Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection

J Exp Med. 2002 Nov 4;196(9):1253-62. doi: 10.1084/jem.20021183.

Abstract

The production of interleukin (IL)-12 is critical for the development of interferon (IFN)-gamma-dependent resistance to Toxoplasma gondii. Nevertheless, when this response is dysregulated, such as occurs in the absence of IL-10, the uncontrolled inflammation that results can have lethal consequences for the host. Recently, we demonstrated that lipoxin (LX)A(4), an eicosanoid mediator that depends on 5-lipoxygenase (LO) for its biosynthesis, exerts a regulatory role on dendritic cell IL-12 production triggered artificially by a T. gondii extract. We now formally establish the physiological relevance of this pathway in the systemic control of IL-12 production induced by live T. gondii infection and demonstrate its function to be distinct from that of IL-10. Thus, T. gondii-exposed wild-type, but not 5-LO-deficient animals, produced high levels of serum LXA(4) beginning at the onset of chronic infection. Moreover, 5-LO(-/-), in contrast to wild-type mice, succumbed during the same period displaying a marked encephalitis. The increased mortality of the 5-LO(-/-) animals was also associated with significant elevations of IL-12 and IFN-gamma and was completely prevented by the administration of a stable LXA(4) analogue. Together, these findings demonstrate a new pathway involving the induction of host LXs for the in vivo regulation of proinflammatory responses during microbial infection.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Arachidonate 5-Lipoxygenase / immunology*
  • Brain / pathology
  • Cells, Cultured
  • Disease Susceptibility / immunology
  • Female
  • Hydroxyeicosatetraenoic Acids / administration & dosage
  • Hydroxyeicosatetraenoic Acids / blood
  • Hydroxyeicosatetraenoic Acids / immunology*
  • Interferon-gamma / blood
  • Interleukin-10 / blood
  • Interleukin-12 / biosynthesis*
  • Interleukin-12 / blood
  • Interleukin-12 / immunology
  • Lipoxins*
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / parasitology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Toxoplasma / immunology
  • Toxoplasmosis / immunology*
  • Toxoplasmosis / mortality
  • Toxoplasmosis / pathology
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Hydroxyeicosatetraenoic Acids
  • Lipoxins
  • Tumor Necrosis Factor-alpha
  • lipoxin A4
  • Interleukin-10
  • Interleukin-12
  • Interferon-gamma
  • Arachidonate 5-Lipoxygenase