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Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers

A monolayer of highly motile cells can establish long-range orientational order, which can be explained by hydrodynamic theory of active gels and fluids. However, it is less clear how cell shape changes and rearrangement are governed when the monolayer is in mechanical equilibrium states when cell m...

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Autores principales: Xie, Tianfa, St Pierre, Sarah R, Olaranont, Nonthakorn, Brown, Lauren E, Wu, Min, Sun, Yubing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8478414/
https://www.ncbi.nlm.nih.gov/pubmed/34542405
http://dx.doi.org/10.7554/eLife.60381
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author Xie, Tianfa
St Pierre, Sarah R
Olaranont, Nonthakorn
Brown, Lauren E
Wu, Min
Sun, Yubing
author_facet Xie, Tianfa
St Pierre, Sarah R
Olaranont, Nonthakorn
Brown, Lauren E
Wu, Min
Sun, Yubing
author_sort Xie, Tianfa
collection PubMed
description A monolayer of highly motile cells can establish long-range orientational order, which can be explained by hydrodynamic theory of active gels and fluids. However, it is less clear how cell shape changes and rearrangement are governed when the monolayer is in mechanical equilibrium states when cell motility diminishes. In this work, we report that rat embryonic fibroblasts (REF), when confined in circular mesoscale patterns on rigid substrates, can transition from the spindle shapes to more compact morphologies. Cells align radially only at the pattern boundary when they are in the mechanical equilibrium. This radial alignment disappears when cell contractility or cell-cell adhesion is reduced. Unlike monolayers of spindle-like cells such as NIH-3T3 fibroblasts with minimal intercellular interactions or epithelial cells like Madin-Darby canine kidney (MDCK) with strong cortical actin network, confined REF monolayers present an actin gradient with isotropic meshwork, suggesting the existence of a stiffness gradient. In addition, the REF cells tend to condense on soft substrates, a collective cell behavior we refer to as the ‘condensation tendency’. This condensation tendency, together with geometrical confinement, induces tensile prestretch (i.e. an isotropic stretch that causes tissue to contract when released) to the confined monolayer. By developing a Voronoi-cell model, we demonstrate that the combined global tissue prestretch and cell stiffness differential between the inner and boundary cells can sufficiently define the cell radial alignment at the pattern boundary.
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spelling pubmed-84784142021-09-30 Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers Xie, Tianfa St Pierre, Sarah R Olaranont, Nonthakorn Brown, Lauren E Wu, Min Sun, Yubing eLife Physics of Living Systems A monolayer of highly motile cells can establish long-range orientational order, which can be explained by hydrodynamic theory of active gels and fluids. However, it is less clear how cell shape changes and rearrangement are governed when the monolayer is in mechanical equilibrium states when cell motility diminishes. In this work, we report that rat embryonic fibroblasts (REF), when confined in circular mesoscale patterns on rigid substrates, can transition from the spindle shapes to more compact morphologies. Cells align radially only at the pattern boundary when they are in the mechanical equilibrium. This radial alignment disappears when cell contractility or cell-cell adhesion is reduced. Unlike monolayers of spindle-like cells such as NIH-3T3 fibroblasts with minimal intercellular interactions or epithelial cells like Madin-Darby canine kidney (MDCK) with strong cortical actin network, confined REF monolayers present an actin gradient with isotropic meshwork, suggesting the existence of a stiffness gradient. In addition, the REF cells tend to condense on soft substrates, a collective cell behavior we refer to as the ‘condensation tendency’. This condensation tendency, together with geometrical confinement, induces tensile prestretch (i.e. an isotropic stretch that causes tissue to contract when released) to the confined monolayer. By developing a Voronoi-cell model, we demonstrate that the combined global tissue prestretch and cell stiffness differential between the inner and boundary cells can sufficiently define the cell radial alignment at the pattern boundary. eLife Sciences Publications, Ltd 2021-09-20 /pmc/articles/PMC8478414/ /pubmed/34542405 http://dx.doi.org/10.7554/eLife.60381 Text en © 2021, Xie et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Physics of Living Systems
Xie, Tianfa
St Pierre, Sarah R
Olaranont, Nonthakorn
Brown, Lauren E
Wu, Min
Sun, Yubing
Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title_full Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title_fullStr Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title_full_unstemmed Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title_short Condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
title_sort condensation tendency and planar isotropic actin gradient induce radial alignment in confined monolayers
topic Physics of Living Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8478414/
https://www.ncbi.nlm.nih.gov/pubmed/34542405
http://dx.doi.org/10.7554/eLife.60381
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