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Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop
Epithelial tissues form folded structures during embryonic development and organogenesis. Whereas substantial efforts have been devoted to identifying mechanical and biochemical mechanisms that induce folding, whether and how their interplay synergistically shapes epithelial folds remains poorly und...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8675927/ https://www.ncbi.nlm.nih.gov/pubmed/34871312 http://dx.doi.org/10.1371/journal.pcbi.1009614 |
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author | Wen, Fu-Lai Kwan, Chun Wai Wang, Yu-Chiun Shibata, Tatsuo |
author_facet | Wen, Fu-Lai Kwan, Chun Wai Wang, Yu-Chiun Shibata, Tatsuo |
author_sort | Wen, Fu-Lai |
collection | PubMed |
description | Epithelial tissues form folded structures during embryonic development and organogenesis. Whereas substantial efforts have been devoted to identifying mechanical and biochemical mechanisms that induce folding, whether and how their interplay synergistically shapes epithelial folds remains poorly understood. Here we propose a mechano–biochemical model for dorsal fold formation in the early Drosophila embryo, an epithelial folding event induced by shifts of cell polarity. Based on experimentally observed apical domain homeostasis, we couple cell mechanics to polarity and find that mechanical changes following the initial polarity shifts alter cell geometry, which in turn influences the reaction-diffusion of polarity proteins, thus forming a feedback loop between cell mechanics and polarity. This model can induce spontaneous fold formation in silico, recapitulate polarity and shape changes observed in vivo, and confer robustness to tissue shape change against small fluctuations in mechanics and polarity. These findings reveal emergent properties of a developing epithelium under control of intracellular mechano–polarity coupling. |
format | Online Article Text |
id | pubmed-8675927 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-86759272021-12-17 Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop Wen, Fu-Lai Kwan, Chun Wai Wang, Yu-Chiun Shibata, Tatsuo PLoS Comput Biol Research Article Epithelial tissues form folded structures during embryonic development and organogenesis. Whereas substantial efforts have been devoted to identifying mechanical and biochemical mechanisms that induce folding, whether and how their interplay synergistically shapes epithelial folds remains poorly understood. Here we propose a mechano–biochemical model for dorsal fold formation in the early Drosophila embryo, an epithelial folding event induced by shifts of cell polarity. Based on experimentally observed apical domain homeostasis, we couple cell mechanics to polarity and find that mechanical changes following the initial polarity shifts alter cell geometry, which in turn influences the reaction-diffusion of polarity proteins, thus forming a feedback loop between cell mechanics and polarity. This model can induce spontaneous fold formation in silico, recapitulate polarity and shape changes observed in vivo, and confer robustness to tissue shape change against small fluctuations in mechanics and polarity. These findings reveal emergent properties of a developing epithelium under control of intracellular mechano–polarity coupling. Public Library of Science 2021-12-06 /pmc/articles/PMC8675927/ /pubmed/34871312 http://dx.doi.org/10.1371/journal.pcbi.1009614 Text en © 2021 Wen et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Wen, Fu-Lai Kwan, Chun Wai Wang, Yu-Chiun Shibata, Tatsuo Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title | Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title_full | Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title_fullStr | Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title_full_unstemmed | Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title_short | Autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
title_sort | autonomous epithelial folding induced by an intracellular mechano–polarity feedback loop |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8675927/ https://www.ncbi.nlm.nih.gov/pubmed/34871312 http://dx.doi.org/10.1371/journal.pcbi.1009614 |
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