DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila

Stress fibers (SFs) are actomyosin bundles commonly found in individually migrating cells in culture. However, whether and how cells use SFs to migrate in vivo or collectively is largely unknown. Studying the collective migration of the follicular epithelial cells in Drosophila, we found that the SF...

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Autores principales:	Kristin M Sherrard, Maureen Cetera, Sally Horne-Badovinac
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	stress fiber focal adhesion collective cell migration epithelium treadmilling Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/581486f5da9f4e0187b8693014584601
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spelling	oai:doaj.org-article:581486f5da9f4e0187b86930145846012021-11-24T12:10:43ZDAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila10.7554/eLife.728812050-084Xe72881https://doaj.org/article/581486f5da9f4e0187b86930145846012021-11-01T00:00:00Zhttps://elifesciences.org/articles/72881https://doaj.org/toc/2050-084XStress fibers (SFs) are actomyosin bundles commonly found in individually migrating cells in culture. However, whether and how cells use SFs to migrate in vivo or collectively is largely unknown. Studying the collective migration of the follicular epithelial cells in Drosophila, we found that the SFs in these cells show a novel treadmilling behavior that allows them to persist as the cells migrate over multiple cell lengths. Treadmilling SFs grow at their fronts by adding new integrin-based adhesions and actomyosin segments over time. This causes the SFs to have many internal adhesions along their lengths, instead of adhesions only at the ends. The front-forming adhesions remain stationary relative to the substrate and typically disassemble as the cell rear approaches. By contrast, a different type of adhesion forms at the SF’s terminus that slides with the cell’s trailing edge as the actomyosin ahead of it shortens. We further show that SF treadmilling depends on cell movement and identify a developmental switch in the formins that mediate SF assembly, with Dishevelled-associated activator of morphogenesis acting during migratory stages and Diaphanous acting during postmigratory stages. We propose that treadmilling SFs keep each cell on a linear trajectory, thereby promoting the collective motility required for epithelial migration.Kristin M SherrardMaureen CeteraSally Horne-BadovinaceLife Sciences Publications Ltdarticlestress fiberfocal adhesioncollective cell migrationepitheliumtreadmillingMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	stress fiber focal adhesion collective cell migration epithelium treadmilling Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	stress fiber focal adhesion collective cell migration epithelium treadmilling Medicine R Science Q Biology (General) QH301-705.5 Kristin M Sherrard Maureen Cetera Sally Horne-Badovinac DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
description	Stress fibers (SFs) are actomyosin bundles commonly found in individually migrating cells in culture. However, whether and how cells use SFs to migrate in vivo or collectively is largely unknown. Studying the collective migration of the follicular epithelial cells in Drosophila, we found that the SFs in these cells show a novel treadmilling behavior that allows them to persist as the cells migrate over multiple cell lengths. Treadmilling SFs grow at their fronts by adding new integrin-based adhesions and actomyosin segments over time. This causes the SFs to have many internal adhesions along their lengths, instead of adhesions only at the ends. The front-forming adhesions remain stationary relative to the substrate and typically disassemble as the cell rear approaches. By contrast, a different type of adhesion forms at the SF’s terminus that slides with the cell’s trailing edge as the actomyosin ahead of it shortens. We further show that SF treadmilling depends on cell movement and identify a developmental switch in the formins that mediate SF assembly, with Dishevelled-associated activator of morphogenesis acting during migratory stages and Diaphanous acting during postmigratory stages. We propose that treadmilling SFs keep each cell on a linear trajectory, thereby promoting the collective motility required for epithelial migration.
format	article
author	Kristin M Sherrard Maureen Cetera Sally Horne-Badovinac
author_facet	Kristin M Sherrard Maureen Cetera Sally Horne-Badovinac
author_sort	Kristin M Sherrard
title	DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
title_short	DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
title_full	DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
title_fullStr	DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
title_full_unstemmed	DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila
title_sort	daam mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in drosophila
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/581486f5da9f4e0187b8693014584601
work_keys_str_mv	AT kristinmsherrard daammediatestheassemblyoflonglivedtreadmillingstressfibersincollectivelymigratingepithelialcellsindrosophila AT maureencetera daammediatestheassemblyoflonglivedtreadmillingstressfibersincollectivelymigratingepithelialcellsindrosophila AT sallyhornebadovinac daammediatestheassemblyoflonglivedtreadmillingstressfibersincollectivelymigratingepithelialcellsindrosophila
_version_	1718415046592167936

DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila

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