Phosphatidylinositol-3,4,5-triphosphate-dependent Rac exchange factor 1 regulates epinephrine-induced exocytosis of Weibel-Palade bodies

J Thromb Haemost. 2014 Feb;12(2):273-81. doi: 10.1111/jth.12460.

Abstract

Background: Weibel-Palade bodies (WPBs) function as storage vesicles for von Willebrand factor (VWF) and a number of other bioactive compounds, including angiopoietin-2 and insulin-like growth factor-binding protein 7. WPBs release their content following stimulation with agonists that increase the level of intracellular Ca²⁺, such as thrombin, or agonists that increase intracellular levels of cAMP, such as epinephrine.

Objective: Previously, we have shown that the exchange protein activated by cAMP, exchange protein activated by cAMP, and the small GTPase Rap1 are involved in cAMP-mediated release of WPBs. In this study, we explored potential downstream effectors of Rap1 in cAMP-mediated WPB release.

Methods: Studies were performed in primary human umbilical vein endothelial cells. Activation of the small GTP-binding protein Rac1 was monitored by its ability to bind to the CRIB domain of the serine/threonine kinase P21-activated kinase (PAK)1. Downstream effectors of Rap1 were identified with a proteomic screen using a glutathione-S-transferase fusion of the Ras-binding domain of RalGDS. Functional involvement of candidate proteins in WPB release was determined by RNA interference (RNAi)-mediated knockdown of gene expression.

Results: Depletion of Rac1 by RNAi prevented epinephrine-induced VWF secretion. Also, the Rac1 inhibitor EHT1864 reduced epinephrine-induced WPB release. We identified the phosphatidylinositol-3,4,5-triphosphate-dependent Rac exchange factor 1 (PREX1) and the regulatory β-subunit of phosphatidylinositol 3-kinase (PI3K) as downstream targets of Rap1. The PI3K inhibitor LY294002 reduced epinephrine-induced release of VWF. RNAi-mediated downregulation of PREX1 abolished epinephrine-induced but not thrombin-induced release of WPBs.

Conclusion: Our findings show that PREX1 regulates epinephrine-induced release of WPBs.

Keywords: PREX1 protein; Rac1 GTP binding protein; Weibel-Palade bodies; endothelial cells; human; von Willebrand factor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cyclic AMP / metabolism
  • Epinephrine / pharmacology*
  • Exocytosis / drug effects*
  • Guanine Nucleotide Exchange Factors / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Phosphatidylinositol Phosphates / metabolism*
  • Signal Transduction
  • Weibel-Palade Bodies / drug effects*
  • Weibel-Palade Bodies / metabolism
  • rac1 GTP-Binding Protein / metabolism*
  • von Willebrand Factor / metabolism

Substances

  • Guanine Nucleotide Exchange Factors
  • Phosphatidylinositol Phosphates
  • phosphatidylinositol 3,4,5-triphosphate
  • von Willebrand Factor
  • Cyclic AMP
  • rac1 GTP-Binding Protein
  • Epinephrine