The IL-6-soluble IL-6Ralpha autocrine loop of endothelial activation as an intermediate between acute and chronic inflammation: an experimental model involving thrombin

J Immunol. 2001 Sep 15;167(6):3435-42. doi: 10.4049/jimmunol.167.6.3435.

Abstract

Thrombin is a procoagulant and proinflammatory molecule in vivo. In vitro, thrombin has been shown to induce endothelial activation, notably IL-8 secretion and adhesion molecule expression. In this study, we showed that thrombin may induce a new cascade leading from acute to chronic inflammation. Thrombin was able to induce the production of both IL-6 and monocyte chemotactic protein-1 (MCP-1) by HUVEC independently of IL-1alphabeta and TNF-alpha. Addition of physiological concentrations of exogenous soluble IL-6Ralpha (sIL-6Ralpha) to thrombin-activated HUVEC was sufficient to increase the amounts of MCP-1 produced, but not those of IL-8. These effects could be blocked by anti-IL-6 or anti-sIL-6Ralpha blocking mAb, demonstrating the existence of an autocrine loop of MCP-1 secretion, involving the IL-6/IL-6Ralpha/gp130 complex on HUVEC. In addition, we identified IL-8-activated neutrophils as a potential source of sIL-6Ralpha because IL-8 induced IL-6Ralpha shedding from the neutrophil membranes and increased in parallel sIL-6Ralpha concentrations in neutrophil supernatants. Furthermore, addition of neutrophils to thrombin-activated HUVEC significantly increased MCP-1 secretion, which could be decreased by blocking IL-6. Thus, thrombin-activated endothelium may induce a cascade of events characterized by IL-8 secretion, neutrophil local infiltration, and the release of IL-6Ralpha from neutrophil membranes. sIL-6Ralpha may then complex with IL-6 and increase the amount of MCP-1 produced by thrombin-activated endothelium, favoring monocyte infiltration, and the transformation of acute into chronic inflammation.

MeSH terms

  • Acute Disease
  • Animals
  • Autocrine Communication / physiology*
  • Blood Coagulation / physiology
  • Cells, Cultured
  • Chemokine CCL2 / metabolism*
  • Chemokine CXCL1
  • Chemokines, CXC*
  • Chemotactic Factors / pharmacology
  • Chemotaxis, Leukocyte / physiology*
  • Chronic Disease
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / metabolism
  • Growth Substances / pharmacology
  • Humans
  • Inflammation / metabolism*
  • Intercellular Signaling Peptides and Proteins*
  • Interleukin-1 / pharmacology
  • Interleukin-6 / metabolism*
  • Interleukin-8 / metabolism
  • Interleukin-8 / pharmacology
  • Macromolecular Substances
  • Mice
  • Models, Animal
  • Neutrophils / drug effects*
  • Neutrophils / metabolism
  • Receptors, Interleukin-6 / genetics
  • Receptors, Interleukin-6 / physiology*
  • Recombinant Fusion Proteins / pharmacology
  • Signal Transduction / drug effects
  • Solubility
  • Thrombin / pharmacology*
  • Thrombin / physiology
  • Tumor Necrosis Factor-alpha / pharmacology
  • Umbilical Veins

Substances

  • CXCL1 protein, human
  • Chemokine CCL2
  • Chemokine CXCL1
  • Chemokines, CXC
  • Chemotactic Factors
  • Cxcl1 protein, mouse
  • Growth Substances
  • Intercellular Signaling Peptides and Proteins
  • Interleukin-1
  • Interleukin-6
  • Interleukin-8
  • Macromolecular Substances
  • Receptors, Interleukin-6
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha
  • Thrombin