Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide

Free Radic Biol Med. 2006 Jul 1;41(1):106-19. doi: 10.1016/j.freeradbiomed.2006.03.021. Epub 2006 Apr 25.

Abstract

Hydrogen sulfide (H(2)S), a regulatory gaseous molecule that is endogenously synthesized by cystathionine gamma-lyase (CSE) and/or cystathionine beta-synthase (CBS) from L-cysteine (L-Cys) metabolism, is a putative vasodilator, and its role in nitric oxide (NO) production is unexplored. Here, we show that at noncytotoxic concentrations, H(2)S was able to inhibit NO production and inducible NO synthase (iNOS) expression via heme oxygenase (HO-1) expression in RAW264.7 macrophages stimulated with lipopolysaccharide (LPS). Both H(2)S solution prepared by bubbling pure H(2)S gas and NaSH, a H(2)S donor, dose dependently induced HO-1 expression through the activation of the extracellular signal-regulated kinase (ERK). Pretreatment with H(2)S or NaHS significantly inhibited LPS-induced iNOS expression and NO production. Moreover, NO production in LPS-stimulated macrophages that are expressing CSE mRNA was significantly reduced by the addition of L-Cys, a substrate for H(2)S, but enhanced by the selective CSE inhibitor beta-cyano-L-alanine but not by the CBS inhibitor aminooxyacetic acid. While either blockage of HO activity by the HO inhibitor, tin protoporphyrin IX, or down-regulation of HO-1 expression by HO-1 small interfering RNA (siRNA) reversed the inhibitory effects of H(2)S on iNOS expression and NO production, HO-1 overexpression produced the same inhibitory effects of H(2)S. In addition, LPS-induced nuclear factor (NF)-kappaB activation was diminished in RAW264.7 macrophages preincubated with H(2)S. Interestingly, the inhibitory effect of H(2)S on NF-kappaB activation was reversed by the transient transfection with HO-1 siRNA, but was mimicked by either HO-1 gene transfection or treatment with carbon monoxide (CO), an end product of HO-1. CO treatment also inhibited LPS-induced NO production and iNOS expression via its inactivation of NF-kappaB. Collectively, our results suggest that H(2)S can inhibit NO production and NF-kappaB activation in LPS-stimulated macrophages through a mechanism that involves the action of HO-1/CO.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carbon Monoxide / metabolism
  • Cell Line
  • Heme Oxygenase-1 / biosynthesis
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Hydrogen Sulfide / metabolism
  • Hydrogen Sulfide / pharmacology*
  • Hydrogen Sulfide / toxicity
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects
  • Macrophages / enzymology
  • Macrophages / metabolism*
  • Mice
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • NF-kappa B / metabolism*
  • Nitric Oxide / antagonists & inhibitors
  • Nitric Oxide / biosynthesis*
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type II / biosynthesis
  • Nitric Oxide Synthase Type II / metabolism
  • Potassium Channels / metabolism
  • Sulfides / pharmacology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Lipopolysaccharides
  • NF-kappa B
  • Potassium Channels
  • Sulfides
  • mitochondrial K(ATP) channel
  • Nitric Oxide
  • Carbon Monoxide
  • Nitric Oxide Synthase Type II
  • Heme Oxygenase-1
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • p38 Mitogen-Activated Protein Kinases
  • sodium bisulfide
  • Hydrogen Sulfide