suggestions that would help the authors improve the presentation of their data and conclusions?
Most of the data is presented reasonably well, but the robustness of the data somewhat retracts from their conclusions. I feel the certainty of their conclusion regarding Xist specific La binding and RNA chaperone activity is still presumptive and should be rewritten unless more robust data can confirm Xist interaction. I would also suggest deciding on the nomenclature for the protein of interest and use either La or Ssb, the continued use of both through the figures and text can get a little confusing to the reader.
In the current literatures, Ssb seems to be commonly used as a gene name and La is used as a protein name. We have revised the manuscript to use one name “Ssb” to describe both the gene and the protein.
Reviewer #1 (Significance (Required)):
*- Describe the nature and significance of the advance (e.g. conceptual, technical, clinical) for the field.*
It was a good trial to use PBSb-PUFb system to purify Xist RNA binding proteins, compared to previous reports had used anti-sense oligo purification using complementary sequence to Xist RNA sequences. But currently the purification still needs further validation and repeats to confirm its use. A potential complementary technique could be to isolate Xist directly by using biotinylated probes against the PBSb sequence.
The authors further claim the identification of a novel Xist RNA chaperone (La/Ssb) which they say facilitates XCI progression. This would be a novel finding in the field; however, the data is currently not robust enough to support this
*- Place the work in the context of the existing literature (provide references, where appropriate).*
This work has focused on the development of a milder methodology for purifying Xist RNA during XCI. Others have published similar methodologies predominantly focusing on purifying Xist RNA directly with biotinylated probes (McHugh et al. 2015; Minaji et al. 2015; and Chu et al. 2015). Although this method boasts a milder purification method, it seems to be low yielding in Xist specific proteins. Others have shown a more robust identification of bona fide Xist binding proteins which are currently missing in this manuscript. A recent preprint from the Plath lab has identified new factors involved in XCI during differentiation and their tethering/rescue experiments are far more convincing than the ones shown in this manuscript https://www.biorxiv.org/content/10.1101/2020.03.09.979369v1. The candidate protein Ha et al. have identified has multiple roles in developing cells and has shown to be important during mouse development. However, Ha et al do not robustly show that the knockdown of Ssb causes X-linked cell mortality. Alternatively, as would be presumed from Ssb's essential role in many housekeeping short non-coding RNAs, the cell death seems more ubiquitous upon shRNA KD. Therefore, the link the authors are making here are relatively weak.
Ssb KD rescues cell death caused by forced induction of Xist in male ESCs. In addition, Ssb KD leads to cell death in differentiating female ESCs, while it has a negligible effect on cell death in differentiating male ESCs. These data clearly demonstrated X-linked cell survival/mortality by Ssb KD.
Plath lab’s work is different from ours. In their manuscript, the authors report the observation of a protein condensation which is assembled by Xist but sustains in absence of Xist. TDP-43 (a.k.a. Tardbp) happens to be one protein factor involved in the protein condensation and also one candidate protein selected for further validation in our study. In our study, Tardbp KD did not rescue cell death caused by induced XCI in male cells. Thus, Tardbp is not further studied. In the manuscript, we have discussed the possibility that low efficiency of knockdown and redundancy might contribute to the failure in validation of Tardbp
*- State what audience might be interested in and influenced by the reported findings.*
The audience may be interested in the novel technique and the finding of a novel Xist binding protein.
*- Define your field of expertise with a few keywords to help the authors contextualize your point of view. Indicate if there are any parts of the paper that you do not have sufficient expertise to evaluate.*
RNA biochemistry and developmental biology
Reviewer #2 (Evidence, reproducibility and clarity (Required)):
**Summary:**
This manuscript describes a novel "FLAG-out" system, where the authors sought to identify Xist RNA binding proteins. The authors focused on a specific protein found in their screen and also identified in several other screens for Xist RNA binding proteins, Ssb/La, and further characterize the role of this protein in XCI. This manuscript describes the loss of Ssb/La and suggest that it predominately impacts the canonical 'cloud' formation of Xist RNA on the X chromosome during XCI initiation. Further, they determine that loss of Ssb/La decreases Xist RNA half-life and alters folding of Xist RNA transcripts. Based on their findings, the authors propose that Ssb/La functions to directly bind and fold Xist RNA transcripts in a manner that stabilizes Xist RNA, allowing for proper 'cloud' formation and successful initiation of XCI.
**Major comments:**
The authors made an interesting findings that the SLE-relevant autoantigen Ssb/La stabilizes Xist RNA transcripts, and there is some evidence that this occurs by binding and maintaining proper folding of Xist RNA. Despite these intriguing observations, there are many parts of the manuscript that need to be addressed in order to support the authors main conclusions.
The most troubling aspect of this manuscript is the persistent use of an artificial XCI system in male cells to draw strong conclusions about the function of Ssb in XCI. This issue is prevalent throughout the manuscript, and I question why the authors chose to perform most of their experiments in male cells when the same experiments can be (and have previously been by other groups) performed in female cells. Using male ESCs and then making conclusions for XCI, which is a female-specific process, is a major concern.
In addition to iXist male ESC line, many experiments, such as cell death/survival (Figure 3B, C), allelotype (Figure 3E), Xist could formation (Figure 4A), H3K27me3 and H2AK119ub IF (Figure 5), were performed in female ESC. We chose to do SHAPE and Xist RNA stability assays in iXist male ESC line, because the onset of XCI is much more synchronized in this system. Moreover, in female cells, Xa causes additional layers of complication/noise in the ATAC-sequencing which may not be fully cleared up by data analysis. On the other hand, inducible Xist expression in male ESCs can be used as an experimental system to recapitulate the silencing step of XCI (Ha et al. 2018; Wutz et al. 2002).
Out of the 138 identified binding proteins, the authors chose to only validate three: Mybbp1a, Tardbp, and Ssb/La. The logic for choosing these candidates is weak, and the authors are only able to validate 1 out of 3 of these proteins.
In theory, all candidate proteins in the list are possibly involved in XCI. There is no method which can help to make accurate prediction. We did not follow a clear-cut logic in selecting candidates for validation, but we do consider the candidate gene’s knockout phenotype, “early embryonic lethality”, as a phenotype consistent with a critical role of the candidate gene in XCI. Meanwhile, in the manuscript, we have discussed why we chose the three proteins for validation as the following:
“……From the candidate proteins, we shortlisted three proteins for individual validation. Myb-binding protein 1A (Mybbp1a, Q7TPV4) and TAR DNA-binding protein 43 (Tardbp, Q921F2) were selected because they are known transcription repressors (11, 12). The Lupus autoantigen La (P32067, encoding-gene name: Ssb) was selected because systemic lupus erythematosus (SLE) is an autoimmune disease characterized by a strikingly high female to male ratios of 9:1 (13). Moreover, its autoimmune antigen La is a ubiquitous and versatile RNA-binding protein and a known RNA chaperone (14). All the three selected candidates have also been identified as Xist-binding proteins in previous studies (2, 4). Moreover, the knockout of these three genes all lead to early embryonic death. Tardbp knockout causes embryonic lethality at the blastocyst implantation stage (15). Mybbp1a and Ssb knockout affect blastocyst formation (16, 17). Early embryonic lethality is a mutant phenotype consistent with a critical role of the mutated gene in XCI (1)** ……”
We used cell death/survival assay to further validate the role of Xist binding protein candidates in XCI. This is a stringent assay. It requires not only that Xist binding protein candidates bind to Xist, but also that the candidates have to be functionally important in XCI.
Indeed, it has been demonstrated by Plath lab (the BioRxix manuscript mentioned by reviewer 1) that Tardbp (also named TDP-43), together with other RBPs, bind to the E repeat of Xist to form a condensate and create an Xi-domain. Yet, Tardbp KD did not rescue cell death caused by forced XCI in male cells in our studies. Thus, only 1 out of 3 of these candidates is validated and further studied. In the manuscript, we also discussed that low efficiency of knockdown and redundancy might contribute to the failure in validation of Tardbp and Mybbp1a.
Use of the cell death assay is not strong enough to "confirm that La is involved in induced XCI" as stated by the authors. This is a huge overstatement.
Given the diverse functions of Ssb in cell differentiation and proliferation, ribosome biogenesis, transcriptional control and tRNA maturation, one would expect less surviving Ssb knockdown cells. In contrast, more Ssb knockdown cells survives in the presence of Dox, suggesting that Ssb plays an important role in XCI. Considering the reviewer’s comment, we revised the sentence to “further suggest that Ssb is involved in induced XCI”.
While the authors observed differences in X-linked gene expression after Ssb KD, they did not examine expression of these genes in after KD of either Mybbp1a or Tardbp. Are the changes observed in these genes specific to Ssb KD? Or could there still be alterations of X-linked gene expression in the non-validated KDs? This experiment should be performed and included in the manuscript, either within Fig 2 or in the supplemental. As well, inclusion of a well characterized positive control, for example Hnrnpu, as comparison to Ssb should be included.
Mybbp1a and Tardbp were not validated by the cell death assay. Thus, compared with Ssb, Mybbp1a and Tardbp are less important for XCI functionally. We only focused on Ssb in the subsequent studies. Mybbp1a and Tardbp KD could be additional negative controls. Yet, we have used empty vector as a negative control. We do not need so many controls.
As mentioned, Tardbp indeed binds to Xist RNA. It is very likely that Tardbp KD might alter some X-linked gene expression. This rules out Tardbp KD as a good negative control.
If we do not see any effect of Ssb KD on X-linked gene expression, a positive control is absolutely required. However, we have detected that Ssb KD compromises the silencing of several X-linked gene. A positive control might not be essential.
The authors perform RIP to validate the interaction of Ssb with Xist, but this is performed in male ES cells with induced Xist RNA and with FLAG-tagged Ssb. Aside from these cells being male, in this system Xist RNA expression is much higher than would be found endogenously. RIP should have been done in female differentiated ESCs if there is in fact a role for XCI.
The authors need to include more details in the methods section to explain how the FLAG-Ssb is expressed in these cells, and why the authors chose to use a tagged contrast over endogenous Ssb. Due to these issues the result from this experiment is essentially meaningless and is not convincing of Ssb interaction with Xist RNA. There is no reason RIP cannot be performed in female cells, and the authors should repeat this experiment in the relevant experimental condition. As well, if a validated Ssb antibody exists the authors should perform RIP using the endogenous protein.
If required, we could try to perform RIP and/or CLIP using Ssb antibody in female cells.
The authors state in Fig 3A-C that the results of the cell death and differentiation experiments "...support a functional role of La in XCI". The authors state earlier that Ssb is a ubiquitous protein that is embryonic lethal (in both female and males). Based on this, the cell death results shown do not support a functional role of La in XCI as the Ssb KD could be having an indirect affect due to its other developmental functions. This manuscript lacks a direct functional link between Ssb and XCI; more data is necessary.
Given the diverse functions of Ssb in cell differentiation and proliferation, ribosome biogenesis, transcriptional control and tRNA maturation, one would expect less surviving Ssb knockdown cells. In contrast, more Ssb knockdown cells survives in the presence of Dox, suggesting that Ssb plays an important role in XCI.
For the data in Fig 3A-C, Ssb KD causes the death of female differentiating cells, but not male differentiating cells. Therefore, it rules out that the death of female cells is due to the general function of Ssb. Rather, the specific role of Ssb in XCI contributes to the female specific cell death.
In Fig 3D, the authors perform ATAC-seq in inducible male ES cells. The authors claim that the extremely slight reduction in chromatin compaction of the Ssb KD compared to control iXist "directly connect La to the heterochromatinization of Xi, supporting a functional role of La in XCI". This is also an overstatement based on the minimal, and possibly indirect, change in compaction. The positive control i-detaA-Xist sample has significantly less compaction (and thus significantly higher compaction defect) than the Ssb KD again disputing the claim stated above. It is unclear why performing ATAC-seq is even necessary, as Ssb isn't stated to have a function in regulating chromatin architecture. In addition, why the authors performed ATAC-seq in the artificial male XCI system and not in the F1 female cells, and the N of the experiment is unclear. If the authors want to include the ATAC-seq in further revisions it should be repeated n=3 in the female system.
The male induced XCI system provides a more synchronized onset of XCI. More importantly, in the male induced XCI system, only one X chromosome exists, avoiding the interference from the active X chromosome in female cells. If ATAC-seq was performed in female cells, only loci with SNPs can be distinguished. The sequencing reads from Xa will create additional layers of complication/noise which may not be cleared up fully by data analysis
“i-delat-Xist” is a positive control to show the experimental system works. It is not justified to compare the chromatin accessibility of the mutant, which is only a Ssb “knockdown” mutant, and the control “i-delat-Xist”, in which the Repeat A is “deleted”. We admit that ATAC-Seq results did not reveal a drastic difference in chromatin accessibility between the wild type sample and the mutant sample. However, as what we discussed in the manuscript, clear difference can still be seen at the 14 h time point. This is shown clearly by the heatmap (Fig. 3E) and the sequencing coverage profile (Fig. S4A).
In Fig 6, the authors state in their methods that "The shRNA construct, which worked efficiently against Ssb, was not designed against the 3' UTR of the RNA. Therefore, the shRNA is against some of the rescue plasmid constructs. Nonetheless, transfecting the Ssb knockdown cells with the rescue plasmids should compensate the effect of Ssb knockdown and serve as a rescue assay to study the functional domains of La.". This is troubling and seems like a major experimental issue; the specific rescue constructs that may be impacted by this issue are not stated and should be explicitly mentioned. This becomes more confusing when examining the data from rescue experiments.
We pointed out this issue in the original manuscript. We agree that the experiment was not perfectly designed. In the revision, we added in the information on the shRNA target site. Our shRNA targets the LAM domain, so the expression of ∆LAM is not affected by the shRNA. We agree that the detected GFP expression levels of ∆RRM1 and ∆RRM2 are too low to be conclusive. In the revision, we have removed the data point of ∆RRM1 and ∆RRM2. Meanwhile, it is clear that ∆RRM1&2 has a better rescuing effect than ∆NLS, when ∆RRM1&2 and ∆NLS are expressed at similar levels. Ssb is a well-known RNA chaperone/RNA helicase. Identifying Ssb is an Xist-binding protein already suggests the functional role of Ssb in XCI. The data of the plasmid rescue experiments further suggests that Ssb is involved in XCI as a RNA chaperone/RNA helicase.
If it is necessary, we could redo this experiments using a shSsb targeting 3’-UTR or expressing GFP-Ssb immune to shSsb.
In Figure S7, the expression of the rescue constructs deltaRRM1 and deltaRRM2 is extremely low, yet the authors observe a rescue of the cloud phenotype (fig 6D) from those constructs that reaches almost the level of full length Ssb. This is confusing, and the authors need to address this by performing a western blot to show the protein levels of these rescue constructs and discuss further how such a low level of expression can show a rescue phenotype. The results would also be stronger if the authors examined H3K27me3 and H2AK119ub1 enrichment since they observed decreased overlap of these marks with Xist RNA after Ssb KD. Finally, the authors state that "...all three RNA-binding domains are required for the functionality of La in XCI..." however I have trouble coming to this conclusion based on the above issues. As well, if the authors want to support direct function, they should repeat the RIP experiments with these rescues constructs to show that the domains capable of rescue can still bind to Xist RNA.
Reviewer 1 raised similar concerns. In Figure 6C, the live cell counts of ∆RRM1 and ∆NLS are about the same. It might be due to the low expression level of ∆RRM1 (Figure S7). It is clear that ∆RRM1&2 has a better rescuing effect than ∆NLS, when ∆RRM1&2 and ∆NLS are expressed as similar levels. To make the data more straight forward, we removed the data point of ∆RRM1 and ∆RRM2, because of their low expression levels.
As for the Western blot and GFP fluorescence (IF), we have tried both. Neither of them detected GFP signal, reflecting the low expression level of these GFP fusion proteins. The shSsb is not targeting the 5’ or 3’-UTR region, therefore interfering the exogenous Ssb as well. This might be a reason for the low expression of these GFP fusion proteins. If it is necessary, we could redo this experiments using a shSsb targeting 3’–UTR or expressing GFP-Ssb immune to shSsb.
We deleted the sentence "all three RNA-binding domains are required for the functionality of La in XCI".
**Minor comments:**
The authors may want to consider better highlighting the strengths of their "FLAG-out" system. As written, is it difficult to tell how this system sets them apart from the previously published studies referenced in the text, especially as some of these studies used similar crosslinking conditions and cell types. Additionally, the logic and questions the authors pose in the introduction as to why they performed this project are too general and not very strong. For example, the authors mention how might protein machinery may assemble on Xist RNA, and how might Xist RNA may spread on the X chromosome. However neither of these topics are actually addressed in their experiments or discussion. These are interesting questions, but the authors should either discuss them further within the context of their results or take these questions out. It would also be helpful if the authors could better label Figure 4, as it is unclear in the figure itself that Fig 4A is in reference to female cells, but remaining panels are in male cells.
The inducible XCI in male cells is a valid system to recapitulate the silencing step of XCI. It also provides unique advantages in many experiments, such as ATAC-seq. Meanwhile, we did perform extensive functional analysis on the endogenous XCI process using female cells. However, we do realize that presenting the data of induced XCI in male cells together with the data from female cells is confusing to many readers. We have revised the labelling on Figure 3, 4, 5, 7 S6 and S9 (S5 and S8 before revision).
To understand “how the protein machinery is assembled by Xist” and “how Xist spreads along its host chromosome territory” are not specifically the initial aims of this study. We removed the sentences from the introduction section. However, we believe Ssb may provide clues for the future studies to fully address these questions, and we did provide the following thoughts in the discussion section:
“……Secondly, as Ssb is able to utilize ATP to unwind RNA-RNA and RNA-DNA duplex, it may play a more active role in controlling the structural dynamics of Xist in living cells (14, 23). These structural dynamics may be important for recruiting proteins onto the RNA and spreading of the RNA along its host chromosome territory……”
Reviewer #2 (Significance (Required)):
I am not convinced the this manuscript, as written, has sufficient novelty. Ssb/La has been previously identified to be an Xist RNA binding protein with older/different approaches. However, there are some interesting observations in this manuscript. Major revisions are necessary.
We agree with the reviewer that identification of Ssb as an Xist RNA binding protein is not novel. The novelty of our discovery lies in: 1) we developed a new method for isolating lincRNA associated proteins; 2) we confirmed that Ssb is an important player involved in XCI; 3) we showed that Ssb regulates the folding of Xist RNA, consequently the stability of Xist and the formation of Xist cloud.
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