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Experimental validation of force inference in epithelia from cell to tissue scale

Morphogenesis relies on the active generation of forces, and the transmission of these forces to surrounding cells and tissues. Hence measuring forces directly in developing embryos is an essential task to study the mechanics of development. Among the experimental techniques that have emerged to mea...

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Autores principales: Kong, Weiyuan, Loison, Olivier, Chavadimane Shivakumar, Pruthvi, Chan, Eunice HoYee, Saadaoui, Mehdi, Collinet, Claudio, Lenne, Pierre-François, Clément, Raphaël
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787039/
https://www.ncbi.nlm.nih.gov/pubmed/31601854
http://dx.doi.org/10.1038/s41598-019-50690-3
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author Kong, Weiyuan
Loison, Olivier
Chavadimane Shivakumar, Pruthvi
Chan, Eunice HoYee
Saadaoui, Mehdi
Collinet, Claudio
Lenne, Pierre-François
Clément, Raphaël
author_facet Kong, Weiyuan
Loison, Olivier
Chavadimane Shivakumar, Pruthvi
Chan, Eunice HoYee
Saadaoui, Mehdi
Collinet, Claudio
Lenne, Pierre-François
Clément, Raphaël
author_sort Kong, Weiyuan
collection PubMed
description Morphogenesis relies on the active generation of forces, and the transmission of these forces to surrounding cells and tissues. Hence measuring forces directly in developing embryos is an essential task to study the mechanics of development. Among the experimental techniques that have emerged to measure forces in epithelial tissues, force inference is particularly appealing. Indeed it only requires a snapshot of the tissue, as it relies on the topology and geometry of cell contacts, assuming that forces are balanced at each vertex. However, establishing force inference as a reliable technique requires thorough validation in multiple conditions. Here we performed systematic comparisons of force inference with laser ablation experiments in four epithelial tissues from two animals, the fruit fly and the quail. We show that force inference accurately predicts single junction tension, tension patterns in stereotyped groups of cells, and tissue-scale stress patterns, in wild type and mutant conditions. We emphasize its ability to capture the distribution of forces at different scales from a single image, which gives it a critical advantage over perturbative techniques such as laser ablation. Overall, our results demonstrate that force inference is a reliable and efficient method to quantify the mechanical state of epithelia during morphogenesis, especially at larger scales when inferred tensions and pressures are binned into a coarse-grained stress tensor.
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spelling pubmed-67870392019-10-17 Experimental validation of force inference in epithelia from cell to tissue scale Kong, Weiyuan Loison, Olivier Chavadimane Shivakumar, Pruthvi Chan, Eunice HoYee Saadaoui, Mehdi Collinet, Claudio Lenne, Pierre-François Clément, Raphaël Sci Rep Article Morphogenesis relies on the active generation of forces, and the transmission of these forces to surrounding cells and tissues. Hence measuring forces directly in developing embryos is an essential task to study the mechanics of development. Among the experimental techniques that have emerged to measure forces in epithelial tissues, force inference is particularly appealing. Indeed it only requires a snapshot of the tissue, as it relies on the topology and geometry of cell contacts, assuming that forces are balanced at each vertex. However, establishing force inference as a reliable technique requires thorough validation in multiple conditions. Here we performed systematic comparisons of force inference with laser ablation experiments in four epithelial tissues from two animals, the fruit fly and the quail. We show that force inference accurately predicts single junction tension, tension patterns in stereotyped groups of cells, and tissue-scale stress patterns, in wild type and mutant conditions. We emphasize its ability to capture the distribution of forces at different scales from a single image, which gives it a critical advantage over perturbative techniques such as laser ablation. Overall, our results demonstrate that force inference is a reliable and efficient method to quantify the mechanical state of epithelia during morphogenesis, especially at larger scales when inferred tensions and pressures are binned into a coarse-grained stress tensor. Nature Publishing Group UK 2019-10-10 /pmc/articles/PMC6787039/ /pubmed/31601854 http://dx.doi.org/10.1038/s41598-019-50690-3 Text en © The Author(s) 2019 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/.
spellingShingle Article
Kong, Weiyuan
Loison, Olivier
Chavadimane Shivakumar, Pruthvi
Chan, Eunice HoYee
Saadaoui, Mehdi
Collinet, Claudio
Lenne, Pierre-François
Clément, Raphaël
Experimental validation of force inference in epithelia from cell to tissue scale
title Experimental validation of force inference in epithelia from cell to tissue scale
title_full Experimental validation of force inference in epithelia from cell to tissue scale
title_fullStr Experimental validation of force inference in epithelia from cell to tissue scale
title_full_unstemmed Experimental validation of force inference in epithelia from cell to tissue scale
title_short Experimental validation of force inference in epithelia from cell to tissue scale
title_sort experimental validation of force inference in epithelia from cell to tissue scale
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787039/
https://www.ncbi.nlm.nih.gov/pubmed/31601854
http://dx.doi.org/10.1038/s41598-019-50690-3
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