Immune escape as a fundamental trait of cancer: Focus on IDO

Oncogene

Volumn 27, Issue 28, 2008, Pages 3889-3900

  Prendergast, G C ^a,b,c  

^a LANKENAU INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Bin1; IDO2; Immunosuppression; Immunotherapy; Indoleamine 2,3 dioxygenase

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; TRYPTOPHAN;

ADVANCED CANCER; CANCER INHIBITION; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE COURSE; DORMANCY; DRUG EFFICACY; EARLY DIAGNOSIS; GENE INACTIVATION; GENETIC POLYMORPHISM; HUMAN; HUMAN CELL; HUMAN TISSUE; IDO2 GENE; IMMUNE ESCAPE; IMMUNOPATHOLOGY; MALIGNANT TRANSFORMATION; ONCOGENE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL PROLIFERATION; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOTHERAPY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MODELS, BIOLOGICAL; NEOPLASMS; NUCLEAR PROTEINS; POLYMORPHISM, GENETIC; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 46249124461     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.35     Document Type: Review

References (78)

1. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A et al. (2007). Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13: 1050-1059.
2. Balkwill F, Charles KA, Mantovani A. (2005). Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7: 211-217.
3. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJ, Astelbauer F, Miu J et al. (2007). Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene 396: 203-213.
4. Banerjee T, DuHadaway JB, Gaspari P, Sutanto-Ward E, Munn DH, Mellor AL et al. (2008). Antitumor properties of chemopreventive natural product brassinin are based upon inhibition of indoleamine 2,3-dioxygenase (IDO). Oncogene (in press).
5. Bild AH, Turkson J, Jove R. (2002). Cytoplasmic transport of Stat3 by receptor-mediated endocytosis. EMBO J 21: 3255-3263.
6. Blank C, Kuball J, Voelkl S, Wiendl H, Becker B, Walter B et al. (2006). Blockade of PD-L1 (B7-H1) augments human tumor-specific T cell responses in vitro. Int J Cancer 119: 317-327.
7. Bronte V, Zanovello P. (2005). Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5: 641-654.
8. Chang M, Boulden J, Katz JB, Wang L, Meyer TJ, Soler AP et al. (2007a). Bin1 ablation increases susceptibility to cancer during aging, particularly lung cancer. Cancer Res 67: 7605-7612.
9. Chang M, Boulden J, Sutanto-Ward E, Duhadaway JB, Soler AP, Muller AJ et al. (2007b). Bin1 ablation in mammary gland delays tissue remodeling and drives cancer progression. Cancer Res 67: 100-107.
10. Colombo MP, Piconese S. (2007). Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer 7: 880-887.
11. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, WerbZ et al. (1999). Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 13: 1382-1397.
12. Curti A, Pandolfi S, Valzasina B, Aluigi M, Isidori A, Ferri E et al. (2007). Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood 109: 2871-2877.
13. Curtis RE, Rowlings PA, Deeg HJ, Shriner DA, Socie G, Travis LB et al. (1997). Solid cancers after bone marrow transplantation. N Engl J Med 336: 897-904.
14. DuHadaway JB, Du W, Liu A-X, Baker J, Donover PS, Sharp DM et al. (2003). Transformation selective apoptosis by farnesyltransferase inhibitors requires Bin1. Oncogene 22: 3578-3588.
15. DuHadaway JB, Sakamuro D, Ewert DL, Prendergast GC. (2001). Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res 16: 3151-3156.
16. Dunn GP, Old LJ, Schreiber RD. (2004). The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148.
17. Elliott K, Ge K, Du W, Prendergast GC. (2000). The c-Myc-interacting adapter protein Bin1 activates a caspase-independent cell death program. Oncogene 19: 4669-4684.
18. Elliott K, Sakamuro D, Basu A, Du W, Wunner W, Staller P et al. (1999). Bin1 functionally interacts with Myc in cells and inhibits cell proliferation by multiple mechanisms. Oncogene 18: 3564-3573.
19. Engels EA, Wu X, Gu J, Dong Q, Liu J, Spitz MR. (2007). Systematic evaluation of genetic variants in the inflammation pathway and risk of lung cancer. Cancer Res 67: 6520-6527.
20. Fallarino F, Grohmann U, Hwang KW, Orabona C, Vacca C, Bianchi R et al. (2003). Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol 4: 1206-1212.
21. Fallarino F, Grohmann U, Vacca C, Bianchi R, Orabona C, Spreca A et al. (2002). T cell apoptosis by tryptophan catabolism. Cell Death Diff 9: 1069-1077.
22. Fallarino F, Grohmann U, You S, McGrath BC, Cavener DR, Vacca C et al. (2006). 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 176: 6752-6761.
23. Friberg M, Jennings R, Alsarraj M, Dessureault S, Cantor A, Extermann M et al. (2002). Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J Cancer 101: 151-155.
24. Gabrilovich DI. (2007). Molecular mechanisms and therapeutic reversal of immune suppression in cancer. Curr Cancer Drug Targets 7: 1.
25. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C et al. (2006). Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
26. Gaspari P, Banerjee T, Malachowski WP, Muller AJ, Prendergast GC, Duhadaway J et al. (2006). Structure-activity study of brassinin derivatives as indoleamine 2,3-dioxygenase inhibitors. J Med Chem 49: 684-692.
27. Ge K, DuHadaway J, Du W, Herlyn M, Rodeck U, Prendergast GC. (1999). Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc Natl Acad Sci USA 96: 9689-9694.
28. Ge K, DuHadaway J, Sakamuro D, Wechsler-Reya R, Reynolds C, Prendergast GC. (2000a). Losses of the tumor suppressor Bin1 in breast carcinoma are frequent and reflect deficits in a programmed cell death capacity. Int. J Cancer 85: 376-383.
29. Ge K, Minhas F, DuHadaway J, Mao N-C, Wilson D, Sakamuro D et al. (2000b). Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int J Cancer 86: 155-161.
30. Grohmann U, Volpi C, Fallarino F, Bozza S, Bianchi R, Vacca C et al. (2007). Reverse signaling through GITR ligands enables dexamethasone to activate IDO allergy. Nature Med 13: 579-586.
31. Hanahan D, Weinberg RA. (2000). The hallmarks of cancer. Cell 100: 57-70.
32. Hou DY, Muller AJ, Sharma MD, DuHadaway J, Banerjee T, Johnson M et al. (2007). Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res 67: 792-801.
33. Huber S, Schramm C. (2006). TGF-beta and CD4+CD25+ regulatory T cells. Front Biosci 11: 1014-1023.
34. Hunter KW, Crawford NP. (2006). Germ line polymorphism in metastatic progression. Cancer Res 66: 1251-1254.
35. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. (2002). Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 99: 12293-12297.
36. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, Krainer AR. (2007). The gene encoding the splicing factor SF2/ASF is a protooncogene. Nat Struct Mol Biol 14: 185-193.
37. Knoepfler PS, Zhang XY, Cheng PF, Gafken PR, McMahon SB, Eisenman RN. (2006). Myc influences global chromatin structure. EMBO J 25: 2723-2734.
38. Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ et al. (2007). Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450: 903-907.
39. Lewis CE, Pollard JW. (2006). Distinct role of macrophages in different tumor microenvironments. Cancer Res 66: 605-612.
40. Lu LF, Lind EF, Gondek DC, Bennett KA, Gleeson MW, Pino-Lagos K et al. (2006). Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442: 997-1002.
41. Machiels JP, Reilly RT, Emens LA, Ercolini AM, Lei RY, WeintraubD et al. (2001). Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 61: 3689-3697.
42. Mehta RG, Liu J, Constantinou A, Thomas CF, Hawthorne M, YouMet al. (1995). Cancer chemopreventive activity of brassinin, a phytoalexin from cabbage. Carcinogenesis 16: 399-404.
43. Mellor AL, Chandler P, Baban B, Hansen AM, Marshall B, Pihkala J et al. (2004). Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. Int Immunol 16: 1391-1401.
44. Mellor AL, Munn DH. (2004). IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 4: 762-774.
45. Mellor AL, Munn DH. (2008). Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat Rev Immunol 8: 74-80.
46. Mellor AL, Sivakumar J, Chandler P, Smith K, Molina H, Mao D et al. (2001). Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat. Immunol 2: 64-68.
47. Metz R, DuHadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC. (2007). Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor IDO inhibitory compound D-1MT. Cancer Res 67: 7082-7087.
48. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B et al. (2004). APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445-456.
49. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. (2004). Targeted deletion of the suppressor gene Bin1/Amphiphysin2 enhances the malignant character of transformed cells. Cancer Biol Ther 3: 1236-1242.
50. Muller AJ, DuHadaway JB, Sutanto-Ward E, Donover PS, Prendergast GC. (2005a). Inhibition of indoleamine 2,3-dioxygenase, an immunomodulatory target of the tumor suppressor gene Bin1, potentiates cancer chemotherapy. Nature Med 11: 312-319.
51. Muller AJ, Malachowski WP, Prendergast GC. (2005b). Indoleamine 2,3-dioxygenase in cancer: targeting pathological immune tolerance with small-molecule inhibitors. Expert Opin Ther Targets 9: 831-849.
52. Muller AJ, Prendergast GC. (2007). Indoleamine 2,3-dioxygenase in immune suppression and cancer. Curr Cancer Drug Targets 7: 31-40.
53. Muller AJ, Scherle PA. (2006). Targeting the mechanisms of tumoral immune tolerance with small-molecule inhibitors. Nat Rev Cancer 6: 613-625.
54. Munn DH, Mellor AL. (2007). Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 117: 1147-1154.
55. Munn DH, Sharma MD, Baban B, Harding HP, Zhang Y, Ron D et al. (2005). GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22: 633-642.
56. Munn DH, Sharma MD, Hou D, Baban B, Lee JR, Antonia SJ et al. (2004). Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clin Invest 114: 280-290.
57. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B et al. (1998). Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-1193.
58. Muto S, Katsuki M, Horie S. (2007). Decreased c-kit function inhibits enhanced skin carcinogenesis in c-Ha-ras protooncogene transgenic mice. Cancer Sci 98: 1549-1556.
59. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL et al. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13: 54-61.
60. Popovic PJ, Zeh III HJ, Ochoa JB. (2007). Arginine and immunity. J Nutr 137: 1681S-1686 S.
61. Prendergast GC, Jaffee EM. (2007). Cancer immunologists and cancer biologists: why we didn0t talk then but need to now. Cancer Res 67: 3500-3504.
62. Ramalingam A, Farmer GE, Stamato TD, Prendergast GC. (2007). Bin1 interacts with and restrains the DNA end-binding protein complex Ku. Cell Cycle 6: 1914-1918.
63. Ramalingam A, Prendergast GC. (2007). Bin1 homolog hob1 supports a rad6-set1 pathway of transcriptional repression in fission yeast. Cell Cycle 6: 1655-1662.
64. Ren G, Vajjhala P, Lee JS, Winsor B, Munn AL. (2006). The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol Mol Biol Rev 70: 37-120.
65. Rose D, Sheff MD. (1967). Tryptophan metabolism in carcinoma of the breast. Lancet 1: 239-241.
66. Routhier EL, Donover PS, Prendergast GC. (2003). hob1+, the homolog of Bin1 in fission yeast, is dispensable for endocytosis but required for the response to starvation or genotoxic stress. Oncogene 22: 637-648.
67. Roy M, Xu Q, Lee C. (2005). Evidence that public database records for many cancer-associated genes reflect a splice form found in tumors and lack normal splice forms. Nucleic Acids Res 33: 5026-5033.
68. Sakamuro D, Elliott K, Wechsler-Reya R, Prendergast GC. (1996). BIN1 is a novel MYC-interacting protein with features of a tumor suppressor. Nature Genet 14: 69-77.
69. Schlee M, Schuhmacher M, Holzel M, Laux G, Bornkamm GW. (2007). c-MYC impairs immunogenicity of human B cells. Adv Cancer Res 97: 167-188.
70. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ et al. (2001). IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410: 1107-1111.
71. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H et al. (2007). Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest 117: 2570-2582.
72. Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. (2007). Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med 13: 1211-1218.
73. Swensen SJ, Jett JR, Hartman TE, Midthun DE, Mandrekar SJ, Hillman SL et al. (2005). CT screening for lung cancer: five-year prospective experience. Radiology 235: 259-265.
74. Tajiri T, Liu X, Thompson PM, Tanaka S, Suita S, Zhao H et al. (2003). Expression of a MYCN-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features. Clin Cancer Res 9: 3345-3355.
75. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, Parmentier N et al. (2003). Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 9: 1269-1274.
76. Wingender G, Garbi N, Schumak B, Jungerkes F, Endl E, von Bubnoff D et al. (2006). Systemic application of CpG-rich DNA suppresses adaptive T cell immunity via induction of IDO. Eur J Immunol 36: 12-20.
77. Xu Q, Lee C. (2003). Discovery of novel splice forms and functional analysis of cancer-specific alternative splicing in human expressed sequences. Nucleic Acids Res 31: 5635-5643.
78. Zou W. (2005). Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5: 263-274.