Suppression of IFNgamma+mycobacterial lipoarabinomannan-induced NO by IL-4 is due to decreased IRF-1 expression

Tuberculosis (Edinb). 2009 Jul;89(4):294-303. doi: 10.1016/j.tube.2009.03.004. Epub 2009 Jun 24.

Abstract

In mice, and possibly in humans, nitric oxide (NO) is an important host-defense molecule against Mycobacterium tuberculosis. Inducible nitric oxide synthase (iNOS) and NO are upregulated in murine macrophages stimulated with interferon-gamma (IFNgamma) and mannose-capped lipoarabinomannan (ManLAM), a major lipoglycan in the cell wall of M. tuberculosis. Interleukin-4 (IL-4) can inhibit NO expression and may impair host immune response to M. tuberculosis. Therefore, we sought to determine the mechanism by which IL-4 inhibits IFNgamma+ManLAM-induced NO production. Since l-arginine is the substrate for both iNOS and arginase, and IL-4 increases arginase activity by inducing its production, a plausible mechanism of IL-4 inhibition of NO expression is via depletion of l-arginine through increased arginase activity. Herein, we show that IL-4 inhibited iNOS gene expression at the transcriptional level, suggesting an inhibitory mechanism that is independent of the competition for l-arginine between iNOS and arginase. Furthermore, pharmacologic inhibition of IL-4-induced arginase activity did not abrogate IL-4 inhibition of IFNgamma+ManLAM-induced NO expression. Instead, inhibition by IL-4 was mediated principally by the ability of IL-4 to inhibit the production of IFNgamma-induced interferon-gamma response factor-1 (IRF-1) protein, a critically important transcriptional element that enhances expression of IFNgamma-inducible genes such as iNOS.

MeSH terms

  • Animals
  • Arginase / metabolism
  • Arginine / metabolism
  • Blotting, Western
  • Cells, Cultured
  • Enzyme-Linked Immunosorbent Assay
  • Gene Expression / drug effects
  • Humans
  • Interferon Regulatory Factor-1 / metabolism
  • Interferon-gamma / metabolism
  • Interferon-gamma / pharmacology*
  • Interleukin-18 / metabolism
  • Interleukin-4 / pharmacology*
  • Lipopolysaccharides / metabolism
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mycobacterium tuberculosis / immunology
  • Nitric Oxide / biosynthesis*
  • Nitric Oxide / genetics
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Promoter Regions, Genetic / physiology
  • RNA, Messenger / metabolism
  • STAT6 Transcription Factor / metabolism

Substances

  • Interferon Regulatory Factor-1
  • Interleukin-18
  • Lipopolysaccharides
  • RNA, Messenger
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • lipoarabinomannan
  • Interleukin-4
  • Nitric Oxide
  • Interferon-gamma
  • Arginine
  • Nitric Oxide Synthase Type II
  • Arginase