L-tryptophan-L-kynurenine pathway metabolism accelerated by Toxoplasma gondii infection is abolished in gamma interferon-gene-deficient mice: cross-regulation between inducible nitric oxide synthase and indoleamine-2,3-dioxygenase

Infect Immun. 2002 Feb;70(2):779-86. doi: 10.1128/IAI.70.2.779-786.2002.

Abstract

L-Tryptophan degradation by indoleamine 2,3-dioxygenase (IDO) might have an important role in gamma interferon (IFN-gamma)-induced antimicrobial effects. In the present study, the effects of Toxoplasma gondii infection on IDO were investigated by using wild-type and IFN-gamma-gene-deficient (knockout) (IFN-gamma KO) mice. In wild-type C57BL/6J mice, enzyme activities and mRNA levels for IDO in both lungs and brain were markedly increased and lung L-tryptophan concentrations were dramatically decreased following T. gondii infection. In contrast, these metabolic changes did not occur in T. gondii-infected IFN-gamma KO mice or in uninfected IFN-gamma KO mice. The levels of inducible nitric oxide synthase (iNOS) induction in infected IFN-gamma KO mice were high in lungs and low in brain compared to those in infected wild-type mice. The extent of increased mRNA expression of T. gondii surface antigen gene 2 (SAG2) induced in lungs and brain by T. gondii infection was significantly enhanced in IFN-gamma KO mice compared to wild-type mice on day 7 postinfection. Treatment with N-nitro-L-arginine methyl ester, an iNOS inhibitor, increased the levels of SAG2 mRNA in brain but not in lungs and of plasma L-kynurenine after T. gondii infection. This in vivo study provides evidence that L-tryptophan depletion caused by T. gondii is directly mediated by IFN-gamma in the lungs, where iNOS is not induced by IFN-gamma. This study suggests that there is an antitoxoplasma mechanism of cross-regulation between iNOS and IDO and that the expression of the main antiparasite effector mechanisms for iNOS and/or IDO may vary among tissues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Protozoan / genetics
  • Antigens, Surface / genetics
  • Brain / metabolism
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Gene Expression / drug effects
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Interferon-gamma / genetics
  • Interferon-gamma / physiology*
  • Kynurenine / metabolism*
  • Lung / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism*
  • Nitric Oxide Synthase Type II
  • Protozoan Proteins*
  • RNA, Messenger / biosynthesis
  • Toxoplasma
  • Toxoplasmosis / metabolism*
  • Tryptophan / metabolism*
  • Tryptophan Oxygenase / genetics
  • Tryptophan Oxygenase / metabolism*

Substances

  • Antigens, Protozoan
  • Antigens, Surface
  • Enzyme Inhibitors
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Protozoan Proteins
  • RNA, Messenger
  • surface antigen P22, Toxoplasma
  • Kynurenine
  • Interferon-gamma
  • Tryptophan
  • Tryptophan Oxygenase
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • NG-Nitroarginine Methyl Ester