Neural Wiskott-Aldrich syndrome protein (N-WASP)-mediated p120-catenin interaction with Arp2-Actin complex stabilizes endothelial adherens junctions

J Biol Chem. 2013 Feb 8;288(6):4241-50. doi: 10.1074/jbc.M112.440396. Epub 2012 Dec 4.

Abstract

Stable adherens junctions (AJs) are required for formation of restrictive endothelial barrier. Vascular endothelial cadherin from contiguous endothelial cells forms AJs, which are stabilized intracellularly by binding of p120-catenin and cortical actin. Mechanisms inducing cortical actin formation and enabling its linkage with p120-catenin remain enigmatic. We altered the function of neural Wiskott-Aldrich syndrome protein (N-WASP), which induces actin polymerization through actin-related protein 2/3 complex (Arp2/3), to address the role of N-WASP in regulating AJ stability and thereby endothelial permeability. We show that depletion of N-WASP in endothelial cells impaired AJ adhesion and favored the organization of actin from cortical actin to stress fibers, resulting thereby in formation of leaky endothelial barrier. Exposure of the N-WASP-depleted endothelial cell monolayer to the permeability-increasing mediator, thrombin, exaggerated AJ disruption and stress fiber formation, leading to an irreversible increase in endothelial permeability. We show that N-WASP binds p120-catenin through its verprolin cofilin acid (VCA) domain, induces cortical actin formation through Arp2, and links p120-catenin with cortical actin. The interaction of N-WASP with p120-catenin, actin, and Arp2 requires phosphorylation of N-WASP at the Tyr-256 residue by focal adhesion kinase. Expression of the VCA domain of N-WASP or phosphomimicking (Y256D)-N-WASP mutant in endothelial cells stabilizes AJs and facilitates barrier recovery after thrombin stimulation. Our study demonstrates that N-WASP, by mediating p120-catenin interaction with actin-polymerizing machinery, maintains AJs and mitigates disruption of endothelial barrier function by edemagenic agents, therefore representing a novel target for preventing leaky endothelial barrier syndrome.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Actin-Related Protein 2 / genetics
  • Actin-Related Protein 2 / metabolism*
  • Actin-Related Protein 2-3 Complex / genetics
  • Actin-Related Protein 2-3 Complex / metabolism
  • Adherens Junctions / genetics
  • Adherens Junctions / metabolism*
  • Animals
  • COS Cells
  • Catenins / genetics
  • Catenins / metabolism*
  • Chlorocebus aethiops
  • Delta Catenin
  • Endothelial Cells / metabolism*
  • Humans
  • Phosphorylation / genetics
  • Protein Binding / genetics
  • Protein Structure, Tertiary
  • Stress Fibers / genetics
  • Stress Fibers / metabolism*
  • Wiskott-Aldrich Syndrome Protein, Neuronal / genetics
  • Wiskott-Aldrich Syndrome Protein, Neuronal / metabolism*

Substances

  • ACTR2 protein, human
  • Actin-Related Protein 2
  • Actin-Related Protein 2-3 Complex
  • Catenins
  • WASL protein, human
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • Delta Catenin