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J. Cell Biol. 150 (3): 567-580

Copyright © 2000 by the Rockefeller University Press.

Original Article

P120 Catenin Regulates the Actin Cytoskeleton via Rho Family Gtpases

Nicole K. Norena, Betty P. Liua, Keith Burridgea, , and Bertolt Krefta

a Department of Cell Biology and Anatomy and the Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599
Department of Cell Biology and Anatomy, 108 Taylor Hall, CB#7090, University of North Carolina, Chapel Hill, NC 27599-7090.(919) 966-1856(919) 966-5783

kburridg{at}med.unc.edu

Abstract: Cadherins are calcium-dependent adhesion molecules responsible for the establishment of tight cell–cell contacts. p120 catenin (p120ctn) binds to the cytoplasmic domain of cadherins in the juxtamembrane region, which has been implicated in regulating cell motility. It has previously been shown that overexpression of p120ctn induces a dendritic morphology in fibroblasts (Reynolds, A.B., J. Daniel, Y. Mo, J. Wu, and Z. Zhang. 1996. Exp. Cell Res. 225:328–337.). We show here that this phenotype is suppressed by coexpression of cadherin constructs that contain the juxtamembrane region, but not by constructs lacking this domain. Overexpression of p120ctn disrupts stress fibers and focal adhesions and results in a decrease in RhoA activity. The p120ctn-induced phenotype is blocked by dominant negative Cdc42 and Rac1 and by constitutively active Rho-kinase, but is enhanced by dominant negative RhoA. p120ctn overexpression increased the activity of endogenous Cdc42 and Rac1. Exploring how p120ctn may regulate Rho family GTPases, we find that p120ctn binds the Rho family exchange factor Vav2. The behavior of p120ctn suggests that it is a vehicle for cross-talk between cell–cell junctions and the motile machinery of cells. We propose a model in which p120ctn can shuttle between a cadherin-bound state and a cytoplasmic pool in which it can interact with regulators of Rho family GTPases. Factors that perturb cell–cell junctions, such that the cytoplasmic pool of p120ctn is increased, are predicted to decrease RhoA activity but to elevate active Rac1 and Cdc42, thereby promoting cell migration.

Key Words: cadherin • Rac • guanine nucleotide exchange factor • Vav2 • migration

N. Noren and B. Kreft contributed equally to this paper.

B. Kreft's present address is Schering AG, Genomics/Bioinformatics, Muellerstr. 178, 13342 Berlin, Germany.

1Abbreviations used in this paper: DN, dominant negative; GAP, GTPase activating proteins; GEF, guanine nucleotide exchange factor; GFP, green fluorescent protein; p120ctn, p120 catenin.

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Two Regions of Cadherin Cytoplasmic Domains Are Involved in Suppressing Motility of a Mammary Carcinoma Cell Line.
M. Fedor-Chaiken, T. E. Meigs, D. D. Kaplan, and R. Brackenbury (2003)
J. Biol. Chem. 278, 52371-52378
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A core function for p120-catenin in cadherin turnover.
M. A. Davis, R. C. Ireton, and A. B. Reynolds (2003)
J. Cell Biol. 163, 525-534
   Abstract »    Full Text »    PDF »
p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions.
X. Chen, S.-i. Kojima, G. G. Borisy, and K. J. Green (2003)
J. Cell Biol. 163, 547-557
   Abstract »    Full Text »    PDF »
Dual regulation of neuronal morphogenesis by a {delta}-catenin-cortactin complex and Rho.
M. C. Martinez, T. Ochiishi, M. Majewski, and K. S. Kosik (2003)
J. Cell Biol. 162, 99-111
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Differential regulation of junctional complex assembly in renal epithelial cell lines.
S. Gopalakrishnan, M. A. Hallett, S. J. Atkinson, and James. A. Marrs (2003)
Am J Physiol Cell Physiol 285, C102-C111
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Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin.
A. S.T. Wong and B. M. Gumbiner (2003)
J. Cell Biol. 161, 1191-1203
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Minimal Mutation of the Cytoplasmic Tail Inhibits the Ability of E-cadherin to Activate Rac but Not Phosphatidylinositol 3-Kinase: DIRECT EVIDENCE OF A ROLE FOR CADHERIN-ACTIVATED Rac SIGNALING IN ADHESION AND CONTACT FORMATION.
M. Goodwin, E. M. Kovacs, M. A. Thoreson, A. B. Reynolds, and A. S. Yap (2003)
J. Biol. Chem. 278, 20533-20539
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Mechanisms of VE-cadherin Processing and Degradation in Microvascular Endothelial Cells.
K. Xiao, D. F. Allison, M. D. Kottke, S. Summers, G. P. Sorescu, V. Faundez, and A. P. Kowalczyk (2003)
J. Biol. Chem. 278, 19199-19208
   Abstract »    Full Text »    PDF »
p120 Catenin Is Required for Growth Factor-dependent Cell Motility and Scattering in Epithelial Cells.
M. Cozzolino, V. Stagni, L. Spinardi, N. Campioni, C. Fiorentini, E. Salvati, S. Alema, and A. M. Salvatore (2003)
Mol. Biol. Cell 14, 1964-1977
   Abstract »    Full Text »    PDF »
NZO-3 Expression Causes Global Changes to Actin Cytoskeleton in Madin-Darby Canine Kidney Cells: Linking a Tight Junction Protein to Rho GTPases.
E. S. Wittchen, J. Haskins, and B. R. Stevenson (2003)
Mol. Biol. Cell 14, 1757-1768
   Abstract »    Full Text »    PDF »

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