Nramp1 functionality increases inducible nitric oxide synthase transcription via stimulation of IFN regulatory factor 1 expression

J Immunol. 2003 Aug 15;171(4):1994-8. doi: 10.4049/jimmunol.171.4.1994.

Abstract

Natural-resistance associated macrophage protein 1 (Nramp1) encodes a transmembrane phagolysosomal protein exerting resistance toward infections with intracellular pathogens by a mechanism not fully elucidated so far. We used the murine macrophage cell line RAW264.7, stably transfected with functional (RAW-37) or nonfunctional (RAW-21) Nramp1, to study for differences in the expression of NO, a central antimicrobial effector molecule of macrophages. Following stimulation with IFN-gamma and LPS, Nramp1-expressing cells exhibit higher enzymatic activity of inducible NO synthase (iNOS) and increased cytoplasmic iNOS mRNA levels than RAW-21 cells. Time-course experiments showed that iNOS-mRNA levels remain increased in RAW-37 cells after prolonged cytokine stimulation while they decrease in RAW-21 cells. Reporter gene assays with iNOS-promoter luciferase constructs demonstrated an increased and prolonged promoter activity in Nramp1-resistant vs susceptible cells. This was paralleled by increased IFN regulatory factor 1 (IRF-1) expression and binding affinity to the iNOS promoter in RAW-37 cells, which may be related to enhanced STAT-1 binding affinity in these cells. A point mutation within the IRF-1 binding site of the iNOS promoter abolished the differences in iNOS transcription between RAW-21 and RAW-37 cells. Cells carrying functional Nramp1 express increased amounts of NO, which may be related to STAT-1-mediated stimulation of IRF-1 expression with subsequent prolonged activation of iNOS transcription. Enhanced NO expression may partly underlie the protection against infection with intracellular pathogens by Nramp1 functionality.

MeSH terms

  • Animals
  • Blotting, Northern
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / physiology*
  • Cell Line
  • DNA-Binding Proteins / biosynthesis*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology
  • Down-Regulation / drug effects
  • Down-Regulation / immunology
  • Enzyme Activation / genetics
  • Enzyme Activation / immunology
  • Gene Expression Regulation / immunology
  • Immunity, Innate / genetics
  • Interferon Regulatory Factor-1
  • Interferon-gamma / pharmacology
  • Iron / pharmacology
  • Lipopolysaccharides / pharmacology
  • Macrophages / enzymology*
  • Macrophages / immunology
  • Macrophages / microbiology
  • Mice
  • Mice, Inbred BALB C
  • Nitric Oxide Synthase / biosynthesis
  • Nitric Oxide Synthase / genetics*
  • Nitric Oxide Synthase / metabolism*
  • Nitric Oxide Synthase Type II
  • Nitrites / metabolism
  • Phosphoproteins / biosynthesis*
  • Phosphoproteins / genetics
  • Phosphoproteins / physiology
  • RNA, Messenger / biosynthesis
  • Salmonella typhimurium / immunology
  • Transcription, Genetic / immunology*
  • Transfection
  • Up-Regulation / drug effects
  • Up-Regulation / genetics*
  • Up-Regulation / immunology*

Substances

  • Cation Transport Proteins
  • DNA-Binding Proteins
  • Interferon Regulatory Factor-1
  • Irf1 protein, mouse
  • Lipopolysaccharides
  • Nitrites
  • Phosphoproteins
  • RNA, Messenger
  • natural resistance-associated macrophage protein 1
  • Interferon-gamma
  • Iron
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse