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Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Tissue morphogenesis relies on the coordinated action of actin networks, cell–cell adhesions, and cell–extracellular matrix (ECM) adhesions. Such coordination can be achieved through cross-talk between cell–cell and cell–ECM adhesions. Drosophila dorsal closure (DC), a morphogenetic process in which...

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Autores principales: Goodwin, Katharine, Lostchuck, Emily E., Cramb, Kaitlyn M. L., Zulueta-Coarasa, Teresa, Fernandez-Gonzalez, Rodrigo, Tanentzapf, Guy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5426845/
https://www.ncbi.nlm.nih.gov/pubmed/28331071
http://dx.doi.org/10.1091/mbc.E17-01-0033
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author Goodwin, Katharine
Lostchuck, Emily E.
Cramb, Kaitlyn M. L.
Zulueta-Coarasa, Teresa
Fernandez-Gonzalez, Rodrigo
Tanentzapf, Guy
author_facet Goodwin, Katharine
Lostchuck, Emily E.
Cramb, Kaitlyn M. L.
Zulueta-Coarasa, Teresa
Fernandez-Gonzalez, Rodrigo
Tanentzapf, Guy
author_sort Goodwin, Katharine
collection PubMed
description Tissue morphogenesis relies on the coordinated action of actin networks, cell–cell adhesions, and cell–extracellular matrix (ECM) adhesions. Such coordination can be achieved through cross-talk between cell–cell and cell–ECM adhesions. Drosophila dorsal closure (DC), a morphogenetic process in which an extraembryonic tissue called the amnioserosa contracts and ingresses to close a discontinuity in the dorsal epidermis of the embryo, requires both cell–cell and cell–ECM adhesions. However, whether the functions of these two types of adhesions are coordinated during DC is not known. Here we analyzed possible interdependence between cell–cell and cell–ECM adhesions during DC and its effect on the actomyosin network. We find that loss of cell–ECM adhesion results in aberrant distributions of cadherin-mediated adhesions and actin networks in the amnioserosa and subsequent disruption of myosin recruitment and dynamics. Moreover, loss of cell–cell adhesion caused up-regulation of cell–ECM adhesion, leading to reduced cell deformation and force transmission across amnioserosa cells. Our results show how interdependence between cell–cell and cell–ECM adhesions is important in regulating cell behaviors, force generation, and force transmission critical for tissue morphogenesis.
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spelling pubmed-54268452017-07-30 Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure Goodwin, Katharine Lostchuck, Emily E. Cramb, Kaitlyn M. L. Zulueta-Coarasa, Teresa Fernandez-Gonzalez, Rodrigo Tanentzapf, Guy Mol Biol Cell Articles Tissue morphogenesis relies on the coordinated action of actin networks, cell–cell adhesions, and cell–extracellular matrix (ECM) adhesions. Such coordination can be achieved through cross-talk between cell–cell and cell–ECM adhesions. Drosophila dorsal closure (DC), a morphogenetic process in which an extraembryonic tissue called the amnioserosa contracts and ingresses to close a discontinuity in the dorsal epidermis of the embryo, requires both cell–cell and cell–ECM adhesions. However, whether the functions of these two types of adhesions are coordinated during DC is not known. Here we analyzed possible interdependence between cell–cell and cell–ECM adhesions during DC and its effect on the actomyosin network. We find that loss of cell–ECM adhesion results in aberrant distributions of cadherin-mediated adhesions and actin networks in the amnioserosa and subsequent disruption of myosin recruitment and dynamics. Moreover, loss of cell–cell adhesion caused up-regulation of cell–ECM adhesion, leading to reduced cell deformation and force transmission across amnioserosa cells. Our results show how interdependence between cell–cell and cell–ECM adhesions is important in regulating cell behaviors, force generation, and force transmission critical for tissue morphogenesis. The American Society for Cell Biology 2017-05-15 /pmc/articles/PMC5426845/ /pubmed/28331071 http://dx.doi.org/10.1091/mbc.E17-01-0033 Text en © 2017 Goodwin, Lostchuck, et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Goodwin, Katharine
Lostchuck, Emily E.
Cramb, Kaitlyn M. L.
Zulueta-Coarasa, Teresa
Fernandez-Gonzalez, Rodrigo
Tanentzapf, Guy
Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title_full Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title_fullStr Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title_full_unstemmed Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title_short Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
title_sort cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5426845/
https://www.ncbi.nlm.nih.gov/pubmed/28331071
http://dx.doi.org/10.1091/mbc.E17-01-0033
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