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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,...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2022
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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. |
format | Online Article Text |
id | pubmed-9187723 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
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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