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Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex

Epithelial monolayers are one-cell thick tissue sheets that line most of the body surfaces, separating internal and external environments. As part of their function, they must withstand extrinsic mechanical stresses applied at high strain rates. However, little is known about how monolayers respond...

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Autores principales: Khalilgharibi, Nargess, Fouchard, Jonathan, Asadipour, Nina, Barrientos, Ricardo, Duda, Maria, Bonfanti, Alessandra, Yonis, Amina, Harris, Andrew, Mosaffa, Payman, Fujita, Yasuyuki, Kabla, Alexandre, Mao, Yanlan, Baum, Buzz, Muñoz, José J, Miodownik, Mark, Charras, Guillaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7116713/
https://www.ncbi.nlm.nih.gov/pubmed/33569083
http://dx.doi.org/10.1038/s41567-019-0516-6
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author Khalilgharibi, Nargess
Fouchard, Jonathan
Asadipour, Nina
Barrientos, Ricardo
Duda, Maria
Bonfanti, Alessandra
Yonis, Amina
Harris, Andrew
Mosaffa, Payman
Fujita, Yasuyuki
Kabla, Alexandre
Mao, Yanlan
Baum, Buzz
Muñoz, José J
Miodownik, Mark
Charras, Guillaume
author_facet Khalilgharibi, Nargess
Fouchard, Jonathan
Asadipour, Nina
Barrientos, Ricardo
Duda, Maria
Bonfanti, Alessandra
Yonis, Amina
Harris, Andrew
Mosaffa, Payman
Fujita, Yasuyuki
Kabla, Alexandre
Mao, Yanlan
Baum, Buzz
Muñoz, José J
Miodownik, Mark
Charras, Guillaume
author_sort Khalilgharibi, Nargess
collection PubMed
description Epithelial monolayers are one-cell thick tissue sheets that line most of the body surfaces, separating internal and external environments. As part of their function, they must withstand extrinsic mechanical stresses applied at high strain rates. However, little is known about how monolayers respond to mechanical deformations. Here, by subjecting suspended epithelial monolayers to stretch, we find that they dissipate stresses on a minute timescale and that relaxation can be described by a power law with an exponential cut-off at timescales larger than ~10 s. This process involves an increase in monolayer length, pointing to active remodelling of cellular biopolymers at the molecular scale during relaxation. Strikingly, monolayers consisting of tens of thousands of cells relax stress with similar dynamics to single rounded cells and both respond similarly to perturbations of the actomyosin cytoskeleton. By contrast, cell-cell junctional complexes and intermediate filaments do not relax tissue stress, but form stable connections between cells, allowing monolayers to behave rheologically as single cells. Taken together our data show that actomyosin dynamics governs the rheological properties of epithelial monolayers, dissipating applied stresses, and enabling changes in monolayer length.
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spelling pubmed-71167132021-02-09 Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex Khalilgharibi, Nargess Fouchard, Jonathan Asadipour, Nina Barrientos, Ricardo Duda, Maria Bonfanti, Alessandra Yonis, Amina Harris, Andrew Mosaffa, Payman Fujita, Yasuyuki Kabla, Alexandre Mao, Yanlan Baum, Buzz Muñoz, José J Miodownik, Mark Charras, Guillaume Nat Phys Article Epithelial monolayers are one-cell thick tissue sheets that line most of the body surfaces, separating internal and external environments. As part of their function, they must withstand extrinsic mechanical stresses applied at high strain rates. However, little is known about how monolayers respond to mechanical deformations. Here, by subjecting suspended epithelial monolayers to stretch, we find that they dissipate stresses on a minute timescale and that relaxation can be described by a power law with an exponential cut-off at timescales larger than ~10 s. This process involves an increase in monolayer length, pointing to active remodelling of cellular biopolymers at the molecular scale during relaxation. Strikingly, monolayers consisting of tens of thousands of cells relax stress with similar dynamics to single rounded cells and both respond similarly to perturbations of the actomyosin cytoskeleton. By contrast, cell-cell junctional complexes and intermediate filaments do not relax tissue stress, but form stable connections between cells, allowing monolayers to behave rheologically as single cells. Taken together our data show that actomyosin dynamics governs the rheological properties of epithelial monolayers, dissipating applied stresses, and enabling changes in monolayer length. 2019-08 2019-05-13 /pmc/articles/PMC7116713/ /pubmed/33569083 http://dx.doi.org/10.1038/s41567-019-0516-6 Text en http://www.nature.com/authors/editorial_policies/license.html#terms Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Khalilgharibi, Nargess
Fouchard, Jonathan
Asadipour, Nina
Barrientos, Ricardo
Duda, Maria
Bonfanti, Alessandra
Yonis, Amina
Harris, Andrew
Mosaffa, Payman
Fujita, Yasuyuki
Kabla, Alexandre
Mao, Yanlan
Baum, Buzz
Muñoz, José J
Miodownik, Mark
Charras, Guillaume
Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title_full Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title_fullStr Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title_full_unstemmed Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title_short Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
title_sort stress relaxation in epithelial monolayers is controlled by the actomyosin cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7116713/
https://www.ncbi.nlm.nih.gov/pubmed/33569083
http://dx.doi.org/10.1038/s41567-019-0516-6
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