Induction of heme-oxygenase 1 inhibits endothelial cell activation by endotoxin and oxidant stress

Surgery. 2003 Aug;134(2):146-52. doi: 10.1067/msy.2003.215.

Abstract

Background: Increased oxidant stress has been implicated in a number of disease states, including systemic inflammation caused by ischemia/reperfusion injury or sepsis. We have demonstrated previously that oxidants enhance the proinflammatory response to endotoxin (lipopolysaccharide), although antioxidants inhibit this response. Heme-oxygenase 1 (HO-1) is an inducible, cytoprotective enzyme, which is up-regulated under conditions of oxidant stress. We hypothesized that the induction of HO-1 protein would attenuate the proinflammatory response of endothelial cells to lipopolysaccharide and oxidant stress.

Methods: Human umbilical vein endothelial cells were pretreated with hemin (100 micromol/L) for 5 hours, and the induction of HO-1 was confirmed by Western blot. After hemin exposure, cells were treated for 1 hour with either diamide, buthione sulfoximine, xanthine oxidase, or glucose oxidase to induce oxidant stress or lipopolysaccharide to induce an inflammatory response. Interleukin 8 (IL-8) and prostaglandin I(2) (PGI(2)) production were measured by enzyme-linked immunosorbent assay; p38 kinase, p42/44 extracellular regulated kinase, and c-jun N terminal kinase activation were measured by Western blot.

Results: HO-1 protein was increased 3-fold by exposure to hemin under all conditions. IL-8 production in response to lipopolysaccharide and xanthine oxidase was inhibited significantly by hemin exposure, although PGI(2) production was not affected. The up-regulation of HO-1 protein levels resulted in the inhibition of the lipopolysaccharide- and oxidant-induced activation of all 3 mitogen-activated protein kinases: p38 kinase, p42/44 extracellular regulated kinase, and c-jun N terminal kinase.

Conclusions: The induction of HO-1 by hemin results in inhibition of the proinflammatory response of endothelial cells, as evidenced by the inhibition of IL-8 production without affecting PGI(2) production. All 3 mitogen-activated protein kinase signaling cascades are affected, which suggests that the mechanism of this effect may be proximal in the cell signaling process.

Publication types

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

MeSH terms

  • Cells, Cultured
  • Cytokines / biosynthesis
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / physiology*
  • Enzyme Activation / physiology
  • Enzyme Induction
  • Heme Oxygenase (Decyclizing) / metabolism*
  • Heme Oxygenase-1
  • Hemin / pharmacology
  • Humans
  • Interleukin-8 / biosynthesis
  • JNK Mitogen-Activated Protein Kinases
  • Lipopolysaccharides / pharmacology*
  • Membrane Proteins
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism
  • Oxidative Stress / physiology*
  • Signal Transduction / drug effects
  • Xanthine Oxidase / pharmacology
  • p38 Mitogen-Activated Protein Kinases

Substances

  • Cytokines
  • Interleukin-8
  • Lipopolysaccharides
  • Membrane Proteins
  • Hemin
  • HMOX1 protein, human
  • Heme Oxygenase (Decyclizing)
  • Heme Oxygenase-1
  • Xanthine Oxidase
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases