Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein

J Biol Chem. 2003 Dec 19;278(51):51006-14. doi: 10.1074/jbc.M304103200. Epub 2003 Sep 30.

Abstract

Heme oxygenase-1 (HO-1) catalyzes the rate-limiting step in heme degradation, protects against oxidative stress, and shows potent anti-inflammatory effects. Oxidized phospholipids, which are generated during inflammation and apoptosis, modulate the inflammatory response by inducing the expression of several genes including HO-1. Here we investigated the signaling pathways and transcriptional events involved in the induction of HO-1 gene expression by oxidized 1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine (OxPAPC) in human umbilical vein endothelial cells. OxPAPC up-regulated HO-1 mRNA and protein in a time- and concentration-dependent manner, whereas pro-inflammatory agents like TNF-alpha and lipopolysaccharide did not significantly induce HO-1 expression in human umbilical vein endothelial cells. Signaling pathways involved in the OxPAPC-mediated HO-1 induction included protein kinases A and C, as well as the mitogen-activated protein kinases p38 and ERK. The cAMP-responsive element-binding protein (CREB) was phosphorylated via these pathways in response to OxPAPC treatment and expression of a dominant-negative mutant of CREB inhibited OxPAPC-induced activity of a human heme oxygenase-1 promoter-driven luciferase reporter construct. We identified a cAMP-responsive element and a Maf recognition element to be involved in the transcriptional activation of the HO-1 promoter by OxPAPC. In gel shift assays we observed binding of CREB to the cAMP-responsive element after OxPAPC treatment. Induction of HO-1 expression by lipid oxidation products via CREB may represent a feedback mechanism to limit inflammation and associated tissue damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cyclic AMP Response Element-Binding Protein / metabolism*
  • Dose-Response Relationship, Drug
  • Endothelial Cells / metabolism
  • Gene Expression Regulation / drug effects*
  • Heme Oxygenase (Decyclizing) / biosynthesis*
  • Heme Oxygenase-1
  • Humans
  • Membrane Proteins
  • Oxidation-Reduction
  • Phospholipids / pharmacology*
  • Phosphorylation / drug effects
  • Promoter Regions, Genetic
  • Response Elements
  • Signal Transduction
  • Umbilical Veins / cytology

Substances

  • Cyclic AMP Response Element-Binding Protein
  • Membrane Proteins
  • Phospholipids
  • HMOX1 protein, human
  • Heme Oxygenase (Decyclizing)
  • Heme Oxygenase-1