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Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface

Pattern formation and morphogenesis of cell populations is essential for successful embryogenesis. Steinberg proposed the differential adhesion hypothesis, and differences in cell–cell adhesion and interfacial tension have proven to be critical for cell sorting. Standard theoretical models such as t...

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Autores principales: Koyama, Hiroshi, Suzuki, Makoto, Yasue, Naoko, Sasaki, Hiroshi, Ueno, Naoto, Fujimori, Toshihiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9001851/
https://www.ncbi.nlm.nih.gov/pubmed/35425767
http://dx.doi.org/10.3389/fcell.2022.864135
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author Koyama, Hiroshi
Suzuki, Makoto
Yasue, Naoko
Sasaki, Hiroshi
Ueno, Naoto
Fujimori, Toshihiko
author_facet Koyama, Hiroshi
Suzuki, Makoto
Yasue, Naoko
Sasaki, Hiroshi
Ueno, Naoto
Fujimori, Toshihiko
author_sort Koyama, Hiroshi
collection PubMed
description Pattern formation and morphogenesis of cell populations is essential for successful embryogenesis. Steinberg proposed the differential adhesion hypothesis, and differences in cell–cell adhesion and interfacial tension have proven to be critical for cell sorting. Standard theoretical models such as the vertex model consider not only cell–cell adhesion/tension but also area elasticity of apical cell surfaces and viscous friction forces. However, the potential contributions of the latter two parameters to pattern formation and morphogenesis remain to be determined. In this theoretical study, we analyzed the effect of both area elasticity and the coefficient of friction on pattern formation and morphogenesis. We assumed the presence of two cell populations, one population of which is surrounded by the other. Both populations were placed on the surface of a uniformly expanding environment analogous to growing embryos, in which friction forces are exerted between cell populations and their expanding environment. When the area elasticity or friction coefficient in the cell cluster was increased relative to that of the surrounding cell population, the cell cluster was elongated. In comparison with experimental observations, elongation of the notochord in mice is consistent with the hypothesis based on the difference in area elasticity but not the difference in friction coefficient. Because area elasticity is an index of cellular stiffness, we propose that differential cellular stiffness may contribute to tissue elongation within an expanding environment.
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spelling pubmed-90018512022-04-13 Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface Koyama, Hiroshi Suzuki, Makoto Yasue, Naoko Sasaki, Hiroshi Ueno, Naoto Fujimori, Toshihiko Front Cell Dev Biol Cell and Developmental Biology Pattern formation and morphogenesis of cell populations is essential for successful embryogenesis. Steinberg proposed the differential adhesion hypothesis, and differences in cell–cell adhesion and interfacial tension have proven to be critical for cell sorting. Standard theoretical models such as the vertex model consider not only cell–cell adhesion/tension but also area elasticity of apical cell surfaces and viscous friction forces. However, the potential contributions of the latter two parameters to pattern formation and morphogenesis remain to be determined. In this theoretical study, we analyzed the effect of both area elasticity and the coefficient of friction on pattern formation and morphogenesis. We assumed the presence of two cell populations, one population of which is surrounded by the other. Both populations were placed on the surface of a uniformly expanding environment analogous to growing embryos, in which friction forces are exerted between cell populations and their expanding environment. When the area elasticity or friction coefficient in the cell cluster was increased relative to that of the surrounding cell population, the cell cluster was elongated. In comparison with experimental observations, elongation of the notochord in mice is consistent with the hypothesis based on the difference in area elasticity but not the difference in friction coefficient. Because area elasticity is an index of cellular stiffness, we propose that differential cellular stiffness may contribute to tissue elongation within an expanding environment. Frontiers Media S.A. 2022-03-29 /pmc/articles/PMC9001851/ /pubmed/35425767 http://dx.doi.org/10.3389/fcell.2022.864135 Text en Copyright © 2022 Koyama, Suzuki, Yasue, Sasaki, Ueno and Fujimori. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Koyama, Hiroshi
Suzuki, Makoto
Yasue, Naoko
Sasaki, Hiroshi
Ueno, Naoto
Fujimori, Toshihiko
Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title_full Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title_fullStr Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title_full_unstemmed Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title_short Differential Cellular Stiffness Contributes to Tissue Elongation on an Expanding Surface
title_sort differential cellular stiffness contributes to tissue elongation on an expanding surface
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9001851/
https://www.ncbi.nlm.nih.gov/pubmed/35425767
http://dx.doi.org/10.3389/fcell.2022.864135
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