Tumoral immune resistance mediated by enzymes that degrade tryptophan

Cancer Immunology Research

Volumn 3, Issue 9, 2015, Pages 978-985

  Baren, Nicolas Van ^a,c   Van Den Eynde, Benoît J ^a,b,c  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^b WELBIO ^*  (Belgium)

^c DE DUVE INSTITUTE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE 2; TRYPTOPHAN 2,3 DIOXYGENASE; UNCLASSIFIED DRUG; INDOLEAMINE 2,3-DIOXYGENASE 1, HUMAN; INDOLEAMINE 2,3-DIOXYGENASE 2, HUMAN; TRYPTOPHAN;

ARTICLE; CANCER IMMUNOLOGY; CATABOLISM; ENZYME DEGRADATION; HUMAN; NONHUMAN; OBSERVATIONAL STUDY; TUMOR IMMUNITY; TUMOR RESISTANCE; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; NEOPLASM; PHYSIOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE;

HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; TRYPTOPHAN; TRYPTOPHAN OXYGENASE; TUMOR ESCAPE;

EID: 84962034404     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0095     Document Type: Article

References (53)

1. Ohaegbulam KC, Assal A, Lazar-Molnar E, Yao Y, Zang X. Human cancer immunotherapy with antibodies to the PD-1 and PD-L1 pathway. Trends Mol Med 2015;21:24-33.
2. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL. Inhibition of T-cell proliferation by macrophage tryptophan catabolism. J Exp Med 1999;189:1363-72.
3. Munn DH, Sharma MD, Baban B, Harding HP, Zhang Y, Ron D, etal. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2, 3-dioxygenase. Immunity 2005;22:633-42.
4. Metz R, Rust S, Duhadaway JB, Mautino MR, Munn DH, Vahanian NN, et al. IDO inhibits a tryptophan sufficiency signal that stimulates mTOR: a novel IDO effector pathway targeted by D-1-methyl-tryptophan. Oncoimmunology 2012;1:1460-8.
5. Fallarino F, Grohmann U, Vacca C, Bianchi R, Orabona C, Spreca A, et al. T-cell apoptosis by tryptophan catabolism. Cell Death Differ 2002;9:1069-77.
6. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T-cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol 2006;176:6752-61.
7. Terness P, Bauer TM, Röse L, Dufter C, Watzlik A, Simon H, 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;196:447-57.
8. Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 2010;185:3190-8.
9. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998;281:1191-3.
10. Mellor AL, Munn DH. Tryptophan catabolism and regulation of adaptive immunity. J Immunol 2003;170:5809-13.
11. Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, Keskin DB, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2, 3-dioxygenase. Science 2002;297:1867-70.
12. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, Parmentier N, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat Med 2003;9:1269-74.
13. Godin-Ethier J, Hanafi LA, Piccirillo CA, Lapointe R. Indoleamine 2, 3-dioxygenase expression in human cancers: clinical and immunologic perspectives. Clin Cancer Res 2011;17:6985-91.
14. Theate I, van Baren N, Pilotte L, Moulin P, Larrieu P, Renauld JC, et al. Extensive profiling of the expression of the indoleamine 2, 3-dioxygenase 1 protein in normal and tumoral human tissues. Cancer Immunol Res 2015;3:161-72.
15. van Baren N, Van den Eynde BJ. Tryptophan-degradingenzymesintumoral immune resistance. Front Immunol 2015;6:34.
16. Blaschitz A, Gauster M, Fuchs D, Lang I, Maschke P, Ulrich D, et al. Vascular endothelial expression of indoleamine 2, 3-dioxygenase 1 forms a positive gradient towards the feto-maternal interface. PLoS ONE 2011;6:e21774.
17. Baban B, Chandler P, McCool D, Marshall B, Munn DH, Mellor AL. Indoleamine 2, 3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J Reprod Immunol 2004;61:67-77.
18. Dai X, Zhu BT. Indoleamine 2, 3-dioxygenase tissue distribution and cellular localization in mice: implications for its biological functions. J Histochem Cytochem 2010;58:17-28.
19. Smith C, Chang MY, Parker KH, Beury DW, Du Hadaway JB, Flick HE, et al. IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov 2012;2:722-35.
20. Sedlmayr P, Blaschitz A, Wintersteiger R, Semlitsch M, Hammer A, MacKenzie CR, et al. Localization of indoleamine 2, 3-dioxygenase in human female reproductive organs and the placenta. Mol Hum Reprod 2002;8:385-91.
21. Orabona C, Pallotta MT, Volpi C, Fallarino F, Vacca C, Bianchi R, et al. SOCS3 drives proteasomal degradation of indoleamine 2, 3-dioxygenase (IDO) and antagonizes IDO-dependent tolerogenesis. Proc Natl Acad Sci U S A 2008;105:20828-33.
22. Pallotta MT, Orabona C, Volpi C, Vacca C, Belladonna ML, Bianchi R, et al. Indoleamine 2, 3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol 2011;12:870-8.
23. Wang Y, Liu H, McKenzie G, Witting PK, Stasch JP, Hahn M, et al. Kynurenine is an endothelium-derived relaxing factor produced during inflammation. Nat Med 2010;16:279-85.
24. Riesenberg R, Weiler C, Spring O, Eder M, Buchner A, Popp T, et al. Expression of indoleamine 2, 3-dioxygenase in tumor endothelial cells correlates with long-term survival of patients with renal cell carcinoma. Clin Cancer Res 2007;13:6993-7002.
25. Lee JR, Dalton RR, Messina JL, Sharma MD, Smith DM, Burgess RE, et al. Pattern of recruitment of immunoregulatory antigen-presenting cells in malignant melanoma. Lab Invest 2003;83:1457-66.
26. Thomas S, DuHadaway J, Prendergast GC, Laury-Kleintop L. Specific in situ detection of murine indoleamine 2, 3-dioxygenase. J Cell Biochem 2014;115:391-6.
27. Knox WE. Two mechanisms which increase in vivo the liver tryptophan peroxidase activity: specific enzyme adaptation and stimulation of the pituitary adrenal system. Br J Exp Pathol 1951;32:462-9.
28. Kanai M, Funakoshi H, Takahashi H, Hayakawa T, Mizuno S, Matsumoto K, et al. Tryptophan 2, 3-dioxygenase is a key modulator of physiological neurogenesis and anxiety-related behavior in mice. Mol Brain 2009;2:8.
29. Bessede A, Gargaro M, Pallotta MT, Matino D, Servillo G, Brunacci C, et al. Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature 2014;511:184-90.
30. Alex Bishop G, Bertolino PD, Bowen DG, McCaughan GW. Tolerance in liver transplantation. Best Pract Res Clin Gastroenterol 2012;26:73-84.
31. Li DD, Gao YJ, Tian XC, Yang ZQ, Cao H, Zhang QL, et al. Differential expression and regulation of Tdo2 during mouse decidualization. J Endocrinol 2014;220:73-83.
32. Pilotte L, Larrieu P, Stroobant V, Colau D, Dolusic E, Frederick R, et al. Reversal of tumoral immune resistance by inhibition of tryptophan 2, 3-dioxygenase. Proc Natl Acad Sci U S A 2012;109:2497-502.
33. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011;478:197-203.
34. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJ, Astelbauer F, Miu J, et al. Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene 2007;396:203-13.
35. Metz R, Duhadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2, 3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res 2007;67:7082-7.
36. Merlo LM, Pigott E, DuHadaway JB, Grabler S, Metz R, Prendergast GC, et al. IDO2 is a critical mediator of autoantibody production and inflammatory pathogenesis in a mouse model of autoimmune arthritis. J Immunol 2014;192:2082-90.
37. Löb S, Konigsrainer A, Zieker D, Brucher BL, Rammensee HG, Opelz G, et al. IDO1 and IDO2 areexpressedinhuman tumors: levo-but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 2008;58:153-7.
38. Witkiewicz AK, Costantino CL, Metz R, Muller AJ, Prendergast GC, Yeo CJ, et al. Genotyping and expression analysis of IDO2 in human pancreatic cancer: a novel, active target. J Am Coll Surg 2009;208:781-7.
39. Heitger A. Regulation of expression and function of IDO in human dendritic cells. Curr Med Chem 2011;18:2222-33.
40. Prendergast GC, Metz R, Muller AJ, Merlo LMF, Mandik-Nayak L. IDO2 in immunomodulation and autoimmune disease. Front Immunol 2014;5:585.
41. Shimizu T, Nomiyama S, Hirata F, Hayaishi O. Indoleamine 2, 3-dioxygenase. Purification and some properties. J Biol Chem 1978;253:4700-6.
42. Pantouris G, Serys M, Yuasa HJ, Ball HJ, Mowat CG. Human indoleamine 2, 3-dioxygenase-2 has substrate specificity and inhibition characteristics distinct from those of indoleamine 2, 3-dioxygenase-1. Amino Acids 2014;46:2155-63.
43. Batabyal D, Yeh S-R. Human tryptophan dioxygenase: a comparison to indoleamine 2, 3-Dioxygenase. J. Am. Chem. Soc. 2007;129:15690-701.
44. Koblish HK, Hansbury MJ, Bowman KJ, Yang G, Neilan CL, Haley PJ, et al. Hydroxyamidine inhibitors of indoleamine-2, 3-dioxygenase potently suppress systemic tryptophan catabolism and the growth of IDO-expressing tumors. Mol Cancer Therap 2010;9:489-98.
45. Li M, Bolduc AR, Hoda MN, Gamble DN, Dolisca SB, Bolduc AK, et al. The indoleamine 2, 3-dioxygenase pathway controls complement-dependent enhancement of chemo-radiation therapy against murine glioblastoma. J Immunother Cancer 2014;2:21.
46. Röhrig U. F, Majjigapu SR, Grosdidier A, Bron S, Stroobant V, Pilotte L, et al. Rational design of 4-Aryl-1, 2, 3-triazoles for indoleamine 2, 3-dioxygenase 1 inhibition. J Med Chem 2012;55:5270-90.
47. Salter M, Hazelwood R, Pogson CI, Iyer Rn Madge DJ. The effects of a novel and selective inhibitor of tryptophan 2, 3-dioxygenase on tryptophan and serotonin metabolism in the rat. Biochem Pharmacol 1995;49:1435-42.
48. Dolusic E, Larrieu P, Moineaux L, Stroobant V, Pilotte L, Colau D, et al. Tryptophan 2, 3-dioxygenase (TDO) inhibitors. 3-(2-(Pyridyl) ethenyl) indoles as potential anticancer immunomodulators. J Med Chem 2011;54:5320-34.
49. Sun T, Chen XH, Tang ZD, Cai J, Wang XY, Wang SC, et al. Novel 1-alkyltryptophan derivatives downregulate IDO1 and IDO2 mRNA expression induced by interferon-gamma in dendritic cells. Mol Cell Biochem 2010;342:29-34.
50. Metz R, Smith C, Du Hadaway JB, Chandler P, Baban B, Merlo LM, et al. IDO2 is critical for IDO1-mediated T-cell regulation and exerts a nonredundant function in inflammation. Int Immunol 2014;26:357-67.
51. Austin CJ, Mailu BM, Maghzal GJ, Sanchez-Perez A, Rahlfs S, Zocher K, et al. Biochemical characteristics and inhibitor selectivity of mouse indoleamine 2, 3-dioxygenase-2. Amino Acids 2010;39:565-78.
52. Watanabe Y, Fujiwara M, Yoshida R, Hayaishi O. Stereospecificity of hepatic Ltryptophan 2, 3-dioxygenase. Biochem J 1980;189:393-405.
53. Fukunaga M, Yamamoto Y, Kawasoe M, Arioka Y, Murakami Y, Hoshi M, et al. Studies on tissue and cellular distribution of indoleamine 2, 3-dioxygenase 2: the absence of IDO1 upregulates IDO2 expression in the epididymis. J Histochem Cytochem 2012;60:854-60.