Indoleamine 2, 3-dioxygenase (IDO): Biology and target in cancer immunotherapies

Current Cancer Drug Targets

Volumn 16, Issue 9, 2016, Pages 755-764

  Selvan, Senthamil R ^a   Dowling, John P ^b   Kelly, William K ^a   Lin, Jianqing ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

3 dioxygenase (IDO); Cancer immunotherapy; Combination therapy; IDO inhibitors; Immune tolerance; Indoleamine 2

Indexed keywords

4 AMINO N (3 CHLORO 4 FLUOROPHENYL) N' HYDROXY 1,2,5 OXADIAZOLE 3 CARBOXIMIDAMIDE; ANTINEOPLASTIC AGENT; DENDRITIC CELL VACCINE; DOCETAXEL; GAMMA INTERFERON; GEMCITABINE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; INDOXIMOD; INTERLEUKIN 6; INTERLEUKIN 8; IPILIMUMAB; MELANOMA VACCINE; METRONIDAZOLE; NLG 919; PACLITAXEL; SIPULEUCEL T; UNCLASSIFIED DRUG; ENZYME INHIBITOR;

CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CHEMICAL STRUCTURE; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; EFFECTOR CELL; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; MELANOMA; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PANCREAS ADENOCARCINOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SUPPRESSOR CELL; TH1 TH2 BALANCE; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; VACCINATION; ANTAGONISTS AND INHIBITORS; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PROCEDURES; TH1 CELL; TH2 CELL;

ENZYME INHIBITORS; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MOLECULAR TARGETED THERAPY; NEOPLASMS; TH1 CELLS; TH2 CELLS; TUMOR MICROENVIRONMENT;

EID: 84995621466     PISSN: 15680096     EISSN: 18735576     Source Type: Journal    
DOI: 10.2174/1568009615666151030102250     Document Type: Review

References (107)

1. Beatty, G.L.; Gladney, W.L. Immune escape mechanisms as a guide for cancer immunotherapy. Clin. Cancer Res., 2015, 21 (4), 687-692.
2. Dunn, G.P.; Old, L.J.; Schreiber, R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity, 2004, 21 (2), 137-148.
3. Ashour, H.M., Niederkorn, J.Y. T cells promote anterior chamberassociated immune deviation and immune privilege through their production of IL-10. J. Immunol., 2006, 177 (12), 8331-8337.
4. Niederkorn, J.Y.; Stevens, C.; Mellon, J.; Mayhew, E. CD4+ Tcell-independent rejection of corneal allografts. Transplantation, 2006, 81 (8), 1171-1178.
5. Malina, H.Z.; Martin, X.D. Indoleamine 2, 3-dioxygenase activity in the aqueous humor, iris/ciliary body, and retina of the bovine eye. Graefes Arch Clin. Exp. Ophthalmol., 1993, 231 (8), 482-486.
6. Malina, H.Z. and X.D. Martin, Indoleamine 2, 3-dioxygenase: antioxidant enzyme in the human eye. Graefes Arch Clin. Exp. Ophthalmol., 1996, 234 (7), 457-462.
7. Bodaghi, B.; Goureau, O.; Zipeto, D.; Laurent, L.; Virelizier, J.L.; Michelson, S. Role of IFN-gamma-induced indoleamine 2, 3 dioxygenase and inducible nitric oxide synthase in the replication of human cytomegalovirus in retinal pigment epithelial cells. J. Immunol., 1999, 162 (2), 957-964.
8. Beutelspacher, S.C.; Pillai, R.; Watson, M.P.; Tan, P.H.; Tsang, J.; McClure, M.O.; George, A.J.; Larkin, D.F. Function of indoleamine 2, 3-dioxygenase in corneal allograft rejection and prolongation of allograft survival by over-expression. Eur. J. Immunol., 2006, 36 (3), 690-700.
9. Serbecic, N.; Beutelspacher S.C. Indoleamine 2, 3-dioxygenase protects corneal endothelial cells from UV mediated damage. Exp. Eye Res., 2006, 82 (3), 416-426.
10. Prendergast, G.C. Immune escape as a fundamental trait of cancer: focus on IDO. Oncogene, 2008, 27 (28), 3889-900.
11. Munn, D.H., et al., Expression of indoleamine 2, 3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest., 2004, 114 (2), 280-290.
12. Fallarino, F.; Grohmann, U.; Vacca, C.; Bianchi, R.; Orabona, C.; Spreca, A.; Fioretti, M.C.; Puccetti, P. T cell apoptosis by tryptophan catabolism. Cell Death Differ, 2002, 9 (10), 1069-1077.
13. Litzenburger, U.M.; Opitz, C.A.; Sahm, F.; Rauschenbach, K.J.; Trump, S.; Winter, M.; Ott, M.; Ochs, K.; Lutz, C.; Liu, X.; Anastasov, N.; Lehmann, I.; Hofer, T.; von Deimling, A.; Wick, W.; Platten, M. Constitutive IDO expression in human cancer is sustained by an autocrine signaling loop involving IL-6, STAT3 and the AHR. Oncotarget, 2014, 5 (4), 1038-1051.
14. van Wissen, M.; Snoek, M.; Smids, B.; Jansen, H.M.; Lutter, R. IFN-gamma amplifies IL-6 and IL-8 responses by airway epithelial-like cells via indoleamine 2, 3-dioxygenase. J. Immunol., 2002, 169 (12), 7039-7044.
15. Mellor, A.L.; Munn D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol., 2004, 4 (10), 762-774.
16. Popov, A.; Schultze J.L. IDO-expressing regulatory dendritic cells in cancer and chronic infection. J. Mol. Med., 2008, 86 (2), p. 145-160.
17. Munn, D.H.; Mellor, A.L. IDO and tolerance to tumors. Trends Mol. Med., 2004, 10 (1), 15-18.
18. Huang, L.; Baban, B.; Johnson, B.A 3rd.; Mellor, A.L. Dendritic cells, indoleamine 2, 3 dioxygenase and acquired immune privilege. Int. Rev. Immunol., 2010, 29 (2), 133-155.
19. Jurgens, B.; Hainz, U.; Fuchs, D.; Felzmann, T.; Heitger, A. Interferon-gamma-triggered indoleamine 2, 3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood, 2009, 114 (15), 3235-3243.
20. von Bergwelt-Baildon, M.S.; Popov, A.; Saric, T.; Chemnitz, J.; Classen S, Stoffel MS, Fiore F, Roth U, Beyer M, Debey S, Wickenhauser C, Hanisch FG, Schultze JL. CD25 and indoleamine 2, 3-dioxygenase are up-regulated by prostaglandin E2 and expressed by tumor-associated dendritic cells in vivo: additional mechanisms of T-cell inhibition. Blood, 2006, 108 (1), 228-237.
21. Carlin, J.M.; Borden, E.C.; Sondel, P.M.; Byrne, G.I. Biologicresponse-modifier-induced indoleamine 2, 3-dioxygenase activity in human peripheral blood mononuclear cell cultures. J. Immunol., 1987, 139 (7), 2414-2418.
22. Lee, S.Y.; Choi, H.K.; Lee, K.J.; Jung, J.Y.; Hur, G.Y.; Jung, K.H.; Kim, J.H.; Shin, C.; Shim, J.J.; In, K.H.; Kang, K.H.; Yoo, S.H. The immune tolerance of cancer is mediated by IDO that is inhibited by COX-2 inhibitors through regulatory T cells. J. Immunother., 2009, 32 (1), 22-28.
23. Shimizu, K.; Nakata, M.; Hirami, Y.; Yukawa, T.; Maeda, A.; Tanemoto, K. Tumor-infiltrating Foxp3+ regulatory T cells are correlated with cyclooxygenase-2 expression and are associated with recurrence in resected non-small cell lung cancer. J. Thorac. Oncol., 2010, 5 (5), 585-590.
24. Taylor, M.W.; Feng, G.S. Relationship between interferon-gamma, indoleamine 2, 3-dioxygenase, and tryptophan catabolism. FASEB J, 1991, 5 (11), 2516-2522.
25. Munn, D.H.; Zhou, M.; Attwood, J.T.; Bondarev, I.; Conway, S.J.; Marshall, B.; Brown, C.; Mellor, A.L. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science, 1998, 281 (5380), p. 1191-1193.
26. Xu, H.; Zhang, G.X.; Ciric, B.; Rostami, A. IDO: a double-edged sword for T (H) 1/T (H) 2 regulation. Immunol Lett., 2008, 121 (1), 1-6.
27. Godin-Ethier, J.; Pelletier, S.; Hanafi, L.A.; Gannon, P.O.; Forget, M.A.; Routy, J.P.; Boulassel, M.R.; Krzemien, U.; Tanguay, S.; Lattouf, J.B.; Arbour, N.; Lapointe, R. Human activated T lymphocytes modulate IDO expression in tumors through Th1/Th2 balance. J. Immunol., 2009, 183 (12), 7752-7760.
28. Scott, G.N.; DuHadaway, J.; Pigott, E.; Ridge, N.; Prendergast, G.C.; Muller, A.J.; Mandik-Nayak, L. The immunoregulatory enzyme IDO paradoxically drives B cell-mediated autoimmunity. J. Immunol., 2009, 182 (12), 7509-7517.
29. Sherin, P.S., et al., Ultrafast excited-state dynamics of kynurenine, a UV filter of the human eye. J. Phys. Chem. B., 2009, 113 (14), 4953-4962.
30. Muller, A.J.; DuHadaway, J.B.; Donover, P.S.; Sutanto-Ward, E.; Prendergast, G.C. Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat. Med., 2005, 11 (3), p. 312-9.
31. Prendergast, G.C.; Muller, A.J.; Ramalingam, A.; Chang, M.Y. BAR the door: cancer suppression by amphiphysin-like genes. Biochim. Biophys. Acta, 2009, 1795 (1), 25-36.
32. Muller, A.J.; DuHadaway, J.B.; Chang, M.Y.; Ramalingam A, Sutanto-Ward E, Boulden J, Soler AP, Mandik-Nayak L, Gilmour SK, Prendergast GC. Non-hematopoietic expression of IDO is integrally required for inflammatory tumor promotion. Cancer Immunol. Immunother., 2010, 59 (11), 1655-1663.
33. Metz, R.; Duhadaway, J.B.; Kamasani, U.; Laury-Kleintop, L.; Muller, A.J.; Prendergast, G.C. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2, 3-dioxygenase inhibitory compound D-1-methyltryptophan. Cancer Res., 2007, 67 (15), 7082-7087.
34. Lob, S.; Konigsrainer, A.; Schafer, R.; Rammensee, H.G.; Opelz, G.; Terness, P. Levo-but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood, 2008, 111 (4), 2152-2154.
35. Colonna, M.; Trinchieri, G.; Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol., 2004, 5 (12), 1219-1226.
36. Elkord, E., et al., T regulatory cells in cancer: recent advances and therapeutic potential. Expert Opin. Biol. Ther., 2010. 10 (11), 1573-1586.
37. Mansfield, A.S.; Heikkila, P.S.; Vaara, A.T.; von Smitten, K.A.; Vakkila, J.M.; Leidenius, M.H. Simultaneous Foxp3 and IDO expression is associated with sentinel lymph node metastases in breast cancer. BMC Cancer, 2009, 9, 231.
38. Aruga, T.; Suzuki, E.; Saji, S.; Horiguchi, S.; Horiguchi, K.; Sekine, S.; Kitagawa, D.; Funata, N.; Toi, M.; Sugihara, K.; Kuroi, K. A low number of tumor-infiltrating FOXP3-positive cells during primary systemic chemotherapy correlates with favorable antitumor response in patients with breast cancer. Oncol. Rep., 2009, 22 (2), 273-278.
39. Salama, P.; Phillips, M.; Grieu, F.; Morris, M.; Zeps, N.; Joseph, D.; Platell, C.; Iacopetta, B. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol., 2009, 27 (2), 186-192.
40. Liyanage, U.K.; Moore, T.T.; Joo, H.G.; Tanaka, Y.; Herrmann, V.; Doherty, G.; Drebin, J.A.; Strasberg, S.M.; Eberlein, T.J.; Goedegebuure, P.S.; Linehan, D.C. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol., 2002, 169 (5), 2756-2761.
41. Viguier, M.; Lemaitre, F.; Verola, O.; Cho, M.S.; Gorochov, G.; Dubertret, L.; Bachelez, H.; Kourilsky, P.; Ferradini, L. Foxp3 expressing CD4+CD25 (high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol., 2004, 173 (2), 1444-1453.
42. Sasada, T.; Kimura, M.; Yoshida, Y.; Kanai, M.; Takabayashi, A. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer, 2003, 98 (5), 1089-1099.
43. Ichihara, F.; Kono, K.; Takahashi, A.; Kawaida, H.; Sugai, H.; Fujii, H. Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin. Cancer Res., 2003, 9 (12), 4404-4408.
44. Curiel, T.J.; Coukos, G.; Zou, L.; Alvarez, X.; Cheng, P.; Mottram, P.; Evdemon-Hogan, M.; Conejo-Garcia, J.R.; Zhang, L.; Burow, M.; Zhu, Y.; Wei, S.; Kryczek, I.; Daniel, B.; Gordon, A.; Myers, L.; Lackner, A.; Disis, M.L.; Knutson, K.L.; Chen, L.; Zou, W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med., 2004, 10 (9), 942-949.
45. Schaefer, C.; Kim, G.G.; Albers, A.; Hoermann, K.; Myers, E.N.; Whiteside, T.L. Characteristics of CD4+CD25+ regulatory T cells in the peripheral circulation of patients with head and neck cancer. Br. J. Cancer, 2005, 92 (5), 913-920.
46. Kryczek, I., et al., FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res., 2009, 69 (9), 3995-4000.
47. Kryczek, I.; Liu, R.; Wang, G.; Wu, K.; Shu, X.; Szeliga, W.; Vatan, L.; Finlayson, E.; Huang, E.; Simeone, D.; Redman, B.; Welling, TH.; Chang, A.; Zou, W. Tumor antigen-specific FOXP3+ CD4 T cells identified in human metastatic melanoma: peptide vaccination results in selective expansion of Th1-like counterparts. Cancer Res., 2009, 69 (20), 8085-8093.
48. Woo, E.Y.; Yeh, H.; Chu, C.S.; Schlienger, K.; Carroll, R.G.; Riley, J.L.; Kaiser, L.R.; June, C.H. Cutting edge: Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J. Immunol., 2002, 168 (9), 4272-4276.
49. Li, L.; Chao, Q.G.; Ping, L.Z.; Xue, C.; Xia, Z.Y.; Qian, D.; Shiang, H. The prevalence of FOXP3+ regulatory T-cells in peripheral blood of patients with NSCLC. Cancer Biother. Radiopharm., 2009, 24 (3), 357-367.
50. Petersen, R.P.; Campa, M.J.; Sperlazza, J.; Conlon, D.; Joshi, M.B.; Harpole, D.H. Jr.; Patz, E.F. Jr. Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer, 2006, 107 (12), 2866-2872.
51. Gobert, M.; Treilleux, I.; Bendriss-Vermare, N.; Bachelot, T.; Goddard-Leon, S.; Arfi, V.; Biota, C.; Doffin, A.C.; Durand, I.; Olive, D.; Perez, S.; Pasqual, N.; Faure, C.; Ray-Coquard, I.; Puisieux, A.; Caux, C.; Blay, J.Y.; Menetrier-Caux, C. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res., 2009, 69 (5), 2000-2009.
52. Mougiakakos, D.; Johansson, C.C.; Trocme, E.; All-Ericsson, C.; Economou, M.A.; Larsson, O.; Seregard, S.; Kiessling, R. Intratumoral forkhead box P3-positive regulatory T cells predict poor survival in cyclooxygenase-2-positive uveal melanoma. Cancer, 2010, 116 (9), 2224-2233.
53. Yuan, X.L.; Chen, L.; Li, M.X.; Dong, P.; Xue, J.; Wang, J.; Zhang, T.T.; Wang, X.A.; Zhang, F.M.; Ge, H.L.; Shen, L.S.; Xu, D. Elevated expression of Foxp3 in tumor-infiltrating Treg cells suppresses T-cell proliferation and contributes to gastric cancer progression in a COX-2-dependent manner. Clin. Immunol., 2010, 134 (3), 277-288.
54. Brody, J.R.; Costantino, C.L.; Berger, A.C.; Sato, T.; Lisanti, M.P.; Yeo, C.J.; Emmons, R.V.; Witkiewicz, A.K. Expression of indoleamine 2, 3-dioxygenase in metastatic malignant melanoma recruits regulatory T cells to avoid immune detection and affects survival. Cell Cycle, 2009, 8 (12), 1930-1934.
55. Mezrich, J.D.; Fechner, J.H.; Zhang, X.; Johnson, B.P.; Burlingham, W.J.; Bradfield, C.A. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J. Immunol., 2010, 185 (6), 3190-3198.
56. Munn, D.H.; Mellor, A.L. Indoleamine 2, 3-dioxygenase and tumorinduced tolerance. J. Clin. Invest., 2007, 117 (5), 1147-1154.
57. Sharma, M.D.; Baban, B.; Chandler, P.; Hou, D.Y.; Singh, N.; Yagita, H.; Azuma, M.; Blazar, BR.; Mellor, A.L.; Munn, D.H. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2, 3-dioxygenase. J. Clin. Invest., 2007, 117 (9), 2570-2582.
58. Strauss, L.; Bergmann, C.; Szczepanski, M.; Gooding, W.; Johnson, J.T.; Whiteside, T.L. A unique subset of CD4+CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin. Cancer Res., 2007, 13 (15 Pt 1), 4345-4354.
59. Fallarino, F.; Grohmann, U.; Hwang, K.W.; Orabona, C.; Vacca, C.; Bianchi, R.; Belladonna, M.L.; Fioretti, M.C.; Alegre, M.L.; Puccetti, P. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol., 2003, 4 (12), p. 1206-1212.
60. Onodera, T.; Jang, M.H.; Guo, Z.; Yamasaki, M.; Hirata, T.; Bai, Z.; Tsuji, N.M.; Nagakubo, D.; Yoshie, O.; Sakaguchi, S.; Takikawa, O.; Miyasaka, M. Constitutive expression of IDO by dendritic cells of mesenteric lymph nodes: functional involvement of the CTLA-4/B7 and CCL22/CCR4 interactions. J. Immunol., 2009, 183 (9), 5608-5614.
61. Sistigu, A.; Viaud, S.; Chaput, N.; Bracci, L.; Proietti, E.; Zitvogel, L. Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Semin. Immunopathol., 2011, 33 (4), 369-83.
62. Kiessling, R., Klein, E.; Wigzell, H. "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur. J. Immunol., 1975, 5 (2), 112-117.
63. Cerwenka, A.; Lanier, L.L. Natural killer cells, viruses and cancer. Nat. Rev. Immunol., 2001, 1 (1), p. 41-49.
64. Montelli, T.C.; Peracoli, M.T.; Gabarra, R.C.; Soares, A.M.; Kurokawa, C.S. Familial cancer: depressed NK-cell cytotoxicity in healthy and cancer affected members. Arq Neuropsiquiatr, 2001, 59 (1), p. 6-10.
65. Bauernhofer, T.; Kuss, I.; Henderson, B.; Baum, A.S.; Whiteside, T.L. Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur. J. Immunol., 2003, 33 (1), 119-124.
66. Ino, K. Indoleamine 2, 3-dioxygenase and immune tolerance in ovarian cancer. Curr. Opin. Obstet. Gynecol., 2011, 23 (1), 13-18.
67. Zhu, L.Y.; Zhou, J.; Liu, Y.Z.; Pan, W.D. Prognostic significance of natural killer cell infiltration in hepatocellular carcinoma. Ai Zheng, 2009, 28 (11), 1198-1202.
68. Hsia, J.Y.; Chen, J.T.; Chen, C.Y.; Hsu, C.P.; Miaw, J.; Huang, Y.S.; Yang, C.Y. Prognostic significance of intratumoral natural killer cells in primary resected esophageal squamous cell carcinoma. Chang Gung Med. J., 2005, 28 (5), 335-340.
69. Takanami, I.; Takeuchi, K.; Giga, M. The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. J. Thorac. Cardiovasc. Surg., 2001, 121 (6), 1058-1063.
70. Villegas, F.R.; Coca, S.; Villarrubia, V.G.; Jimenez, R.; Chillon, M.J.; Jareno, J.; Zuil, M.; Callol, L. Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer, 2002, 35 (1), 23-28.
71. Hayakawa, K.; Salmeron, M.A.; Parkinson, D.R.; Markowitz, A.B.; von Eschenbach, A.C.; Legha, S.S.; Balch, C.M.; Ross, M.I.; Augustus, L.B.; Itoh, K. Study of tumor-infiltrating lymphocytes for adoptive therapy of renal cell carcinoma (RCC) and metastatic melanoma: sequential proliferation of cytotoxic natural killer and noncytotoxic T cells in RCC. J. Immunother., (1991), 1991, 10 (5), 313-325.
72. Azogui, O.; Avril, M.F.; Margulis, A.; Guillard, M.; Caillou, B.; Prade, M. Tumor-infiltrating CD3-NK cells are more effective than CD3+ T cells in killing autologous melanoma cells. J. Invest. Dermatol., 1991, 97 (3), 425-429.
73. Ma, D.; Luyten, G.P.; Luider, T.M.; Niederkorn, J.Y. Relationship between natural killer cell susceptibility and metastasis of human uveal melanoma cells in a murine model. Invest. Ophthalmol. Vis. Sci., 1995, 36 (2), 435-441.
74. Maat, W.; van der Slik, A.R.; Verhoeven, D.H.; Alizadeh, B.Z.; Ly, L.V.; Verduijn, W.; Luyten, G.P.; Mulder, A.; van Hall, T.; Koning, F.; Jager, M.J.; van Bergen, J. Evidence for natural killer cell-mediated protection from metastasis formation in uveal melanoma patients. Invest. Ophthalmol. Vis. Sci., 2009, 50 (6), 2888-2895.
75. Harning, R.; Koo, G.C.; Szalay, J. Regulation of the metastasis of murine ocular melanoma by natural killer cells. Invest. Ophthalmol. Vis. Sci., 1989, 30 (9), 1909-1915.
76. Werneck, M.B.; Lugo-Villarino, G.; Hwang, E.S.; Cantor, H.; Glimcher, L.H. T-bet plays a key role in NK-mediated control of melanoma metastatic disease. J. Immunol., 2008, 180 (12), 8004-8010.
77. Brandau, S.; Riemensberger, J.; Jacobsen, M.; Kemp, D.; Zhao, W.; Zhao, X.; Jocham, D.; Ratliff, T.L.; Bohle, A. NK cells are essential for effective BCG immunotherapy. Int. J. Cancer, 2001, 92 (5), 697-702.
78. Smyth, M.J.; Cretney, E.; Kershaw, M.H.; Hayakawa, Y. Cytokines in cancer immunity and immunotherapy. Immunol. Rev., 2004, 202, 275-293.
79. Selvan, S.; Dowling, J. “Adherent” versus other isolation strategies for expanding purified, potent and activated human NK cells for Cancer Immunotherapy. Biomed. Res. Int., 2015, 869547.
80. Frumento, G.; Rotondo, R.; Tonetti, M.; Damonte, G.; Benatti, U.; Ferrara, G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2, 3-dioxygenase. J. Exp. Med., 2002, 196 (4), 459-468.
81. Della Chiesa, M.; Carlomagno, S.; Frumento, G.; Balsamo, M.; Cantoni, C.; Conte, R.; Moretta, L.; Moretta, A.; Vitale, M. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46-and NKG2D-activating receptors and regulates NK-cell function. Blood, 2006, 108 (13), 4118-4125.
82. Spaggiari, G.M.; Capobianco, A.; Abdelrazik, H.; Becchetti, F.; Mingari, M.C.; Moretta, L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood, 2008, 111 (3), 1327-1333.
83. Wang, C.; Tay, S.S.; Tran, G.T.; Hodgkinson, S.J.; Allen, R.D.; Hall, B.M.; McCaughan, G.W.; Sharland, A.F.; Bishop, G.A. Donor IL-4-treatment induces alternatively activated liver macrophages and IDO-expressing NK cells and promotes rat liver allograft acceptance. Transpl. Immunol., 2010, 22 (3-4), 172-178.
84. Gabrilovich, D.I.; Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol., 2009, 9 (3), 162-174.
85. Bronte, V.; P. Zanovello. Regulation of immune responses by Larginine metabolism. Nat. Rev. Immunol., 2005. 5 (8), p. 641-654.
86. Cripps, J.G.; Wang, J.; Maria, A.; Blumenthal, I.; Gorham, J.D. Type 1 T helper cells induce the accumulation of myeloid-derived suppressor cells in the inflamed Tgfb1 knockout mouse liver. Hepatology, 2010, 52 (4), 1350-1359.
87. Diaz-Montero, C.M.; Salem, M.L.; Nishimura, M.I.; Garrett-Mayer, E.; Cole, D.J.; Montero, A.J. Increased circulating myeloidderived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother., 2009, 58 (1), 49-59.
88. Ilkovitch, D.; Lopez, D.M. The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression. Cancer Res., 2009, 69 (13), 5514-5521.
89. Ellis, L.M.; Hicklin, D.J. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat. Rev. Cancer, 2008, 8 (8), p. 579-591.
90. Yang, L.; Huang, J.; Ren, X.; Gorska, A.E.; Chytil, A.; Aakre, M.; Carbone, D.P.; Matrisian, L.M.; Richmond, A.; Lin, P.C.; Moses, H.L. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell, 2008, 13 (1), 23-35.
91. Serafini, P.; Mgebroff, S.; Noonan, K.; Borrello, I. Myeloidderived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res., 2008, 68 (13), 5439-5449.
92. Marigo, I.; Dolcetti, L.; Serafini, P.; Zanovello, P.; Bronte, V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev., 2008, 222, 162-179.
93. Lechner, M.G.; Liebertz, D.J.; Epstein, A.L. Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol., 2010, 185 (4), 2273-2284.
94. Lechner, M.G.; Megiel, C.; Russell, S.M.; Bingham, B.; Arger, N.; Woo, T.; Epstein, A.L. Functional characterization of human Cd33+ And Cd11b+ myeloid-derived suppressor cell subsets induced from peripheral blood mononuclear cells co-cultured with a diverse set of human tumor cell lines. J. Transl. Med., 2011, 9, 90.
95. Jia, W.; Jackson-Cook, C.; Graf, M.R. Tumor-infiltrating, myeloidderived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma + vaccination model. J. Neuroimmunol., 2010, 223 (1-2), 20-30.
96. Astigiano, S.; Morandi, B.; Costa, R.; Mastracci, L.; D'Agostino, A.; Ratto, G.B.; Melioli, G.; Frumento, G. Eosinophil granulocytes account for indoleamine 2, 3-dioxygenase-mediated immune escape in human non-small cell lung cancer. Neoplasia, 2005, 7 (4), 390-396.
97. Li, H.; Han, Y.; Guo, Q.; Zhang, M.; Cao, X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J. Immunol., 2009, 182 (1), 240-249.
98. Muller, A.J.; Prendergast, G.C. Indoleamine 2, 3-dioxygenase in immune suppression and cancer. Curr. Cancer Drug Targ., 2007, 7 (1), 31-40.
99. Geiger, J.D.; Hutchinson, R.J.; Hohenkirk, L.F.; McKenna, E.A.; Yanik, G.A.; Levine, J.E.; Chang, A.E.; Braun, T.M.; Mule, J.J. Vaccination of pediatric solid tumor patients with tumor lysatepulsed dendritic cells can expand specific T cells and mediate tumor regression. Cancer Res., 2001, 61 (23), 8513-8519.
100. Theoret, M.R.; Arlen, P.M.; Pazdur, M.; Dahut, W.L.; Schlom, J.; Gulley, J.L. Phase I trial of an enhanced prostate-specific antigenbased vaccine and anti-CTLA-4 antibody in patients with metastatic androgen-independent prostate cancer. Clin. Genitourin Cancer, 2007, 5 (5), 347-350.
101. Gulley, J.L.; Arlen, P.M.; Madan, R.A.; Tsang, K.Y.; Pazdur, M.P.; Skarupa, L.; Jones, J.L.; Poole, D.J.; Higgins, J.P.; Hodge, J.W.; Cereda, V.; Vergati, M.; Steinberg, S.M.; Halabi, S.; Jones, E.; Chen, C.; Parnes, H.; Wright, J.J.; Dahut, W.L.; Schlom, J. Immunologic and prognostic factors associated with overall survival employing a poxviral-based PSA vaccine in metastatic castrate-resistant prostate cancer. Cancer Immunol. Immunother., 2010, 59 (5), 663-674.
102. Ridolfi, L.; Petrini, M.; Fiammenghi, L.; Granato, A.M.; Ancarani, V.; Pancisi, E.; Scarpi, E.; Guidoboni, M.; Migliori, G.; Sanna, S.; Tauceri, F.; Verdecchia, G.M.; Riccobon, A.; Valmorri, L.; Ridolfi, R. Unexpected high response rate to traditional therapy after dendritic cell-based vaccine in advanced melanoma: update of clinical outcome and subgroup analysis. Clin. Dev. Immunol., 2010, 504979.
103. Rosenberg, S.A.; Yang, J.C.; Restifo, N.P. Cancer immunotherapy: moving beyond current vaccines. Nat. Med., 2004, 10 (9), 909-915.
104. Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer, 2005, 5 (4), 263-274.
105. Jia Y, Wang H, Wang Y, Wang T, Wang M, Ma M, Duan Y, Meng X, Liu L. Low expression of Bin1, along with high expression of IDO in tumor tissue and draining lymph nodes, are predictors of poor prognosis for esophageal squamous cell cancer patients. Int. J. Cancer, 2015, 137 (5), 1095-1106
106. Wainwright, D.A.; Balyasnikova, I.V.; Chang, A.L.; Ahmed, A.U.; Moon, K.S.; Auffinger, B.; Tobias, A.L.; Han, Y.; Lesniak, M.S. IDO expression in brain tumors increases the recruitment of regulatory T cells and negatively impacts survival. Clin. Cancer Res., 2012, 18 (22), 6110-6121.
107. Karanikas, V.; Zamanakou, M.; Kerenidi, T.; Dahabreh, J.; Hevas, A.; Nakou, M.; Gourgoulianis, K.I.; Germenis, A.E. Indoleamine 2, 3-dioxygenase (IDO) expression in lung cancer. Cancer Biol. Ther., 2007, 6 (8), 1258-1262.