Vinculin phosphorylation differentially regulates mechanotransduction at cell–cell and cell–matrix adhesions

Jennifer L. Bays; Catlin E. Tolbert; Christophe Guilluy; Ashley E. Angell; Yuan Pan; Richard Superfine; Keith Burridge; Kris A. DeMali

doi:10.1083/jcb.201309092

journal article Apr 21, 2014

Vinculin phosphorylation differentially regulates mechanotransduction at cell–cell and cell–matrix adhesions

Jennifer L. Bays Catlin E. Tolbert Christophe Guilluy Ashley E. Angell Yuan Pan

Richard Superfine Keith Burridge Kris A. DeMali

Journal of Cell Biology Vol. 205 No. 2 pp. 251-263 · Rockefeller University Press

View at Publisher Save 10.1083/jcb.201309092

Abstract

Cells experience mechanical forces throughout their lifetimes. Vinculin is critical for transmitting these forces, yet how it achieves its distinct functions at cell–cell and cell–matrix adhesions remains unanswered. Here, we show vinculin is phosphorylated at Y822 in cell–cell, but not cell–matrix, adhesions. Phosphorylation at Y822 was elevated when forces were applied to E-cadherin and was required for vinculin to integrate into the cadherin complex. The mutation Y822F ablated these activities and prevented cells from stiffening in response to forces on E-cadherin. In contrast, Y822 phosphorylation was not required for vinculin functions in cell–matrix adhesions, including integrin-induced cell stiffening. Finally, forces applied to E-cadherin activated Abelson (Abl) tyrosine kinase to phosphorylate vinculin; Abl inhibition mimicked the loss of vinculin phosphorylation. These data reveal an unexpected regulatory mechanism in which vinculin Y822 phosphorylation determines whether cadherins transmit force and provides a paradigm for how a shared component of adhesions can produce biologically distinct functions.

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Details

Published: Apr 21, 2014
Vol/Issue: 205(2)
Pages: 251-263

Authors

J

Jennifer L. Bays

Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 1

C

Catlin E. Tolbert

Departments of Cell Biology 2 and 3; Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 2 and 3

C

Christophe Guilluy

Departments of Cell Biology 2 and 3; Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 2 and 3

A

Ashley E. Angell

Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 1

Y

Yuan Pan

Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 1

R

Richard Superfine

Departments of Cell Biology 2 and 3; Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 2 and 3

K

Keith Burridge

Departments of Cell Biology 2 and 3; Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 2 and 3

K

Kris A. DeMali

Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 1

Cite This Article

Jennifer L. Bays, Catlin E. Tolbert, Christophe Guilluy, et al. (2014). Vinculin phosphorylation differentially regulates mechanotransduction at cell–cell and cell–matrix adhesions. Journal of Cell Biology, 205(2), 251-263. https://doi.org/10.1083/jcb.201309092

Vinculin phosphorylation differentially regulates mechanotransduction at cell–cell and cell–matrix adhesions

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