VASP is involved in cAMP-mediated Rac 1 activation in microvascular endothelial cells

Am J Physiol Cell Physiol. 2009 Mar;296(3):C453-62. doi: 10.1152/ajpcell.00360.2008. Epub 2008 Dec 31.

Abstract

Accumulating evidence points to a significant role of vasodilator-stimulated phosphoprotein (VASP) in the maintenance of endothelial barrier functions. We have recently shown that impaired barrier functions in VASP-deficient microvascular myocardial endothelial cells (MyEnd VASP(-/-)) correlated with decreased Rac 1 activity. To further test the hypothesis that VASP is involved in regulation of Rac 1 activity, we studied cAMP-dependent Rac 1 activation. Both inhibition of Rac 1 activation by NSC-23766 and inhibition of PKA by PKI completely blunted the efficacy of forskolin/rolipram (F/R)-mediated cAMP increase to stabilize barrier functions as revealed by measurements of transendothelial resistance (TER). Because these results indicate that PKA/Rac 1 activation is important for barrier stabilization, we tested this signaling pathway in VASP(-/-) cells. We found that F/R and isoproterenol reduced permeability measured as FITC-dextran flux across VASP(-/-) monolayers, but not below baseline levels of wild-type cells (WT). Moreover, cAMP-mediated Rac 1 activation was reduced to approximately 50% of WT levels, and both PKA inhibition by PKI and PKA anchoring via A kinase anchoring peptides (AKAPs) by HT31 almost completely abolished Rac 1 activation in VASP(-/-) and WT endothelium. Accordingly, HT31 significantly reduced F/R-mediated TER increase in WT cells and completely blocked the protective effect of cAMP on endothelial barrier properties. Together, our data underline the significant role of cAMP-mediated Rac 1 activation for endothelial barrier stabilization and demonstrate that both AKAP-mediated PKA anchoring and VASP are required for this process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A Kinase Anchor Proteins / metabolism
  • Animals
  • Capillary Permeability*
  • Cell Adhesion Molecules / deficiency
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Line
  • Cyclic AMP / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Dextrans / metabolism
  • Electric Impedance
  • Endothelial Cells / drug effects
  • Endothelial Cells / enzymology*
  • Enzyme Activation
  • Enzyme Activators / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Fluorescein-5-isothiocyanate / analogs & derivatives
  • Fluorescein-5-isothiocyanate / metabolism
  • Fluorescent Dyes / metabolism
  • Mice
  • Mice, Knockout
  • Microfilament Proteins / deficiency
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Microvessels / enzymology
  • Neuropeptides / genetics
  • Neuropeptides / metabolism*
  • Phosphoproteins / deficiency
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Protein Binding
  • Second Messenger Systems*
  • Time Factors
  • Transfection
  • rac GTP-Binding Proteins / genetics
  • rac GTP-Binding Proteins / metabolism*
  • rac1 GTP-Binding Protein

Substances

  • A Kinase Anchor Proteins
  • Cell Adhesion Molecules
  • Dextrans
  • Enzyme Activators
  • Enzyme Inhibitors
  • Fluorescent Dyes
  • Microfilament Proteins
  • Neuropeptides
  • Phosphoproteins
  • Rac1 protein, mouse
  • fluorescein isothiocyanate dextran
  • vasodilator-stimulated phosphoprotein
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • rac GTP-Binding Proteins
  • rac1 GTP-Binding Protein
  • Fluorescein-5-isothiocyanate