Cargando…

Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue

Migrating cells need to overcome physical constraints from the local microenvironment to navigate their way through tissues. Cells that move collectively have the additional challenge of negotiating complex environments in vivo while maintaining cohesion of the group as a whole. The mechanisms by wh...

Descripción completa

Detalles Bibliográficos
Autores principales: Aranjuez, George, Burtscher, Ashley, Sawant, Ketki, Majumder, Pralay, McDonald, Jocelyn A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4907723/
https://www.ncbi.nlm.nih.gov/pubmed/27122602
http://dx.doi.org/10.1091/mbc.E15-10-0744
_version_ 1782437586357190656
author Aranjuez, George
Burtscher, Ashley
Sawant, Ketki
Majumder, Pralay
McDonald, Jocelyn A.
author_facet Aranjuez, George
Burtscher, Ashley
Sawant, Ketki
Majumder, Pralay
McDonald, Jocelyn A.
author_sort Aranjuez, George
collection PubMed
description Migrating cells need to overcome physical constraints from the local microenvironment to navigate their way through tissues. Cells that move collectively have the additional challenge of negotiating complex environments in vivo while maintaining cohesion of the group as a whole. The mechanisms by which collectives maintain a migratory morphology while resisting physical constraints from the surrounding tissue are poorly understood. Drosophila border cells represent a genetic model of collective migration within a cell-dense tissue. Border cells move as a cohesive group of 6−10 cells, traversing a network of large germ line–derived nurse cells within the ovary. Here we show that the border cell cluster is compact and round throughout their entire migration, a shape that is maintained despite the mechanical pressure imposed by the surrounding nurse cells. Nonmuscle myosin II (Myo-II) activity at the cluster periphery becomes elevated in response to increased constriction by nurse cells. Furthermore, the distinctive border cell collective morphology requires highly dynamic and localized enrichment of Myo-II. Thus, activated Myo-II promotes cortical tension at the outer edge of the migrating border cell cluster to resist compressive forces from nurse cells. We propose that dynamic actomyosin tension at the periphery of collectives facilitates their movement through restrictive tissues.
format Online
Article
Text
id pubmed-4907723
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher The American Society for Cell Biology
record_format MEDLINE/PubMed
spelling pubmed-49077232016-08-30 Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue Aranjuez, George Burtscher, Ashley Sawant, Ketki Majumder, Pralay McDonald, Jocelyn A. Mol Biol Cell Articles Migrating cells need to overcome physical constraints from the local microenvironment to navigate their way through tissues. Cells that move collectively have the additional challenge of negotiating complex environments in vivo while maintaining cohesion of the group as a whole. The mechanisms by which collectives maintain a migratory morphology while resisting physical constraints from the surrounding tissue are poorly understood. Drosophila border cells represent a genetic model of collective migration within a cell-dense tissue. Border cells move as a cohesive group of 6−10 cells, traversing a network of large germ line–derived nurse cells within the ovary. Here we show that the border cell cluster is compact and round throughout their entire migration, a shape that is maintained despite the mechanical pressure imposed by the surrounding nurse cells. Nonmuscle myosin II (Myo-II) activity at the cluster periphery becomes elevated in response to increased constriction by nurse cells. Furthermore, the distinctive border cell collective morphology requires highly dynamic and localized enrichment of Myo-II. Thus, activated Myo-II promotes cortical tension at the outer edge of the migrating border cell cluster to resist compressive forces from nurse cells. We propose that dynamic actomyosin tension at the periphery of collectives facilitates their movement through restrictive tissues. The American Society for Cell Biology 2016-06-15 /pmc/articles/PMC4907723/ /pubmed/27122602 http://dx.doi.org/10.1091/mbc.E15-10-0744 Text en © 2016 Aranjuez 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
Aranjuez, George
Burtscher, Ashley
Sawant, Ketki
Majumder, Pralay
McDonald, Jocelyn A.
Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title_full Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title_fullStr Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title_full_unstemmed Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title_short Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
title_sort dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4907723/
https://www.ncbi.nlm.nih.gov/pubmed/27122602
http://dx.doi.org/10.1091/mbc.E15-10-0744
work_keys_str_mv AT aranjuezgeorge dynamicmyosinactivationpromotescollectivemorphologyandmigrationbylocallybalancingoppositionalforcesfromsurroundingtissue
AT burtscherashley dynamicmyosinactivationpromotescollectivemorphologyandmigrationbylocallybalancingoppositionalforcesfromsurroundingtissue
AT sawantketki dynamicmyosinactivationpromotescollectivemorphologyandmigrationbylocallybalancingoppositionalforcesfromsurroundingtissue
AT majumderpralay dynamicmyosinactivationpromotescollectivemorphologyandmigrationbylocallybalancingoppositionalforcesfromsurroundingtissue
AT mcdonaldjocelyna dynamicmyosinactivationpromotescollectivemorphologyandmigrationbylocallybalancingoppositionalforcesfromsurroundingtissue