The Geometric Basis of Epithelial Convergent Extension
Curation statements for this article:-
Curated by eLife
eLife assessment
This is a very strong, well-written, and interesting paper analyzing in an original way how tension pattern dynamics can reveal the contribution of active versus passive intercalation during tissue elongation. The authors apply a new concept of isogonal tension decomposition to extract a global map of tissue mechanics that will be extremely valuable in the field of biomechanics. The model is convincing to explain the authors' data but could be strengthened further by analyzing data from mutant backgrounds that could serve as a test.
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Abstract
Shape changes of epithelia during animal development, such as convergent extension, are achieved through concerted mechanical activity of individual cells. While much is known about the corresponding large scale tissue flow and its genetic drivers, fundamental questions regarding local control of contractile activity on cellular scale and its embryo-scale coordination remain open. To address these questions, we develop a quantitative, model-based analysis framework to relate cell geometry to local tension in recently obtained timelapse imaging data of gastrulating Drosophila embryos. This analysis provides a systematic decomposition of cell shape changes and T1-rearrangements into internally driven, active, and externally driven, passive, contributions. Our analysis provides evidence that germ band extension is driven by active T1 processes that self-organize through positive feedback acting on tensions. More generally, our findings suggest that epithelial convergent extension results from controlled transformation of internal force balance geometry which combines the effects of bottom-up local self-organization with the top-down, embryo-scale regulation by gene expression.
Article activity feed
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eLife assessment
This is a very strong, well-written, and interesting paper analyzing in an original way how tension pattern dynamics can reveal the contribution of active versus passive intercalation during tissue elongation. The authors apply a new concept of isogonal tension decomposition to extract a global map of tissue mechanics that will be extremely valuable in the field of biomechanics. The model is convincing to explain the authors' data but could be strengthened further by analyzing data from mutant backgrounds that could serve as a test.
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Joint Public Review:
Summary:
Brauns et al. work to decipher the respective contribution of active versus passive contributions to cell shape changes during germ band elongation. Using a novel quantification tool of local tension, their results suggest that epithelial convergent extension results from internal forces.
Strengths:
The approach developed here, tension isogonal decomposition, is original and the authors made the demonstration that we can extract comprehensive data on tissue mechanics from this type of analysis.
They present an elegant diagram that quantifies how active and passive forces interact to drive cell intercalations.
The model qualitatively recapitulates the features of passive and active intercalation for a T1 event.
Regions of high isogonal strains are consistent with the proximity of known active regions.
They …
Joint Public Review:
Summary:
Brauns et al. work to decipher the respective contribution of active versus passive contributions to cell shape changes during germ band elongation. Using a novel quantification tool of local tension, their results suggest that epithelial convergent extension results from internal forces.
Strengths:
The approach developed here, tension isogonal decomposition, is original and the authors made the demonstration that we can extract comprehensive data on tissue mechanics from this type of analysis.
They present an elegant diagram that quantifies how active and passive forces interact to drive cell intercalations.
The model qualitatively recapitulates the features of passive and active intercalation for a T1 event.
Regions of high isogonal strains are consistent with the proximity of known active regions.
They define a parameter (the LTC parameter) which encompasses the geometry of the tension triangles and allows the authors to define a criterium for T1s to occur.
The data are clearly presented, going from cellular scale to tissue scale, and integrating modeling approach to complement the thoughtful description of tension patterns.
Weaknesses:
The modeling is interesting, with the integration of tension through tension triangulation around vertices and thus integrating force inference directly in the vertex model. However, the authors are not using it to test their hypothesis and support their analysis at the tissue level. Thus, although interesting, the analysis at the tissue level stays mainly descriptive.
Major points:
(1) The authors mention that from their analysis, they can predict what is the tension threshold required for intercalations in different conditions and predict that in Snail and Twist mutants the T1 tension threshold would be around √2. Since movies of these mutants are most probably available, it would be nice to confirm these predictions.
(2) While the formalism is very elegant and convincing, and also convincingly allows making sense of the data presented in the paper, it is not all that clear whether the claims are compatible with previous experimental observations. In particular, it has been reported in different papers (including Collinet et al NCB 2015, Clement et al Curr Biol 2017) that affecting the initial Myosin polarity or the rate of T1s does not affect tissue-scale convergent extension. Analysis/discussion of the Tor phenotype (no extension with myosin anisotropy) and the Eve/Runt phenotype (extension without Myosin anisotropy), which seem in contradiction with an extension mostly driven by myosin anisotropy.
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