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Polarized Dishevelled dissolution and condensation drives embryonic axis specification in oocytes

S. Zachary Swartz, Tzer Han Tan, Margherita Perillo, Nikta Fakhri, Gary M. Wessel, Athula H. Wikramanayake, Iain M. Cheeseman

Preprint posted on 18 May 2021 https://www.biorxiv.org/content/10.1101/2021.05.17.444558v1

Article now published in Current Biology at http://dx.doi.org/10.1016/j.cub.2021.10.022

Preprint from @ZakSwartz at @iaincheeseman lab on dynamic spatial distribution and condensation behaviour of Dishevelled, #Wnt signaling cascade, during #primary axis specification in sea star, Patiria miniata oocytes

Selected by Sukriti Kapoor

Categories: cell biology, developmental biology

Background

Establishment of long-range concentration gradients of signaling molecules, called morphogens (Greek, ‘form givers’), is essential for embryogenesis. One such morphogen is the Wnt family of secretory signaling ligands. Highly conserved Wnt genes are found in all animal genomes and are critical for several events during embryogenesis, such as axis specification, body segmentation, fate specification and cell differentiation1,2.

When Wnt is OFF, beta-catenin is continually degraded in the cells. Wnt signaling is ON when the Wnt ligand binds to the Frizzled (Fz)/Low density lipoprotein related-receptor protein (LRP) transmembrane receptors which leads to phosphorylation and activation of Dishevelled (Dvl). Activated Dvl associates with Axin and this complex prevents the degradation of beta-catenin which leads to the accumulation of beta-catenin in the cell and the nucleus3. Beta-catenin in the nucleus turns on the transcription of Wnt target genes.

To ensure axis specification, Wnt signaling must be activated asymmetrically at one pole of the embryo4,5. The current study on sea star, Patiria miniata oocytes sheds light on the polarized molecular assembly of Dvl, necessary for the establishment of body axis. The authors find that Dvl associates with the late endosomes and that it preferentially condenses into granular punctate assemblies at the posterior axis. These assemblies are dynamic, i.e., they (1) rapidly exchange with the cytoplasm, (2) display fusion and fission events, and (3) can easily dissolve and reform in a matter of minutes.

Figure (adapted from manuscript) shows the spatial distribution of Dishevelled (Dvl) during meiosis and development of sea star (Patiria miniate) oocytes. In prophase arrested oocytes, Dvl is uniformly distributed at the cortex in the form of puncta. Following hormonal stimulation (fertilization mimic) meiosis resumes in the oocytes with the simultaneous dissolution of Dvl puncta. Dvl puncta then re-appear and form larger, more stable condensates, asymmetrically enriched at the posterior.

Key findings

Beta-catenin protein (Wnt pathway, above) forms a concentration gradient along the anterior (low)-posterior (high) axis of the sea star oocytes. Gradation in protein levels result in highest Wnt activity at the posterior and lowest at the anterior. The differential activity of beta-catenin leads to altered transcription across different sections of oocyte, i.e., regions with highest levels of beta catenin will turn on a set of genes different from the ones with intermediate or low levels of beta catenin. This is the basis of axis formation and fate specification in the oocytes. In the absence of beta-catenin concentration or activity gradient, the oocytes fail to establish their primary anterior-posterior axis and do not proceed to gastrulation. Hence, the spatial restriction of beta-catenin activity in the posterior is crucial for embryogenesis

What regulates beta-catenin protein concentration gradient required for differential Wnt signaling along the anterior-posterior axis of the oocytes? Dvl accumulates at the cortex of the posterior axis and restricts the activity of beta-catenin at the posterior of the embryo. In this study, the authors show that inhibition of Dvl activity using specific morpholinos blocked the expression of Wnt responsive genes in the posterior region of the oocytes and these oocytes also failed to undergo gastrulation. Thus, Dvl acts upstream of beta-catenin activity regulation and is likewise required for the formation anterior-posterior body axis.

Dvl restricts beta-catenin at the posterior, but how is Dvl itself restricted to the posterior? Of note, Wnt signaling is cell-autonomous because of the absence of any contact of the oocyte with neighboring somatic cells in these experiments. Hence, the mechanism by which Dvl is restricted is regulated by a yet unknown inherent asymmetry within the oocyte itself. To better understand the localization pattern of Dvl in oocytes, the authors in the study performed live-imaging of oocytes expressing GFP-tagged Dvl during the oocyte-embryo transition. Initially, in oocytes arrested in meiosis, Dvl protein was found to assemble as puncta throughout the cortex. Upon hormonal stimulation, however, when meiosis resumes in the oocyte, there was a simultaneous loss of Dvl puncta from the cortex. These puncta then re-appeared and enriched at the posterior cortex at the completion of meiosis. These observations indicate that the localization of Dvl in oocytes is under cell cycle regulation.

Noting that Dvl assembles as puncta, the authors in this study propose that the dissolution and reappearance of Dvl may be governed by phase-transition and condensation-like process. Using image segmentation and particle analysis tools, Dvl puncta was categorized into two discrete populations – (1) cytoplasmic and (2) cortical. Time-lapse imaging showed that puncta could undergo fusion and fission events. These observations suggest that Dvl forms dynamic molecular condensates. Interestingly, FRAP experiments showed that the larger, uniformly distributed puncta (in meiosis arrested oocytes) were more mobile than the Dvl puncta which concentrated at the posterior of the oocytes upon meiosis completion.

What could be the difference between uniformly distributed puncta and the smaller, more dynamic puncta that asymmetrically enrich at the posterior of the oocytes and are responsible for the determination of body axis? The authors propose that the difference could be because of (a) more stable binding of Dvl at the posterior cortex or (b) an inherent cellular asymmetry within the oocytes. In line with the second hypothesis, the authors found a tight correlation between the movement of the Dvl puncta and that of the endosomes. The nature of association with the endosomes and the role of endosomes in Dvl condensation and its enrichment at the posterior is an exciting area for future studies.

What I like about this preprint?

Establishment of cellular asymmetry is required for axis specification during embryogenesis across the animal kingdom. In this study, the authors have made use of a simple model organism (sea-star oocytes) to study the molecular nature of assembly of Dvl, key member of the highly conserved Wnt signaling cascade, during axis specification. Dvl was shown to assemble into condensates that could freely exchange with the cytoplasm. The Dvl condensates at the posterior axis were more stable than the condensates which were uniformly distributed at the time of meiosis arrest, and before axis determination. While an exact, detailed process of Dvl self-assembly is still unclear from the current study, this model system could be extremely useful in studying the dynamics of phase transition and condensation events in future.

Observations in the study indicate that the endosomes may have some role in establishing the asymmetric activity gradient of Dvl. This hypothesis is intriguing and demands a much more detailed examination of the role of polarized trafficking in generating cellular asymmetry. The significance of endosomes and polarized trafficking during axis establishment and fate specification during embryogenesis is an exciting area of study for future research.

Conclusions and future outlook

  1. Can the authors describe what would happen to the Dvl protein in meiosis-arrested oocytes? Will it get degraded over time? What would happen to the protein pool associated with the endosomes?
  2. The authors show that Dvl condensation at the posterior pole is cell-cycle regulated. Can the authors comment on whether biochemical changes (pH, for instance) that could occur in the oocyte upon hormonal stimulation have any role to play in Dvl condensation. Specifically, are there any potential physical or chemical cues that could be activated upon hormonal stimulation?
  3. In the study, it is shown that the dissected portion of the posterior pole alone is capable of condensing and enriching Dvl. Are these Dvl puncta similar in terms of mobility when compared to the intact oocyte? Have the authors checked the association of Dvl with the endosomes in the cut-out posterior portion of the oocyte?
  4. Can the authors comment on the organization of the endosomes in oocytes? What can the authors say about the role of polarized trafficking, if any, in Dvl enrichment at the posterior?
  5. The mobility and assembly of the Dvl puncta is under cell cycle regulation. Do the authors think that the Dvl protein which forms puncta at the posterior is different in terms of specific post-translational modifications (specifically, its phosphorylation status)?
  6. Would the authors like to comment on proteins that interact with Dvl that help with the condensation?
  7. Can the authors make a generalised comment on the significance of puncta formation and phase transition in the generation of asymmetric cues during embryogenesis?
References
  1. Logan, C. Y. & Nusse, R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781–810 (2004).
  2. Clevers, H. Wnt/β-Catenin Signaling in Development and Disease. Cell 127, 469–480 (2006).
  3. Kan, W. et al. Limited dishevelled/axin oligomerization determines efficiency of wnt/b-catenin signal transduction. Elife 9, 1–33 (2020).
  4. Petersen, C. P. & Reddien, P. W. Wnt Signaling and the Polarity of the Primary Body Axis. Cell 139, 1056–1068 (2009).
  5. McCauley, B. S., Akyar, E., Rosa Saad, H. & Hinman, V. F. Dose-dependent nuclear β-catenin response segregates endomesoderm along the sea star primary axis. Dev. 142, 207–217 (2015).

Tags: body axis, embryogenesis, sea star, wnt signaling

Posted on: 15 July 2021

doi: https://doi.org/10.1242/prelights.30074

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Author's response

S. Zachary Swartz shared

Can the authors describe what would happen to the Dvl protein in meiosis-arrested oocytes? Will it get degraded over time? What would happen to the protein pool associated with the endosomes?

ZS: This is an interesting idea. The half-life of Dvl has been measured to be roughly 8 hours in some mammalian cell lines (https://www.jbc.org/article/S0021-9258(19)62608-6/fulltext). Dvl is also subject to ubiquitination (https://pubmed.ncbi.nlm.nih.gov/25907794/). We don’t yet have a good sense for the stability of Dvl protein in oocytes, but one of our ideas is that its association with endosomes may promote its stability and inheritance as a signaling domain across the cell cycle. Indeed, a link between Dvl stability and endocytosis has been previous suggested (https://onlinelibrary.wiley.com/doi/10.1111/j.1365-201X.2007.01688.x). Lastly, our preliminary work suggest that ongoing protein synthesis is dispensable for Dvl localization, which could indicate that turnover is not a major component of this phenomenon. We are excited follow up on this in future work.

The authors show that Dvl condensation at the posterior pole is cell-cycle regulated. Can the authors comment on whether biochemical changes (pH, for instance) that could occur in the oocyte upon hormonal stimulation have any role to play in Dvl condensation. Specifically, are there any potential physical or chemical cues that could be activated upon hormonal stimulation?

ZS: Great question. Our work (https://www.biorxiv.org/content/10.1101/2020.08.21.260216v1.full) and work from others (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5968197/) has demonstrated that there is an enormous amount of phosphorylation that occurs across the proteome in response to hormonal reception. One possibility is that a cell-cycle related kinase, such as cyclin-dependent kinase, directly or indirectly phosphorylates Dvl downstream of the hormone receptor.

In the study, it is shown that the dissected portion of the posterior pole alone is capable of condensing and enriching Dvl. Are these Dvl puncta similar in terms of mobility when compared to the intact oocyte? Have the authors checked the association of Dvl with the endosomes in the cut-out posterior portion of the oocyte?

ZS: We have not tested this, but we should as a future experiment! We predict that the association with endosomes will be retained in the isolated vegetal fragments. However, there could be some differences in mobility or residence time on the endosomes in this experimental context. As these experiments to dissect the oocyte are technically challenging, this will need a separate sustained effort.

Can the authors comment on the organization of the endosomes in oocytes? What can the authors say about the role of polarized trafficking, if any, in Dvl enrichment at the posterior?

ZS: At this point, the most we can say is that these endosomes are positive for Lamp1 and Rab7, which could mean this is a type of late endosome, a de facto lysosome, or an oocyte-specific organelle such as the reserve granules (https://pubmed.ncbi.nlm.nih.gov/12464181/). One possibility is that these endosomes are derived from the plasma membrane, and contain internalized frizzled receptors (see https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5809524/). Polarized trafficking in the endocytic pathway is an interesting hypothesis. In future work, we hope to better resolve the spatial arrangement of the ER, Golgi, and other endomembrane compartments in the oocyte.

The mobility and assembly of the Dvl puncta is under cell cycle regulation. Do the authors think that the Dvl protein which forms puncta at the posterior is different in terms of specific post-translational modifications (specifically, its phosphorylation status)?

ZS: We think this is a strong possibility. Prior work in the sea urchin has found that the vegetally-localized Dvl has different mobility characteristics under 2D gel electrophoresis (https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0080693) indicative of post-translational modifications. Phosphorylation by a specific kinase would be a strong candidate for this, and we plan to test this in future studies.

Would the authors like to comment on proteins that interact with Dvl that help with the condensation?

ZS: Having now established the sea star oocyte as a system for studying Dvl localization and function, we hope to perform immunoprecipitation and mass spectrometry in the future to identify potential binding partners – please stay tuned!

Can the authors make a generalized comment on the significance of puncta formation and phase transition in the generation of asymmetric cues during embryogenesis?

ZS: The ability to selectively partition molecular determinants into certain cell lineages is an important and fundamental principle in developmental biology. We see this in many contexts in nature, from the formation of the Balbiani body in frogs, the germ plasm in Drosophila, and the p-granules in elegans, which Branwynn and colleagues beautifully showed form by selective condensation (https://science.sciencemag.org/content/324/5935/1729.abstract). We are excited to see here in the sea star oocyte that these principles may also apply to other paradigms, including the Wnt pathway and primary axis specification.

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