Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta

FASEB J. 2002 Jul;16(9):950-62. doi: 10.1096/fj.01-0870com.

Abstract

The stabilization of endothelial cell (EC) barrier function within newly formed capillaries is a critical feature of angiogenesis. We examined human lung EC barrier regulation elicited by hepatocyte growth factor (HGF), a recognized angiogenic factor and EC chemoattractant. HGF rapidly and dose-dependently elevated transendothelial electrical resistance (TER) of EC monolayers (>50% increase at 100 ng/ml), with immunofluorescence microscopic evidence of both cytoplasmic actin stress fiber dissolution and strong augmentation of the cortical actin ring. HGF rapidly stimulated phosphatidylinositol 3'-kinase, ERK, p38 mitogen-activated protein kinase, and protein kinase C activities. Pharmacological inhibitor studies demonstrated each pathway to be intimately involved in HGF-induced increases in TER, cortical actin thickening, and phosphorylation of the Ser/Thr glycogen synthase kinase-3beta (GSK-3beta), a potential target for the HGF barrier-promoting response. GSK-3beta phosphorylation was strongly correlated with reductions in both HGF-induced TER and enhanced beta-catenin immunoreactivity observed at cell-cell junctions. Our data suggest a model in which HGF-mediated EC cytoskeletal rearrangement and barrier enhancement depend critically on the activation of a complex kinase cascade that converges at GSK-3beta to increase the availability of beta-catenin, thereby enhancing endothelial junctional integrity and vascular barrier function.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Actin Cytoskeleton / chemistry
  • Actin Cytoskeleton / enzymology
  • Actin Cytoskeleton / ultrastructure*
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinases / physiology*
  • Cattle
  • Cell Line
  • Cell Membrane Permeability
  • Cells, Cultured
  • Cytoskeletal Proteins / analysis
  • Dose-Response Relationship, Drug
  • Electric Impedance
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / physiology*
  • Endothelium, Vascular / ultrastructure*
  • Glycogen Synthase Kinase 3
  • Glycogen Synthase Kinases
  • Hepatocyte Growth Factor / pharmacology*
  • Humans
  • Kinetics
  • Mitogen-Activated Protein Kinases / physiology
  • Phosphatidylinositol 3-Kinases / physiology
  • Protein Kinase C / physiology
  • Pulmonary Artery / cytology*
  • Trans-Activators*
  • beta Catenin
  • rac GTP-Binding Proteins / physiology

Substances

  • CTNNB1 protein, human
  • Cytoskeletal Proteins
  • Trans-Activators
  • beta Catenin
  • Hepatocyte Growth Factor
  • Phosphatidylinositol 3-Kinases
  • Glycogen Synthase Kinases
  • Protein Kinase C
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Mitogen-Activated Protein Kinases
  • Glycogen Synthase Kinase 3
  • rac GTP-Binding Proteins