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Mechanical Tension Drives Elongational Growth of the Embryonic Gut

During embryonic development, most organs are in a state of mechanical compression because they grow in a confined and limited amount of space within the embryo’s body; the early gut is an exception because it physiologically herniates out of the coelom. We demonstrate here that physiological hernia...

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Autores principales: Chevalier, Nicolas R., de Witte, Tinke-Marie, Cornelissen, Annemiek J. M., Dufour, Sylvie, Proux-Gillardeaux, Véronique, Asnacios, Atef
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5902462/
https://www.ncbi.nlm.nih.gov/pubmed/29662083
http://dx.doi.org/10.1038/s41598-018-24368-1
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author Chevalier, Nicolas R.
de Witte, Tinke-Marie
Cornelissen, Annemiek J. M.
Dufour, Sylvie
Proux-Gillardeaux, Véronique
Asnacios, Atef
author_facet Chevalier, Nicolas R.
de Witte, Tinke-Marie
Cornelissen, Annemiek J. M.
Dufour, Sylvie
Proux-Gillardeaux, Véronique
Asnacios, Atef
author_sort Chevalier, Nicolas R.
collection PubMed
description During embryonic development, most organs are in a state of mechanical compression because they grow in a confined and limited amount of space within the embryo’s body; the early gut is an exception because it physiologically herniates out of the coelom. We demonstrate here that physiological hernia is caused by a tensile force transmitted by the vitelline duct on the early gut loop at its attachment point at the umbilicus. We quantify this tensile force and show that applying tension for 48 h induces stress-dependent elongational growth of the embryonic gut in culture, with an average 90% length increase (max: 200%), 65% volume increase (max: 160%), 50% dry mass increase (max: 100%), and 165% cell number increase (max: 300%); this mechanical cue is required for organ growth as guts not subject to tension do not grow. We demonstrate that growth results from increased cell proliferation when tension is applied. These results outline the essential role played by mechanical forces in shaping and driving the proliferation of embryonic organs.
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spelling pubmed-59024622018-04-25 Mechanical Tension Drives Elongational Growth of the Embryonic Gut Chevalier, Nicolas R. de Witte, Tinke-Marie Cornelissen, Annemiek J. M. Dufour, Sylvie Proux-Gillardeaux, Véronique Asnacios, Atef Sci Rep Article During embryonic development, most organs are in a state of mechanical compression because they grow in a confined and limited amount of space within the embryo’s body; the early gut is an exception because it physiologically herniates out of the coelom. We demonstrate here that physiological hernia is caused by a tensile force transmitted by the vitelline duct on the early gut loop at its attachment point at the umbilicus. We quantify this tensile force and show that applying tension for 48 h induces stress-dependent elongational growth of the embryonic gut in culture, with an average 90% length increase (max: 200%), 65% volume increase (max: 160%), 50% dry mass increase (max: 100%), and 165% cell number increase (max: 300%); this mechanical cue is required for organ growth as guts not subject to tension do not grow. We demonstrate that growth results from increased cell proliferation when tension is applied. These results outline the essential role played by mechanical forces in shaping and driving the proliferation of embryonic organs. Nature Publishing Group UK 2018-04-16 /pmc/articles/PMC5902462/ /pubmed/29662083 http://dx.doi.org/10.1038/s41598-018-24368-1 Text en © The Author(s) 2018 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
Chevalier, Nicolas R.
de Witte, Tinke-Marie
Cornelissen, Annemiek J. M.
Dufour, Sylvie
Proux-Gillardeaux, Véronique
Asnacios, Atef
Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title_full Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title_fullStr Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title_full_unstemmed Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title_short Mechanical Tension Drives Elongational Growth of the Embryonic Gut
title_sort mechanical tension drives elongational growth of the embryonic gut
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5902462/
https://www.ncbi.nlm.nih.gov/pubmed/29662083
http://dx.doi.org/10.1038/s41598-018-24368-1
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