Hepatocyte growth factor-induced Asef-IQGAP1 complex controls cytoskeletal remodeling and endothelial barrier

J Biol Chem. 2015 Feb 13;290(7):4097-109. doi: 10.1074/jbc.M114.620377. Epub 2014 Dec 9.

Abstract

Hepatocyte growth factor (HGF) attenuates agonist-induced endothelial cell (EC) permeability and increases pulmonary endothelial barrier function via Rac-dependent enhancement of the peripheral actin cytoskeleton. However, the precise mechanisms of HGF effects on the peripheral cytoskeleton are not well understood. This study evaluated a role for Rac/Cdc42-specific guanine nucleotide exchange factor Asef and the multifunctional Rac effector, IQGAP1, in the mechanism of HGF-induced EC barrier enhancement. HGF induced Asef and IQGAP1 co-localization at the cell cortical area and stimulated formation of an Asef-IQGAP1 functional protein complex. siRNA-induced knockdown of Asef or IQGAP1 attenuated HGF-induced EC barrier enhancement. Asef knockdown attenuated HGF-induced Rac activation and Rac association with IQGAP1, and it abolished both IQGAP1 accumulation at the cell cortical layer and IQGAP1 interaction with actin cytoskeletal regulators cortactin and Arp3. Asef activation state was essential for Asef interaction with IQGAP1 and protein complex accumulation at the cell periphery. In addition to the previously reported role of the IQGAP1 RasGAP-related domain in the Rac-dependent IQGAP1 activation and interaction with its targets, we show that the IQGAP1 C-terminal domain is essential for HGF-induced IQGAP1/Asef interaction and Asef-Rac-dependent activation leading to IQGAP1 interaction with Arp3 and cortactin as a positive feedback mechanism of IQGAP1 activation. These results demonstrate a novel feedback mechanism of HGF-induced endothelial barrier enhancement via Asef/IQGAP1 interactions, which regulate the level of HGF-induced Rac activation and promote cortical cytoskeletal remodeling via IQGAP1-Arp3/cortactin interactions.

Keywords: Endothelium; Lung Injury; Permeability; Rac GTPases; Signal Transduction; Vascular Biology.

Publication types

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

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Blotting, Western
  • Cell Membrane Permeability*
  • Cells, Cultured
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / metabolism*
  • Fluorescent Antibody Technique
  • Hepatocyte Growth Factor / pharmacology*
  • Humans
  • Immunoprecipitation
  • Pulmonary Artery / cytology
  • Pulmonary Artery / metabolism*
  • RNA, Small Interfering / genetics
  • Rho Guanine Nucleotide Exchange Factors / antagonists & inhibitors
  • Rho Guanine Nucleotide Exchange Factors / genetics
  • Rho Guanine Nucleotide Exchange Factors / metabolism
  • rac GTP-Binding Proteins / metabolism
  • ras GTPase-Activating Proteins / antagonists & inhibitors
  • ras GTPase-Activating Proteins / genetics
  • ras GTPase-Activating Proteins / metabolism*

Substances

  • ARHGEF4 protein, human
  • IQ motif containing GTPase activating protein 1
  • RNA, Small Interfering
  • Rho Guanine Nucleotide Exchange Factors
  • ras GTPase-Activating Proteins
  • Hepatocyte Growth Factor
  • rac GTP-Binding Proteins