Indoleamine 2,3-dioxygenase in intestinal immunity and inflammation

Inflammatory Bowel Diseases

Volumn 15, Issue 9, 2009, Pages 1391-1396

  Cherayil, Bobby J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Inflammation in IBD; Mucosal immunology

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 2; INTERFERON; INTERLEUKIN 17; INTERLEUKIN 4; OXYGENASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVITY; CELL SURVIVAL; ENTERITIS; ENZYME ACTIVITY; GASTROINTESTINAL TRACT; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNITY; IMMUNOREGULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; UPREGULATION; ENZYMOLOGY; IMMUNOLOGY; INTESTINE MUCOSA; PHYSIOLOGY; SMALL INTESTINE; T LYMPHOCYTE SUBPOPULATION;

ENTERITIS; HUMANS; IMMUNITY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTESTINAL MUCOSA; INTESTINE, SMALL; T-LYMPHOCYTE SUBSETS;

EID: 70449727864     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20910     Document Type: Review

References (60)

1. Shimizu T, Nomiyama S, Hirata F, et al. Indoleamine 2,3-dioxygenase. Purification and some properties. J Biol Chem. 1978;253:4700-4706. (Pubitemid 8372084)
2. Tone S, Takikawa O, Habara-Ohkubo A, et al. Primary structure of human indoleamine 2,3-dioxygenase deduced from the nucleotide sequence of its cDNA. Nucleic Acids Res. 1990;18:367.
3. Dai W, Gupta SL. Molecular cloning, sequencing and expression of human interferon-gamma-inducible indoleamine 2,3-dioxygenase cDNA. Biochem Biophys Res Commun. 1990;168:1-8. (Pubitemid 20142577)
4. Habara-Ohkubo A, Takikawa O, Yoshida R. Cloning and expression of a cDNA encoding mouse indoleamine 2,3-dioxygenase. Gene. 1991;105:221-227.
5. Munn DH, Zhou M, Attwood JT, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998;281:1191-1193. (Pubitemid 28406294)
6. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-774.
7. Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest. 2007;117:1147-1154.
8. Metz R, Duhadaway JB, Kamasani U, et al. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the anti-tumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res. 2007;67:7082-7087. (Pubitemid 47206533)
9. Ball HJ, Sanchez-Perez A, Weiser S, et al. Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene. 2007;396:203-213. (Pubitemid 46818792)
10. Thackray SJ, Mowat CG, Chapman SK. Exploring the mechanism of tryptophan 2,3-dioxygenase. Biochem Soc Trans. 2008;36:1120-1123.
11. Munn DH, Sharma MD, Lee JR, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science. 2002;297:1867-1870.
12. Mellor AL, Baban B, Chandler P, et al. Cutting edge: induced indoleamine 2,3-dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol. 2003;171:1652-1655. (Pubitemid 36966447)
13. Adikari SB, Lian H, Link H, et al. IFNγ-modified dendritic cells suppress B cell function and ameliorate the development of experimental autoimmune myasthenia gravis. Clin Exp Immunol. 2004;138:230-236. (Pubitemid 39472438)
14. Munn DH, Sharma MD, Baban B, et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity. 2005;22:633-642. (Pubitemid 40719198)
15. Terness P, Bauer TM, Rose L, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med. 2002;196:447-457. (Pubitemid 34940984)
16. Frumento G, Rotondo R, Tonetti M, et al. Tryptophan-derived catabolites are responsible for inhibition of T and NK cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med. 2002;196:459-468. (Pubitemid 34940985)
17. Romani L, Fallarino F, De Luca A, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature. 2008;451:211-215.
18. Mellor AL, Sivakumar J, Chandler P, et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol. 2001;2:64-68. (Pubitemid 33704955)
19. Gurtner GJ, Newberry RD, Schloemann SR, et al. Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology. 2003;125:1762-1773.
20. Uyttenhove C, Pilotte L, Theate I, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med. 2003;9:1269-1274. (Pubitemid 37279849)
21. Hayashi T, Beck L, Rossetto C, et al. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J Clin Invest. 2004;114:270-279. (Pubitemid 39071632)
22. Bozza S, Fallarino F, Pitzurra L, et al. A crucial role for tryptophan catabolism at the host/Candida albicans interface. J Immunol. 2005;174:2910-2918. (Pubitemid 40279709)
23. Hayaishi O. Properties and function of indoleamine 2,3-dioxygenase. J Biochem (Tokyo). 1976;79:13P-21P.
24. Harrington L, Srikanth CV, Antony R, et al. Deficiency of indoleamine 2,3-dioxygenase enhances commensal-induced antibody responses and protects against Citrobacter rodentium-induced colitis. Infect Immun. 2008;76:3045-3053.
25. Rhee SJ, Walker WA, Cherayil BJ. Developmentally regulated intestinal expression of IFNγ and its target genes and the age-specific response to enteric Salmonella infection. J Immunol. 2005;175:1127-1136.
26. Dieckgraefe BK, Stenson WF, Korzenik JR, et al. Analysis of mucosal gene expression in inflammatory bowel disease by parallel oligonucleotide arrays. Physiol Genomics. 2000;4:1-11.
27. Barcelo-Batliori S, Andre M, Servis C, et al. Proteomic analysis of cytokine-induced proteins in human intestinal epithelial cells: implications for inflammatory bowel diseases. Proteomics. 2002;2:551-560. (Pubitemid 34507345)
28. Mizoguchi E, Xavier RJ, Reinecker HC, et al. Colonic epithelial functional phenotype varies with type and phase of experimental colitis. Gastroenterology. 2003;125:148-161. (Pubitemid 36799116)
29. Wolf AM, Wolf D, Rumpold H, et al. Over-expression of indoleamine 2,3-dioxygenase in human inflammatory bowel disease. Clin Immunol. 2004;113:47-55. (Pubitemid 39468267)
30. Torres MI, Lopez-Casado MA, Lorite P, et al. Tryptophan metabolism and indoleamine 2,3-dioxygenase in celiac disease. Clin Exp Immunol. 2007;148:419-424. (Pubitemid 46701028)
31. Jasperson LK, Bucher C, Panoskaltsis-Mortari A, et al. Indoleamine 2,3-dioxygenase is a critical regulator of acute graft-versus-host disease lethality. Blood. 2008;111:3257-3265.
32. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science. 2004;303:1662-1665. (Pubitemid 38338323)
33. Macpherson AJ. IgA adaptation to the presence of commensal bacteria in the intestine. Curr Top Microbiol Immunol. 2006;308:117-136. (Pubitemid 47400299)
34. Casola S, Rajewsky K. B cell recruitment and selection in mouse GALT germinal centers. Curr Top Microbiol Immunol. 2006;308:155-171. (Pubitemid 47400301)
35. Bos NA, Jiang HQ, Cebra JJ. T cell control of the gut IgA response against commensal bacteria. Gut. 2001;48:762-764.
36. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol. 2004;4:478-485. (Pubitemid 38745559)
37. Backhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science. 2005;307:1915-1920.
38. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol. 2007;19:59-69. (Pubitemid 46810285)
39. Zhu J, Paul WE. CD4 T cells: fates, functions and faults. Blood. 2008;112:1557-1569.
40. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-434. (Pubitemid 47123518)
41. Fallarino F, Grohmann U, You S, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor ζ-chain and induce a regulatory phenotype in naïve T cells. J Immunol. 2006;176:6752-6761.
42. Sharma MD, Baban B, Chandler P, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest. 2007;117:2570-2582. (Pubitemid 47494358)
43. Curti A, Pandolfi S, Valzasina B, et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25-into CD25+ T regulatory cells. Blood. 2007;109:2871-2877.
44. De Luca V, Montagnoli C, Zelante T, et al. Functional yet balanced reactivity to Candida albicans requires TRIF, MyD88 and IDO-dependent inhibition of Rorc. J Immunol. 2007;179:5999-6008.
45. Hill M, Tanguy-Royer S, Royer P, et al. IDO expands human CD4+CD25high regulatory T cells by promoting maturation of LPS-treated dendritic cells. Eur J Immunol. 2007;37:3054-3062. (Pubitemid 350131285)
46. Chen W, Liang X, Peterson AJ, et al. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol. 2008;181:5396-5404.
47. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature. 2006;441:235-238.
48. Zhou L, Lopes JE, Chong MM, et al. TGFβ-induced Foxp3 inhibits Th17 cell differentiation by antagonizing RORγt function. Nature. 2008;453:236-240. (Pubitemid 351667978)
49. Park MJ, Min SY, Park KS, et al. Indoleamine 2,3-dioxygenase-expressing dendritic cells are involved in the generation of CD4+CD25+ regulatory T cells in Peyer's patches in an orally tolerized, collagen-induced arthritis mouse model. Arthritis Res Ther. 2008;10:R11.
50. Romani L, Fallarino F, De Luca A, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature. 2008;451:211-215.
51. Xu H, Oriss TB, Fei M, et al. Indoleamine 2,3-dioxygenase in lung dendritic cells promotes Th2 responses and allergic inflammation. Proc Natl Acad Sci U S A. 2008;105:6690-6695. (Pubitemid 351754568)
52. Platten M, Ho PP, Youssef S, et al. Treatment of autoimmune neuroinflammation with a synthetic tryptophan metabolite. Science. 2005;310:850-855. (Pubitemid 41567343)
53. Veldhoen M, Hirota K, Westendorf AM, et al. The aryl hydrocarbon receptor links Th17-mediated autoimmunity to environmental toxins. Nature. 2008;453:106-109. (Pubitemid 351630329)
54. Quintana FJ, Basso AS, Iglesias AH, et al. Control of Treg and Th17 cell differentiation by the aryl hydrocarbon receptor. Nature. 2008;453:65-71.
55. Denison MS, Nagy SR. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol. 2003;43:309-334.
56. Veldhoen M, Hirota K, Christensen J, et al. Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J Exp Med. 2009;206:43-49.
57. Ivanov II, de Llanos Frutos R, Manel N, et al. Specific microbiota direct the differentiation of IL-17-producing T helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008;4:337-349.
58. Perdew GH, Babbs CF. Production of AhR ligands in rat fecal suspensions containing tryptophan or indole-3-carbinol. Nutr Cancer. 1991;16:209-218.
59. MacKenzie CR, Heseler K, Muller A, et al. Role of indoleamine 2,3-dioxygenase in anti-microbial defence and immunoregulation: tryptophan depletion versus production of toxic kynurenines. Curr Drug Metab. 2007;8:237-244. (Pubitemid 46621673)
60. Costedio MM, Hyman N, Mawe GM. Serotonin and its role in colonic function and in gastrointestinal disorders. Dis Colon Rectum. 2007;50:376-388. (Pubitemid 46394454)