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Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers

Adherens junctions and desmosomes integrate the cytoskeletons of adjacent cells into a mechanical syncitium. In doing so, intercellular junctions endow tissues with the strength needed to withstand the mechanical stresses encountered in normal physiology and to coordinate tension during morphogenesi...

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Autores principales: Harris, Andrew R., Daeden, Alicia, Charras, Guillaume T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4043320/
https://www.ncbi.nlm.nih.gov/pubmed/24659804
http://dx.doi.org/10.1242/jcs.142349
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author Harris, Andrew R.
Daeden, Alicia
Charras, Guillaume T.
author_facet Harris, Andrew R.
Daeden, Alicia
Charras, Guillaume T.
author_sort Harris, Andrew R.
collection PubMed
description Adherens junctions and desmosomes integrate the cytoskeletons of adjacent cells into a mechanical syncitium. In doing so, intercellular junctions endow tissues with the strength needed to withstand the mechanical stresses encountered in normal physiology and to coordinate tension during morphogenesis. Though much is known about the biological mechanisms underlying junction formation, little is known about how tissue-scale mechanical properties are established. Here, we use deep atomic force microscopy (AFM) indentation to measure the apparent stiffness of epithelial monolayers reforming from dissociated cells and examine which cellular processes give rise to tissue-scale mechanics. We show that the formation of intercellular junctions coincided with an increase in the apparent stiffness of reforming monolayers that reflected the generation of a tissue-level tension. Tension rapidly increased, reaching a maximum after 150 min, before settling to a lower level over the next 3 h as monolayers established homeostasis. The emergence of tissue tension correlated with the formation of adherens junctions but not desmosomes. As a consequence, inhibition of any of the molecular mechanisms participating in adherens junction initiation, remodelling and maturation significantly impeded the emergence of tissue-level tension in monolayers.
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spelling pubmed-40433202014-06-12 Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers Harris, Andrew R. Daeden, Alicia Charras, Guillaume T. J Cell Sci Research Article Adherens junctions and desmosomes integrate the cytoskeletons of adjacent cells into a mechanical syncitium. In doing so, intercellular junctions endow tissues with the strength needed to withstand the mechanical stresses encountered in normal physiology and to coordinate tension during morphogenesis. Though much is known about the biological mechanisms underlying junction formation, little is known about how tissue-scale mechanical properties are established. Here, we use deep atomic force microscopy (AFM) indentation to measure the apparent stiffness of epithelial monolayers reforming from dissociated cells and examine which cellular processes give rise to tissue-scale mechanics. We show that the formation of intercellular junctions coincided with an increase in the apparent stiffness of reforming monolayers that reflected the generation of a tissue-level tension. Tension rapidly increased, reaching a maximum after 150 min, before settling to a lower level over the next 3 h as monolayers established homeostasis. The emergence of tissue tension correlated with the formation of adherens junctions but not desmosomes. As a consequence, inhibition of any of the molecular mechanisms participating in adherens junction initiation, remodelling and maturation significantly impeded the emergence of tissue-level tension in monolayers. The Company of Biologists 2014-06-01 /pmc/articles/PMC4043320/ /pubmed/24659804 http://dx.doi.org/10.1242/jcs.142349 Text en © 2014. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Harris, Andrew R.
Daeden, Alicia
Charras, Guillaume T.
Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title_full Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title_fullStr Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title_full_unstemmed Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title_short Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
title_sort formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4043320/
https://www.ncbi.nlm.nih.gov/pubmed/24659804
http://dx.doi.org/10.1242/jcs.142349
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