Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration

A key regulator of collective cell migrations, which drive development and cancer metastasis, is substrate stiffness. Increased substrate stiffness promotes migration and is controlled by Myosin. Using Drosophila border cell migration as a model of collective cell migration, we identify, for the fir...

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Autores principales:	Maureen C Lamb, Chathuri P Kaluarachchi, Thiranjeewa I Lansakara, Samuel Q Mellentine, Yiling Lan, Alexei V Tivanski, Tina L Tootle
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	Fascin collective cell migration myosin stiffness border cells mechanotransduction Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/710d2b662d4c4d41bf665362766d6c6e
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spelling	oai:doaj.org-article:710d2b662d4c4d41bf665362766d6c6e2021-11-30T10:04:09ZFascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration10.7554/eLife.698362050-084Xe69836https://doaj.org/article/710d2b662d4c4d41bf665362766d6c6e2021-10-01T00:00:00Zhttps://elifesciences.org/articles/69836https://doaj.org/toc/2050-084XA key regulator of collective cell migrations, which drive development and cancer metastasis, is substrate stiffness. Increased substrate stiffness promotes migration and is controlled by Myosin. Using Drosophila border cell migration as a model of collective cell migration, we identify, for the first time, that the actin bundling protein Fascin limits Myosin activity in vivo. Loss of Fascin results in: increased activated Myosin on the border cells and their substrate, the nurse cells; decreased border cell Myosin dynamics; and increased nurse cell stiffness as measured by atomic force microscopy. Reducing Myosin restores on-time border cell migration in fascin mutant follicles. Further, Fascin’s actin bundling activity is required to limit Myosin activation. Surprisingly, we find that Fascin regulates Myosin activity in the border cells to control nurse cell stiffness to promote migration. Thus, these data shift the paradigm from a substrate stiffness-centric model of regulating migration, to uncover that collectively migrating cells play a critical role in controlling the mechanical properties of their substrate in order to promote their own migration. This understudied means of mechanical regulation of migration is likely conserved across contexts and organisms, as Fascin and Myosin are common regulators of cell migration.Maureen C LambChathuri P KaluarachchiThiranjeewa I LansakaraSamuel Q MellentineYiling LanAlexei V TivanskiTina L TootleeLife Sciences Publications LtdarticleFascincollective cell migrationmyosinstiffnessborder cellsmechanotransductionMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Fascin collective cell migration myosin stiffness border cells mechanotransduction Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	Fascin collective cell migration myosin stiffness border cells mechanotransduction Medicine R Science Q Biology (General) QH301-705.5 Maureen C Lamb Chathuri P Kaluarachchi Thiranjeewa I Lansakara Samuel Q Mellentine Yiling Lan Alexei V Tivanski Tina L Tootle Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
description	A key regulator of collective cell migrations, which drive development and cancer metastasis, is substrate stiffness. Increased substrate stiffness promotes migration and is controlled by Myosin. Using Drosophila border cell migration as a model of collective cell migration, we identify, for the first time, that the actin bundling protein Fascin limits Myosin activity in vivo. Loss of Fascin results in: increased activated Myosin on the border cells and their substrate, the nurse cells; decreased border cell Myosin dynamics; and increased nurse cell stiffness as measured by atomic force microscopy. Reducing Myosin restores on-time border cell migration in fascin mutant follicles. Further, Fascin’s actin bundling activity is required to limit Myosin activation. Surprisingly, we find that Fascin regulates Myosin activity in the border cells to control nurse cell stiffness to promote migration. Thus, these data shift the paradigm from a substrate stiffness-centric model of regulating migration, to uncover that collectively migrating cells play a critical role in controlling the mechanical properties of their substrate in order to promote their own migration. This understudied means of mechanical regulation of migration is likely conserved across contexts and organisms, as Fascin and Myosin are common regulators of cell migration.
format	article
author	Maureen C Lamb Chathuri P Kaluarachchi Thiranjeewa I Lansakara Samuel Q Mellentine Yiling Lan Alexei V Tivanski Tina L Tootle
author_facet	Maureen C Lamb Chathuri P Kaluarachchi Thiranjeewa I Lansakara Samuel Q Mellentine Yiling Lan Alexei V Tivanski Tina L Tootle
author_sort	Maureen C Lamb
title	Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
title_short	Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
title_full	Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
title_fullStr	Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
title_full_unstemmed	Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration
title_sort	fascin limits myosin activity within drosophila border cells to control substrate stiffness and promote migration
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/710d2b662d4c4d41bf665362766d6c6e
work_keys_str_mv	AT maureenclamb fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT chathuripkaluarachchi fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT thiranjeewailansakara fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT samuelqmellentine fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT yilinglan fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT alexeivtivanski fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration AT tinaltootle fascinlimitsmyosinactivitywithindrosophilabordercellstocontrolsubstratestiffnessandpromotemigration
_version_	1718406690025504768

Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration

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