Asef mediates HGF protective effects against LPS-induced lung injury and endothelial barrier dysfunction

Am J Physiol Lung Cell Mol Physiol. 2015 Mar 1;308(5):L452-63. doi: 10.1152/ajplung.00170.2014. Epub 2014 Dec 24.

Abstract

Increased vascular endothelial permeability and inflammation are major pathological mechanisms of pulmonary edema and its life-threatening complication, the acute respiratory distress syndrome (ARDS). We have previously described potent protective effects of hepatocyte growth factor (HGF) against thrombin-induced hyperpermeability and identified the Rac pathway as a key mechanism of HGF-mediated endothelial barrier protection. However, anti-inflammatory effects of HGF are less understood. This study examined effects of HGF on the pulmonary endothelial cell (EC) inflammatory activation and barrier dysfunction caused by the gram-negative bacterial pathogen lipopolysaccharide (LPS). We tested involvement of the novel Rac-specific guanine nucleotide exchange factor Asef in the HGF anti-inflammatory effects. HGF protected the pulmonary EC monolayer against LPS-induced hyperpermeability, disruption of monolayer integrity, activation of NF-kB signaling, expression of adhesion molecules intercellular adhesion molecule-1 and vascular cell adhesion molecule-1, and production of IL-8. These effects were critically dependent on Asef. Small-interfering RNA-induced downregulation of Asef attenuated HGF protective effects against LPS-induced EC barrier failure. Protective effects of HGF against LPS-induced lung inflammation and vascular leak were also diminished in Asef knockout mice. Taken together, these results demonstrate potent anti-inflammatory effects by HGF and delineate a key role of Asef in the mediation of the HGF barrier protective and anti-inflammatory effects. Modulation of Asef activity may have important implications in therapeutic strategies aimed at the treatment of sepsis and acute lung injury/ARDS-induced gram-negative bacterial pathogens.

Keywords: cytoskeleton; guanine nucleotide exchange factors; hepatocyte growth factor; inflammation; permeability; pulmonary endothelium; vascular leak.

Publication types

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

MeSH terms

  • Cell Adhesion / drug effects
  • Cell Membrane Permeability / drug effects
  • Cell Movement / drug effects
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / pathology*
  • Endothelium, Vascular / physiopathology*
  • Guanine Nucleotide Exchange Factors / metabolism*
  • Hepatocyte Growth Factor / pharmacology*
  • Humans
  • Inflammation / pathology
  • Lipopolysaccharides
  • Lung / drug effects
  • Lung / pathology
  • Lung / physiopathology
  • Lung Injury / pathology*
  • Lung Injury / physiopathology*
  • Neutrophils / cytology
  • Neutrophils / drug effects
  • Protective Agents / pharmacology
  • Rho Guanine Nucleotide Exchange Factors / metabolism
  • Signal Transduction / drug effects

Substances

  • ARHGEF4 protein, human
  • Arhgef4 protein, mouse
  • Guanine Nucleotide Exchange Factors
  • Lipopolysaccharides
  • Protective Agents
  • Rho Guanine Nucleotide Exchange Factors
  • Hepatocyte Growth Factor