Negative feedback regulation of lipopolysaccharide-induced inducible nitric oxide synthase gene expression by heme oxygenase-1 induction in macrophages

Mol Immunol. 2008 Apr;45(7):2106-15. doi: 10.1016/j.molimm.2007.10.011. Epub 2007 Nov 19.

Abstract

Heme oxygenase-1 (HO-1) is induced under infectious diseases in macrophages. We performed experiments using various gene deficient mouse-derived macrophages to determine a detailed induction mechanism of HO-1 by lipopolysaccharide (LPS) and the functional role of HO-1 induction in macrophages. LPS (1 microg/mL) maximally induced inducible nitric oxide synthase (iNOS) and HO-1 mRNAs in wild-type (WT) macrophages at 6h and 12h after treatment, respectively, and liberated tumor necrosis factor alpha (TNFalpha) from WT macrophages. LPS also induced iNOS and HO-1 in TNFalpha(-/-) macrophages, but not in iNOS(-/-) macrophages. Interestingly, although LPS strongly induced iNOS, it failed to induce HO-1 almost completely in nuclear-factor erythroid 2-related factor 2 (Nrf2)(-/-) macrophages. The LPS-induced iNOS gene expression was suppressed by pretreatment with HO-1 inducers, hemin and Co-protoporphyrin (CoPP), but not with HO-1 inhibitor, Sn-protoporphyrin in WT macrophages. In the Nrf2(-/-) macrophages, the ability of CoPP to induce HO-1 and its inhibitory effect on the LPS-induced iNOS gene expression were lower than seen in WT macrophages. The present findings suggest that HO-1 is induced via NO-induced nuclear translocation of Nrf2, and the enzymatic function of HO-1 inhibits the overproduction of NO in macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cytokines / metabolism
  • Enzyme Induction / drug effects
  • Feedback, Physiological / drug effects*
  • Gene Expression Regulation, Enzymologic / drug effects*
  • Heme Oxygenase-1 / biosynthesis*
  • I-kappa B Proteins / metabolism
  • Inflammation Mediators / metabolism
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects*
  • Macrophages / enzymology*
  • Macrophages / metabolism
  • Metalloporphyrins / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • NF-E2-Related Factor 2 / metabolism
  • NF-KappaB Inhibitor alpha
  • Nitric Oxide Synthase Type II / deficiency
  • Nitric Oxide Synthase Type II / genetics*
  • Phosphorylation / drug effects
  • Protoporphyrins / pharmacology
  • Time Factors
  • Tumor Necrosis Factor-alpha / deficiency

Substances

  • Cytokines
  • I-kappa B Proteins
  • Inflammation Mediators
  • Lipopolysaccharides
  • Metalloporphyrins
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • Nfkbia protein, mouse
  • Protoporphyrins
  • Tumor Necrosis Factor-alpha
  • NF-KappaB Inhibitor alpha
  • cobaltiprotoporphyrin
  • tin protoporphyrin IX
  • Nitric Oxide Synthase Type II
  • Heme Oxygenase-1