IDO1 plays an immunosuppressive role in 2,4,6-trinitrobenzene sulfate-induced colitis in mice

J Immunol. 2013 Sep 15;191(6):3057-64. doi: 10.4049/jimmunol.1203306. Epub 2013 Aug 16.

Abstract

IDO, an enzyme that degrades the essential amino acid L-tryptophan to N-formylkynurenine, is known to exert immunomodulatory effects in a number of diseases and disorders. IDO expression is increased in tumors, where it is thought to be involved in tumor evasion by suppressing the immune response. A competitive inhibitor of IDO is currently being tested in clinical trials for relapsed or refractory solid tumors; however, there remains a concern that attenuation of the immunosuppressive function of IDO might exacerbate inflammatory responses. In this study, we investigated the role of IDO in 2,4,6-trinitrobenzene sulfate (TNBS)-induced colitis in mice by gene deletion and pharmacological inhibition. TNBS treatment induced significantly more severe colitis in Ido1 gene-deficient (Ido1⁻/⁻) mice than in Ido1 wild-type (Ido1⁺/⁺) mice, indicating a role for IDO1 in suppression of acute colitis. Consistent with this, the expression of Ido1 was increased in the colonic interstitial tissues of TNBS-treated Ido1⁺/⁺ mice. Furthermore, transplantation of Ido1⁺/⁺ bone marrow cells into Ido1⁻/⁻ mice reduced the pathological damage associated with colitis, altered the expression of cytokines, including IFN-γ, TNF-α, and IL-10, and increased the number of CD4⁺ Foxp3⁺ regulatory T cells in the colon. Pharmacological inhibition of IDO enzymatic activity by oral administration of 1-methyltryptophan (1-methyl-L-tryptophan or 1-methyl-D-tryptophan) significantly increased the severity of TNBS-induced colitis in mice, demonstrating that both stereoisomers can promote colitis. Collectively, our data indicate that IDO1 plays an important immunoregulatory role in the colon.

MeSH terms

  • Animals
  • Colitis / chemically induced
  • Colitis / enzymology*
  • Colitis / immunology
  • Disease Models, Animal
  • Immune Tolerance / immunology*
  • Immunohistochemistry
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / immunology*
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Real-Time Polymerase Chain Reaction
  • Trinitrobenzenes / toxicity

Substances

  • IDO1 protein, mouse
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Trinitrobenzenes