Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium

Eur J Immunol. 2008 Jul;38(7):1923-36. doi: 10.1002/eji.200738056.

Abstract

In stimulating effector functions of mononuclear phagocytes, IFN-gamma is of pivotal importance in host defense against intramacrophage pathogens including salmonellae. As the activity of IFN-gamma is modulated by iron and since a sufficient availability of iron is essential for the growth of pathogens, we investigated the regulatory effects of IFN-gamma on iron homeostasis and immune function in murine macrophages infected with Salmonella typhimurium. In Salmonella-infected phagocytes, IFN-gamma caused a significant reduction of iron uptake via transferrin receptor 1 and resulted in an increased iron efflux caused by an enhanced expression of the iron exporter ferroportin 1. Moreover, the expression of haem oxygenase 1 and of the siderophore-capturing antimicrobial peptide lipocalin 2 was markedly elevated following bacterial invasion, with IFN-gamma exerting a super-inducing effect. This observed regulatory impact of IFN-gamma reduced the intracellular iron pools within infected phagocytes, thus restricting the acquisition of iron by engulfed Salmonella typhimurium while concomitantly promoting NO and TNF-alpha production. Our data suggest that the modulation of crucial pathways of macrophage iron metabolism in response to IFN-gamma concordantly aims at withdrawing iron from intracellular Salmonella and at strengthening macrophage immune response functions. These regulations are thus consistent with the principles of nutritional immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute-Phase Proteins / metabolism
  • Animals
  • Antimicrobial Cationic Peptides / metabolism
  • Cation Transport Proteins / metabolism
  • Cell Line
  • Ferritins / metabolism
  • Heme Oxygenase (Decyclizing) / metabolism
  • Hepcidins
  • Interferon-gamma / immunology*
  • Interferon-gamma / metabolism
  • Iron / metabolism*
  • Lipocalin-2
  • Lipocalins / metabolism
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Mice
  • Nitric Oxide / metabolism
  • Oncogene Proteins / metabolism
  • Salmonella typhimurium / growth & development
  • Salmonella typhimurium / immunology
  • Salmonella typhimurium / metabolism*
  • Transferrin / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Acute-Phase Proteins
  • Antimicrobial Cationic Peptides
  • Cation Transport Proteins
  • Hepcidins
  • Lipocalin-2
  • Lipocalins
  • Oncogene Proteins
  • Transferrin
  • Tumor Necrosis Factor-alpha
  • metal transporting protein 1
  • Lcn2 protein, mouse
  • Nitric Oxide
  • Interferon-gamma
  • Ferritins
  • Iron
  • Heme Oxygenase (Decyclizing)