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Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

Cell apical constriction driven by actomyosin contraction forces is a conserved mechanism during tissue folding in embryo development. While much is now understood of the molecular mechanism responsible for apical constriction and of the tissue-scale integration of the ensuing in-plane deformations,...

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Autores principales: Fierling, Julien, John, Alphy, Delorme, Barthélémy, Torzynski, Alexandre, Blanchard, Guy B., Lye, Claire M., Popkova, Anna, Malandain, Grégoire, Sanson, Bénédicte, Étienne, Jocelyn, Marmottant, Philippe, Quilliet, Catherine, Rauzi, Matteo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9187723/
https://www.ncbi.nlm.nih.gov/pubmed/35688832
http://dx.doi.org/10.1038/s41467-022-30493-3
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author Fierling, Julien
John, Alphy
Delorme, Barthélémy
Torzynski, Alexandre
Blanchard, Guy B.
Lye, Claire M.
Popkova, Anna
Malandain, Grégoire
Sanson, Bénédicte
Étienne, Jocelyn
Marmottant, Philippe
Quilliet, Catherine
Rauzi, Matteo
author_facet Fierling, Julien
John, Alphy
Delorme, Barthélémy
Torzynski, Alexandre
Blanchard, Guy B.
Lye, Claire M.
Popkova, Anna
Malandain, Grégoire
Sanson, Bénédicte
Étienne, Jocelyn
Marmottant, Philippe
Quilliet, Catherine
Rauzi, Matteo
author_sort Fierling, Julien
collection PubMed
description Cell apical constriction driven by actomyosin contraction forces is a conserved mechanism during tissue folding in embryo development. While much is now understood of the molecular mechanism responsible for apical constriction and of the tissue-scale integration of the ensuing in-plane deformations, it is still not clear if apical actomyosin contraction forces are necessary or sufficient per se to drive tissue folding. To tackle this question, we use the Drosophila embryo model system that forms a furrow on the ventral side, initiating mesoderm internalization. Past computational models support the idea that cell apical contraction forces may not be sufficient and that active or passive cell apico-basal forces may be necessary to drive cell wedging leading to tissue furrowing. By using 3D computational modelling and in toto embryo image analysis and manipulation, we now challenge this idea and show that embryo-scale force balance at the tissue surface, rather than cell-autonomous shape changes, is necessary and sufficient to drive a buckling of the epithelial surface forming a furrow which propagates and initiates embryo gastrulation.
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spelling pubmed-91877232022-06-12 Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation Fierling, Julien John, Alphy Delorme, Barthélémy Torzynski, Alexandre Blanchard, Guy B. Lye, Claire M. Popkova, Anna Malandain, Grégoire Sanson, Bénédicte Étienne, Jocelyn Marmottant, Philippe Quilliet, Catherine Rauzi, Matteo Nat Commun Article Cell apical constriction driven by actomyosin contraction forces is a conserved mechanism during tissue folding in embryo development. While much is now understood of the molecular mechanism responsible for apical constriction and of the tissue-scale integration of the ensuing in-plane deformations, it is still not clear if apical actomyosin contraction forces are necessary or sufficient per se to drive tissue folding. To tackle this question, we use the Drosophila embryo model system that forms a furrow on the ventral side, initiating mesoderm internalization. Past computational models support the idea that cell apical contraction forces may not be sufficient and that active or passive cell apico-basal forces may be necessary to drive cell wedging leading to tissue furrowing. By using 3D computational modelling and in toto embryo image analysis and manipulation, we now challenge this idea and show that embryo-scale force balance at the tissue surface, rather than cell-autonomous shape changes, is necessary and sufficient to drive a buckling of the epithelial surface forming a furrow which propagates and initiates embryo gastrulation. Nature Publishing Group UK 2022-06-10 /pmc/articles/PMC9187723/ /pubmed/35688832 http://dx.doi.org/10.1038/s41467-022-30493-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Fierling, Julien
John, Alphy
Delorme, Barthélémy
Torzynski, Alexandre
Blanchard, Guy B.
Lye, Claire M.
Popkova, Anna
Malandain, Grégoire
Sanson, Bénédicte
Étienne, Jocelyn
Marmottant, Philippe
Quilliet, Catherine
Rauzi, Matteo
Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title_full Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title_fullStr Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title_full_unstemmed Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title_short Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
title_sort embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9187723/
https://www.ncbi.nlm.nih.gov/pubmed/35688832
http://dx.doi.org/10.1038/s41467-022-30493-3
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