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Microtubules promote intercellular contractile force transmission during tissue folding

During development, forces transmitted between cells are critical for sculpting epithelial tissues. Actomyosin contractility in the middle of the cell apex (medioapical) can change cell shape (e.g., apical constriction) but can also result in force transmission between cells via attachments to adher...

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Detalles Bibliográficos
Autores principales: Ko, Clint S., Tserunyan, Vardges, Martin, Adam C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6683747/
https://www.ncbi.nlm.nih.gov/pubmed/31227595
http://dx.doi.org/10.1083/jcb.201902011
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author Ko, Clint S.
Tserunyan, Vardges
Martin, Adam C.
author_facet Ko, Clint S.
Tserunyan, Vardges
Martin, Adam C.
author_sort Ko, Clint S.
collection PubMed
description During development, forces transmitted between cells are critical for sculpting epithelial tissues. Actomyosin contractility in the middle of the cell apex (medioapical) can change cell shape (e.g., apical constriction) but can also result in force transmission between cells via attachments to adherens junctions. How actomyosin networks maintain attachments to adherens junctions under tension is poorly understood. Here, we discovered that microtubules promote actomyosin intercellular attachments in epithelia during Drosophila melanogaster mesoderm invagination. First, we used live imaging to show a novel arrangement of the microtubule cytoskeleton during apical constriction: medioapical Patronin (CAMSAP) foci formed by actomyosin contraction organized an apical noncentrosomal microtubule network. Microtubules were required for mesoderm invagination but were not necessary for initiating apical contractility or adherens junction assembly. Instead, microtubules promoted connections between medioapical actomyosin and adherens junctions. These results delineate a role for coordination between actin and microtubule cytoskeletal systems in intercellular force transmission during tissue morphogenesis.
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spelling pubmed-66837472020-02-05 Microtubules promote intercellular contractile force transmission during tissue folding Ko, Clint S. Tserunyan, Vardges Martin, Adam C. J Cell Biol Research Articles During development, forces transmitted between cells are critical for sculpting epithelial tissues. Actomyosin contractility in the middle of the cell apex (medioapical) can change cell shape (e.g., apical constriction) but can also result in force transmission between cells via attachments to adherens junctions. How actomyosin networks maintain attachments to adherens junctions under tension is poorly understood. Here, we discovered that microtubules promote actomyosin intercellular attachments in epithelia during Drosophila melanogaster mesoderm invagination. First, we used live imaging to show a novel arrangement of the microtubule cytoskeleton during apical constriction: medioapical Patronin (CAMSAP) foci formed by actomyosin contraction organized an apical noncentrosomal microtubule network. Microtubules were required for mesoderm invagination but were not necessary for initiating apical contractility or adherens junction assembly. Instead, microtubules promoted connections between medioapical actomyosin and adherens junctions. These results delineate a role for coordination between actin and microtubule cytoskeletal systems in intercellular force transmission during tissue morphogenesis. Rockefeller University Press 2019-08-05 2019-06-21 /pmc/articles/PMC6683747/ /pubmed/31227595 http://dx.doi.org/10.1083/jcb.201902011 Text en © 2019 Ko et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
Ko, Clint S.
Tserunyan, Vardges
Martin, Adam C.
Microtubules promote intercellular contractile force transmission during tissue folding
title Microtubules promote intercellular contractile force transmission during tissue folding
title_full Microtubules promote intercellular contractile force transmission during tissue folding
title_fullStr Microtubules promote intercellular contractile force transmission during tissue folding
title_full_unstemmed Microtubules promote intercellular contractile force transmission during tissue folding
title_short Microtubules promote intercellular contractile force transmission during tissue folding
title_sort microtubules promote intercellular contractile force transmission during tissue folding
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6683747/
https://www.ncbi.nlm.nih.gov/pubmed/31227595
http://dx.doi.org/10.1083/jcb.201902011
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