Fascin Regulates Nuclear Movement and Deformation in Migrating Cells

Asier Jayo; Majid Malboubi; Susumu Antoku; Wakam Chang; Elena Ortiz-Zapater; Christopher Groen; Karin Pfisterer; Tina Tootle; Guillaume Charras; Gregg G. Gundersen; Maddy Parsons

doi:10.1016/j.devcel.2016.07.021

Fascin Regulates Nuclear Movement and Deformation in Migrating Cells

Asier Jayo, Majid Malboubi, Susumu Antoku, Wakam Chang, Elena Ortiz-Zapater, Christopher Groen, Karin Pfisterer, Tina Tootle, Guillaume Charras, Gregg G. Gundersen, Maddy Parsons

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Abstract

Summary Fascin is an F-actin-bundling protein shown to stabilize filopodia and regulate adhesion dynamics in migrating cells, and its expression is correlated with poor prognosis and increased metastatic potential in a number of cancers. Here, we identified the nuclear envelope protein nesprin-2 as a binding partner for fascin in a range of cell types in vitro and in vivo. Nesprin-2 interacts with fascin through a direct, F-actin-independent interaction, and this binding is distinct and separable from a role for fascin within filopodia at the cell periphery. Moreover, disrupting the interaction between fascin and nesprin-2 C-terminal domain leads to specific defects in F-actin coupling to the nuclear envelope, nuclear movement, and the ability of cells to deform their nucleus to invade through confined spaces. Together, our results uncover a role for fascin that operates independently of filopodia assembly to promote efficient cell migration and invasion.

Original language	English
Pages (from-to)	371-383
Number of pages	13
Journal	Developmental Cell
Volume	38
Issue number	4
Early online date	22 Aug 2016
DOIs	https://doi.org/10.1016/j.devcel.2016.07.021
Publication status	Published - 22 Aug 2016

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Fascin Regulates Nuclear Movement_JAYO_Accepted25July2016_GOLD VoRFinal published version, 4.11 MBLicence: CC BY-NC-ND

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title = "Fascin Regulates Nuclear Movement and Deformation in Migrating Cells",

abstract = "Summary Fascin is an F-actin-bundling protein shown to stabilize filopodia and regulate adhesion dynamics in migrating cells, and its expression is correlated with poor prognosis and increased metastatic potential in a number of cancers. Here, we identified the nuclear envelope protein nesprin-2 as a binding partner for fascin in a range of cell types in vitro and in vivo. Nesprin-2 interacts with fascin through a direct, F-actin-independent interaction, and this binding is distinct and separable from a role for fascin within filopodia at the cell periphery. Moreover, disrupting the interaction between fascin and nesprin-2 C-terminal domain leads to specific defects in F-actin coupling to the nuclear envelope, nuclear movement, and the ability of cells to deform their nucleus to invade through confined spaces. Together, our results uncover a role for fascin that operates independently of filopodia assembly to promote efficient cell migration and invasion.",

author = "Asier Jayo and Majid Malboubi and Susumu Antoku and Wakam Chang and Elena Ortiz-Zapater and Christopher Groen and Karin Pfisterer and Tina Tootle and Guillaume Charras and Gregg G. Gundersen and Maddy Parsons",

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T1 - Fascin Regulates Nuclear Movement and Deformation in Migrating Cells

AU - Jayo, Asier

AU - Malboubi, Majid

AU - Antoku, Susumu

AU - Chang, Wakam

AU - Ortiz-Zapater, Elena

AU - Groen, Christopher

AU - Pfisterer, Karin

AU - Tootle, Tina

AU - Charras, Guillaume

AU - Gundersen, Gregg G.

AU - Parsons, Maddy

PY - 2016/8/22

Y1 - 2016/8/22

N2 - Summary Fascin is an F-actin-bundling protein shown to stabilize filopodia and regulate adhesion dynamics in migrating cells, and its expression is correlated with poor prognosis and increased metastatic potential in a number of cancers. Here, we identified the nuclear envelope protein nesprin-2 as a binding partner for fascin in a range of cell types in vitro and in vivo. Nesprin-2 interacts with fascin through a direct, F-actin-independent interaction, and this binding is distinct and separable from a role for fascin within filopodia at the cell periphery. Moreover, disrupting the interaction between fascin and nesprin-2 C-terminal domain leads to specific defects in F-actin coupling to the nuclear envelope, nuclear movement, and the ability of cells to deform their nucleus to invade through confined spaces. Together, our results uncover a role for fascin that operates independently of filopodia assembly to promote efficient cell migration and invasion.

AB - Summary Fascin is an F-actin-bundling protein shown to stabilize filopodia and regulate adhesion dynamics in migrating cells, and its expression is correlated with poor prognosis and increased metastatic potential in a number of cancers. Here, we identified the nuclear envelope protein nesprin-2 as a binding partner for fascin in a range of cell types in vitro and in vivo. Nesprin-2 interacts with fascin through a direct, F-actin-independent interaction, and this binding is distinct and separable from a role for fascin within filopodia at the cell periphery. Moreover, disrupting the interaction between fascin and nesprin-2 C-terminal domain leads to specific defects in F-actin coupling to the nuclear envelope, nuclear movement, and the ability of cells to deform their nucleus to invade through confined spaces. Together, our results uncover a role for fascin that operates independently of filopodia assembly to promote efficient cell migration and invasion.

U2 - 10.1016/j.devcel.2016.07.021

DO - 10.1016/j.devcel.2016.07.021

M3 - Article

SN - 1534-5807

VL - 38

SP - 371

EP - 383

JO - Developmental Cell

JF - Developmental Cell

IS - 4

ER -

Fascin Regulates Nuclear Movement and Deformation in Migrating Cells

Abstract

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