Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth

Ingo Thievessen, Peter M. Thompson, Sylvain Berlemont, Karen M. Plevock, Sergey V. Plotnikov, Alice Zemljic-Harpf, Robert S. Ross, Michael W. Davidson, Gaudenz Danuser, Sharon L. Campbell, Clare M. Waterman

Research output: Contribution to journalArticle

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Abstract

In migrating cells, integrin-based focal adhesions (FAs) assemble in protruding lamellipodia in association with rapid filamentous actin (F-actin) assembly and retrograde flow. How dynamic F-actin is coupled to FA is not known. We analyzed the role of vinculin in integrating Factin and FA dynamics by vinculin gene disruption in primary fibroblasts. Vinculin slowed F-actin flow in maturing FA to establish a lamellipodium-lamellum border and generate high extracellular matrix (ECM) traction forces. In addition, vinculin promoted nascent FA formation and turnover in lamellipodia and inhibited the frequency and rate of FA maturation. Characterization of a vinculin point mutant that specifically disrupts Factin binding showed that vinculin-F-actin interaction is critical for these functions. However, FA growth rate correlated with F-actin flow speed independently of vinculin. Thus, vinculin functions as a molecular clutch, organizing leading edge F-actin, generating ECM traction, and promoting FA formation and turnover, but vinculin is dispensible for FA growth.

Original languageEnglish (US)
Pages (from-to)163-177
Number of pages15
JournalJournal of Cell Biology
Volume202
Issue number1
DOIs
StatePublished - 2013

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Vinculin
Focal Adhesions
Actins
Growth
Pseudopodia
Traction
Extracellular Matrix
Integrins
Fibroblasts

ASJC Scopus subject areas

  • Cell Biology

Cite this

Thievessen, I., Thompson, P. M., Berlemont, S., Plevock, K. M., Plotnikov, S. V., Zemljic-Harpf, A., ... Waterman, C. M. (2013). Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. Journal of Cell Biology, 202(1), 163-177. https://doi.org/10.1083/jcb.201303129

Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. / Thievessen, Ingo; Thompson, Peter M.; Berlemont, Sylvain; Plevock, Karen M.; Plotnikov, Sergey V.; Zemljic-Harpf, Alice; Ross, Robert S.; Davidson, Michael W.; Danuser, Gaudenz; Campbell, Sharon L.; Waterman, Clare M.

In: Journal of Cell Biology, Vol. 202, No. 1, 2013, p. 163-177.

Research output: Contribution to journalArticle

Thievessen, I, Thompson, PM, Berlemont, S, Plevock, KM, Plotnikov, SV, Zemljic-Harpf, A, Ross, RS, Davidson, MW, Danuser, G, Campbell, SL & Waterman, CM 2013, 'Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth', Journal of Cell Biology, vol. 202, no. 1, pp. 163-177. https://doi.org/10.1083/jcb.201303129
Thievessen, Ingo ; Thompson, Peter M. ; Berlemont, Sylvain ; Plevock, Karen M. ; Plotnikov, Sergey V. ; Zemljic-Harpf, Alice ; Ross, Robert S. ; Davidson, Michael W. ; Danuser, Gaudenz ; Campbell, Sharon L. ; Waterman, Clare M. / Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. In: Journal of Cell Biology. 2013 ; Vol. 202, No. 1. pp. 163-177.
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