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Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II

Collective cell migration is emerging as a major driver of embryonic development, organogenesis, tissue homeostasis, and tumor dissemination. In contrast to individually migrating cells, collectively migrating cells maintain cell–cell adhesions and coordinate direction-sensing as they move. While no...

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Autores principales: Mishra, Abhinava K., Mondo, James A., Campanale, Joseph P., Montell, Denise J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743363/
https://www.ncbi.nlm.nih.gov/pubmed/31390285
http://dx.doi.org/10.1091/mbc.E19-02-0124
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author Mishra, Abhinava K.
Mondo, James A.
Campanale, Joseph P.
Montell, Denise J.
author_facet Mishra, Abhinava K.
Mondo, James A.
Campanale, Joseph P.
Montell, Denise J.
author_sort Mishra, Abhinava K.
collection PubMed
description Collective cell migration is emerging as a major driver of embryonic development, organogenesis, tissue homeostasis, and tumor dissemination. In contrast to individually migrating cells, collectively migrating cells maintain cell–cell adhesions and coordinate direction-sensing as they move. While nonmuscle myosin II has been studied extensively in the context of cells migrating individually in vitro, its roles in cells migrating collectively in three-dimensional, native environments are not fully understood. Here we use genetics, Airyscan microscopy, live imaging, optogenetics, and Förster resonance energy transfer to probe the localization, dynamics, and functions of myosin II in migrating border cells of the Drosophila ovary. We find that myosin accumulates transiently at the base of protrusions, where it functions to retract them. E-cadherin and myosin colocalize at border cell-border cell contacts and cooperate to transmit directional information. A phosphomimetic form of myosin is sufficient to convert border cells to a round morphology and blebbing migration mode. Together these studies demonstrate that distinct and dynamic pools of myosin II regulate protrusion dynamics within and between collectively migrating cells and suggest a new model for the role of protrusions in collective direction sensing in vivo.
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spelling pubmed-67433632019-11-16 Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II Mishra, Abhinava K. Mondo, James A. Campanale, Joseph P. Montell, Denise J. Mol Biol Cell Articles Collective cell migration is emerging as a major driver of embryonic development, organogenesis, tissue homeostasis, and tumor dissemination. In contrast to individually migrating cells, collectively migrating cells maintain cell–cell adhesions and coordinate direction-sensing as they move. While nonmuscle myosin II has been studied extensively in the context of cells migrating individually in vitro, its roles in cells migrating collectively in three-dimensional, native environments are not fully understood. Here we use genetics, Airyscan microscopy, live imaging, optogenetics, and Förster resonance energy transfer to probe the localization, dynamics, and functions of myosin II in migrating border cells of the Drosophila ovary. We find that myosin accumulates transiently at the base of protrusions, where it functions to retract them. E-cadherin and myosin colocalize at border cell-border cell contacts and cooperate to transmit directional information. A phosphomimetic form of myosin is sufficient to convert border cells to a round morphology and blebbing migration mode. Together these studies demonstrate that distinct and dynamic pools of myosin II regulate protrusion dynamics within and between collectively migrating cells and suggest a new model for the role of protrusions in collective direction sensing in vivo. The American Society for Cell Biology 2019-09-01 /pmc/articles/PMC6743363/ /pubmed/31390285 http://dx.doi.org/10.1091/mbc.E19-02-0124 Text en © 2019 Mishra et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 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.
spellingShingle Articles
Mishra, Abhinava K.
Mondo, James A.
Campanale, Joseph P.
Montell, Denise J.
Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title_full Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title_fullStr Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title_full_unstemmed Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title_short Coordination of protrusion dynamics within and between collectively migrating border cells by myosin II
title_sort coordination of protrusion dynamics within and between collectively migrating border cells by myosin ii
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743363/
https://www.ncbi.nlm.nih.gov/pubmed/31390285
http://dx.doi.org/10.1091/mbc.E19-02-0124
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