Vinculin phosphorylation differentially regulates mechanotransduction at cell-cell and cell-matrix adhesions
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,...
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| Published in | The Journal of cell biology Vol. 205; no. 2; pp. 251 - 263 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
28.04.2014
The Rockefeller University Press |
| Subjects | |
| Online Access | Get full text |
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| 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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| AbstractList | 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. Vinculin phosphorylation on residue Y822 is necessary for cell stiffening in response to tension on cadherins but not integrins. 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. 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. [PUBLICATION ABSTRACT] |
| Author | Guilluy, Christophe Superfine, Richard Angell, Ashley E DeMali, Kris A Peng, Xiao Tolbert, Catlin E Bays, Jennifer L Pan, Yuan Burridge, Keith |
| AuthorAffiliation | 1 Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 2 Departments of Cell Biology and 3 Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 |
| AuthorAffiliation_xml | – name: 2 Departments of Cell Biology and 3 Physiology and Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599 – name: 1 Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 |
| Author_xml | – sequence: 1 givenname: Jennifer L surname: Bays fullname: Bays, Jennifer L organization: Department of Biochemistry, University of Iowa Roy J. Carver College of Medicine, Iowa City, IA 52242 – sequence: 2 givenname: Xiao surname: Peng fullname: Peng, Xiao – sequence: 3 givenname: Catlin E surname: Tolbert fullname: Tolbert, Catlin E – sequence: 4 givenname: Christophe surname: Guilluy fullname: Guilluy, Christophe – sequence: 5 givenname: Ashley E surname: Angell fullname: Angell, Ashley E – sequence: 6 givenname: Yuan surname: Pan fullname: Pan, Yuan – sequence: 7 givenname: Richard surname: Superfine fullname: Superfine, Richard – sequence: 8 givenname: Keith surname: Burridge fullname: Burridge, Keith – sequence: 9 givenname: Kris A surname: DeMali fullname: DeMali, Kris A |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24751539$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright Rockefeller University Press Apr 28, 2014 2014 Bays et al. 2014 |
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| Snippet | Cells experience mechanical forces throughout their lifetimes. Vinculin is critical for transmitting these forces, yet how it achieves its distinct functions... Vinculin phosphorylation on residue Y822 is necessary for cell stiffening in response to tension on cadherins but not integrins. Cells experience mechanical... |
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| SubjectTerms | Cadherins - genetics Cadherins - metabolism Cell adhesion & migration Cell Adhesion - physiology Cell Communication - physiology Cell Line, Tumor Cellular biology Extracellular Matrix - genetics Extracellular Matrix - metabolism Humans Kinases Mechanotransduction, Cellular - physiology Mutation Phosphorylation Phosphorylation - physiology Proto-Oncogene Proteins c-abl - genetics Proto-Oncogene Proteins c-abl - metabolism Signal transduction Vinculin - genetics Vinculin - metabolism |
| Title | Vinculin phosphorylation differentially regulates mechanotransduction at cell-cell and cell-matrix adhesions |
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