Synergistic effects of tumor necrosis factor-alpha and thrombin in increasing endothelial permeability

Am J Physiol Lung Cell Mol Physiol. 2001 Oct;281(4):L958-68. doi: 10.1152/ajplung.2001.281.4.L958.

Abstract

Because activation of the coagulation cascade and the generation of thrombin coexist with sepsis and the release of tumor necrosis factor (TNF)-alpha, we determined the effects of TNF-alpha on the mechanism of thrombin-induced increase in endothelial permeability. We assessed Ca(2+) signaling in human umbilical vein endothelial cells. In human umbilical vein endothelial cells exposed to TNF-alpha for 2 h, thrombin produced a rise in the intracellular Ca(2+) concentration ([Ca(2+)](i)) lasting up to 10 min. In contrast, thrombin alone produced a rise in [Ca(2+)](i) lasting for 3 min, whereas TNF-alpha alone had no effect on [Ca(2+)](i.) Thrombin-induced inositol 1,4,5-trisphosphate generation was not different between control and TNF-alpha-exposed cells. In the absence of extracellular Ca(2+), thrombin produced similar increases in [Ca(2+)](i) in both control and TNF-alpha-exposed cells. In TNF-alpha-exposed cells, the thrombin-induced Ca(2+) influx after intracellular Ca(2+) store depletion was significantly greater and prolonged compared with control cells. Increased Ca(2+) entry was associated with an approximately fourfold increase in Src activity and was sensitive to the Src kinase inhibitor PP1. After TNF-alpha exposure, thrombin caused increased tyrosine phosphorylation of junctional proteins and actin stress fiber formation as well as augmented endothelial permeability. These results suggest that TNF-alpha stimulation of endothelial cells results in amplification of the thrombin-induced Ca(2+) influx by an Src-dependent mechanism, thereby promoting loss of endothelial barrier function.

Publication types

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

MeSH terms

  • Albumins / pharmacokinetics
  • Calcium / metabolism
  • Cell Membrane Permeability / drug effects
  • Cell Membrane Permeability / physiology
  • Cells, Cultured
  • Drug Synergism
  • Electric Impedance
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Enzyme Activation / drug effects
  • Hemostatics / pharmacology*
  • Humans
  • Inositol 1,4,5-Trisphosphate / biosynthesis
  • Stress Fibers / drug effects
  • Stress Fibers / metabolism
  • Thrombin / pharmacology*
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Umbilical Veins / cytology
  • src-Family Kinases / metabolism

Substances

  • Albumins
  • Hemostatics
  • Tumor Necrosis Factor-alpha
  • Inositol 1,4,5-Trisphosphate
  • src-Family Kinases
  • Thrombin
  • Calcium