Indoleamine 2,3-dioxygenase regulates anti-tumor immunity in lung cancer by metabolic reprogramming of immune cells in the tumor microenvironment

Oncotarget

Volumn 7, Issue 46, 2016, Pages 75407-75424

  Schafer, Cara C ^a   Wang, Yong ^a   Hough, Kenneth P ^a   Sawant, Anandi ^b   Grant, Stefan C ^a   Thannickal, Victor J ^a   Zmijewski, Jaroslaw ^a   Ponnazhagan, Selvarangan ^b   Deshane, Jessy S ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Combination therapy; Indoleamine 2,3 dioxygenase; Lung cancer; Metabolism; Myeloid derived suppressor cells

Indexed keywords

ANTINEOPLASTIC AGENT; GEMCITABINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INDOLEAMINE 2,3 DIOXYGENASE; MAMMALIAN TARGET OF RAPAMYCIN; PROGRAMMED DEATH 1 LIGAND 1; SUPEROXIDE DISMUTASE MIMETIC; UNCLASSIFIED DRUG; EIF2AK4 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOCOMPETENT CELL; INTRACELLULAR SIGNALING; LUNG CANCER; LYMPHOCYTIC INFILTRATION; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TARGETING; SUPPRESSOR CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOLOGICAL MODEL; DISEASE MODEL; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; KNOCKOUT MOUSE; LUNG TUMOR; METABOLISM; MYELOID-DERIVED SUPPRESSOR CELL; PATHOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; IMMUNOMODULATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LUNG NEOPLASMS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MYELOID-DERIVED SUPPRESSOR CELLS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TOR SERINE-THREONINE KINASES; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84996917607     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12249     Document Type: Article

References (54)

1. Platten M, Wick W and Van den Eynde BJ. Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer research. 2012; 72:5435-5440.
2. Muller AJ, DuHadaway JB, Chang MY, Ramalingam A, Sutanto-Ward E, Boulden J, Soler AP, Mandik-Nayak L, Gilmour SK and Prendergast GC. Non-hematopoietic expression of IDO is integrally required for inflammatory tumor promotion. Cancer immunology, immunotherapy. 2010; 59:1655-1663.
3. Munn DH and Mellor AL. Indoleamine 2, 3-dioxygenase and tumor-induced tolerance. The Journal of clinical investigation. 2007; 117:1147-1154.
4. Schrocksnadel K, Wirleitner B, Winkler C and Fuchs D. Monitoring tryptophan metabolism in chronic immune activation. Clinica chimica acta. 2006; 364:82-90.
5. Kurz K, Schroecksnadel S, Weiss G and Fuchs D. Association between increased tryptophan degradation and depression in cancer patients. Current opinion in clinical nutrition and metabolic care. 2011; 14:49-56.
6. Smith C, Chang MY, Parker KH, Beury DW, DuHadaway JB, Flick HE, Boulden J, Sutanto-Ward E, Soler AP, Laury-Kleintop LD, Mandik-Nayak L, Metz R, Ostrand-Rosenberg S, Prendergast GC and Muller AJ. IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer discovery. 2012; 2:722-735.
7. Wang R and Green DR. Metabolic reprogramming and metabolic dependency in T cells. Immunological reviews. 2012; 249:14-26.
8. Sharma P and Allison JP. The future of immune checkpoint therapy. Science (New York, NY). 2015; 348:56-61.
9. Vanneman M and DranoffG. Combining immunotherapy and targeted therapies in cancer treatment. Nature reviews Cancer. 2012; 12:237-251.
10. Metz R, Rust S, Duhadaway JB, Mautino MR, Munn DH, Vahanian NN, Link CJ and Prendergast GC. IDO inhibits a tryptophan sufficiency signal that stimulates mTOR: A novel IDO effector pathway targeted by D-1-methyl-tryptophan. Oncoimmunology. 2012; 1:1460-1468.
11. Prendergast GC, Smith C, Thomas S, Mandik-Nayak L, Laury-Kleintop L, Metz R and Muller AJ. Indoleamine 2, 3-dioxygenase pathways of pathogenic inflammation and immune escape in cancer. Cancer immunology, immunotherapy. 2014; 63:721-735.
12. Inoki K, Kim J and Guan KL. AMPK and mTOR in cellular energy homeostasis and drug targets. Annual review of pharmacology and toxicology. 2012; 52:381-400.
13. Magnuson B, Ekim B and Fingar DC. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. The Biochemical journal. 2012; 441:1-21.
14. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM and Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molecular cell. 2003; 11:619-633.
15. Sawant A, Schafer CC, Jin TH, Zmijewski J, Tse HM, Roth J, Sun Z, Siegal GP, Thannickal VJ, Grant SC, Ponnazhagan S and Deshane JS. Enhancement of antitumor immunity in lung cancer by targeting myeloid-derived suppressor cell pathways. Cancer research. 2013; 73:6609-6620.
16. Wesolowski R, Markowitz J and Carson WE, 3rd. Myeloid derived suppressor cells-a new therapeutic target in the treatment of cancer. Journal for immunotherapy of cancer. 2013; 1:10.
17. Sharma MD, Baban B, Chandler P, Hou DY, Singh N, Yagita H, Azuma M, Blazar BR, Mellor AL and Munn DH. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2, 3-dioxygenase. The Journal of clinical investigation. 2007; 117:2570-2582.
18. Luo Z, Zang M and Guo W. AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future oncology (London, England). 2010; 6:457-470.
19. Li W, Saud SM, Young MR, Chen G and Hua B. Targeting AMPK for cancer prevention and treatment. Oncotarget. 2015; 6:7365-7378. doi:10.18632/oncotarget.3629.
20. Blagih J, Coulombe F, Vincent EE, Dupuy F, Galicia-Vazquez G, Yurchenko E, Raissi TC, van der Windt GJ, Viollet B, Pearce EL, Pelletier J, Piccirillo CA, Krawczyk CM, Divangahi M and Jones RG. The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo. Immunity. 2015; 42:41-54.
21. Ros S and Schulze A. Balancing glycolytic flux: the role of 6-phosphofructo-2-kinase/fructose 2, 6-bisphosphatases in cancer metabolism. Cancer & metabolism. 2013; 1:8.
22. Faubert B, Vincent EE, Poffenberger MC and Jones RG. The AMP-activated protein kinase (AMPK) and cancer: many faces of a metabolic regulator. Cancer letters. 2015; 356:165-170.
23. Rolf J, Zarrouk M, Finlay DK, Foretz M, Viollet B and Cantrell DA. AMPKalpha1: a glucose sensor that controls CD8 T-cell memory. European journal of immunology. 2013; 43:889-896.
24. Yu J, Du W, Yan F, Wang Y, Li H, Cao S, Yu W, Shen C, Liu J and Ren X. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. Journal of immunology (Baltimore, Md: 1950). 2013; 190:3783-3797.
25. Platten M, von Knebel Doeberitz N, Oezen I, Wick W and Ochs K. Cancer Immunotherapy by Targeting IDO1/TDO and Their Downstream Effectors. Front Immunol. 2014; 5:673.
26. Alizadeh D, Trad M, Hanke NT, Larmonier CB, Janikashvili N, Bonnotte B, Katsanis E and Larmonier N. Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer research. 2014; 74:104-118.
27. Jitschin R, Braun M, Buttner M, Dettmer-Wilde K, Bricks J, Berger J, Eckart MJ, Krause SW, Oefner PJ, Le Blanc K, Mackensen A and Mougiakakos D. CLL-cells induce IDOhi CD14+HLA-DRlo myeloid-derived suppressor cells that inhibit T-cell responses and promote TRegs. Blood. 2014; 124:750-760.
28. Zaidi MR and Merlino G. The two faces of interferon-gamma in cancer. Clinical cancer research. 2011; 17:6118-6124.
29. Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ and Vonderheide RH. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer cell. 2012; 21:822-835.
30. Talmadge JE and Gabrilovich DI. History of myeloid-derived suppressor cells. Nature reviews Cancer. 2013; 13:739-752.
31. Kao J, Ko EC, Eisenstein S, Sikora AG, Fu S and Chen SH. Targeting immune suppressing myeloid-derived suppressor cells in oncology. Critical reviews in oncology/hematology. 2011; 77:12-19.
32. Monu NR and Frey AB. Myeloid-derived suppressor cells and anti-tumor T cells: a complex relationship. Immunological investigations. 2012; 41:595-613.
33. Mellor AL and Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nature reviews Immunology. 2004; 4:762-774.
34. Murakami Y, Hoshi M, Imamura Y, Arioka Y, Yamamoto Y and Saito K. Remarkable role of indoleamine 2, 3-dioxygenase and tryptophan metabolites in infectious diseases: potential role in macrophage-mediated inflammatory diseases. Mediators of inflammation. 2013; 2013:391984.
35. Rao E, Zhang Y, Zhu G, Hao J, Persson XM, Egilmez NK, Suttles J and Li B. Deficiency of AMPK in CD8+ T cells suppresses their anti-tumor function by inducing protein phosphatase-mediated cell death. Oncotarget. 2015; 6:7944-7958. doi:10.18632/oncotarget.3501.
36. Araki K and Ahmed R. AMPK: a metabolic switch for CD8+ T-cell memory. European journal of immunology. 2013; 43:878-881.
37. Yang K and Chi H. AMPK helps T cells survive nutrient starvation. Immunity. 2015; 42:4-6.
38. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
39. Holmgaard RB, Zamarin D, Munn DH, Wolchok JD and Allison JP. Indoleamine 2, 3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. The Journal of experimental medicine. 2013; 210:1389-1402.
40. Fallarino F, Grohmann U and Puccetti P. Indoleamine 2, 3-dioxygenase: from catalyst to signaling function. European journal of immunology. 2012; 42:1932-1937.
41. Ninomiya S, Narala N, Huye L, Yagyu S, Savoldo B, Dotti G, Heslop HE, Brenner MK, Rooney CM and Ramos CA. Tumor indoleamine 2, 3-dioxygenase (IDO) inhibits CD19-CAR T cells and is downregulated by lymphodepleting drugs. Blood. 2015; 125:3905-3916.
42. Khaled YS, Ammori BJ and Elkord E. Myeloid-derived suppressor cells in cancer: recent progress and prospects. Immunology and cell biology. 2013; 91:493-502.
43. Raber P, Ochoa AC and Rodriguez PC. Metabolism of L-arginine by myeloid-derived suppressor cells in cancer: mechanisms of T cell suppression and therapeutic perspectives. Immunological investigations. 2012; 41:614-634.
44. Gabrilovich DI, Ostrand-Rosenberg S and Bronte V. Coordinated regulation of myeloid cells by tumours. Nature reviews Immunology. 2012; 12:253-268.
45. Sim SH, Ahn YO, Yoon J, Kim TM, Lee SH, Kim DW and Heo DS. Influence of chemotherapy on nitric oxide synthase, indole-amine-2, 3-dioxygenase and CD124 expression in granulocytes and monocytes of non-small cell lung cancer. Cancer science. 2012; 103:155-160.
46. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E and Prendergast GC. Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nature medicine. 2005; 11:312-319.
47. Chang CH, Qiu J, O'Sullivan D, Buck MD, Noguchi T, Curtis JD, Chen Q, Gindin M, Gubin MM, van der Windt GJ, Tonc E, Schreiber RD, Pearce EJ and Pearce EL. Metabolic Competition in the Tumor Microenvironment Is a Driver of Cancer Progression. Cell. 2015; 162:1229-1241.
48. Spranger S, Koblish HK, Horton B, Scherle PA, Newton R and Gajewski TF. Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8(+) T cells directly within the tumor microenvironment. Journal for immunotherapy of cancer. 2014; 2:3.
49. Maleki Vareki S, Chen D, Di Cresce C, Ferguson PJ, Figueredo R, Pampillo M, Rytelewski M, Vincent M, Min W, Zheng X and Koropatnick J. IDO Downregulation Induces Sensitivity to Pemetrexed, Gemcitabine, FK866, and Methoxyamine in Human Cancer Cells. PloS one. 2015; 10:e0143435.
50. Zhai L, Spranger S, Binder DC, Gritsina G, Lauing KL, Giles FJ and Wainwright DA. Molecular Pathways: Targeting IDO1 and Other Tryptophan Dioxygenases for Cancer Immunotherapy. Clinical cancer research. 2015; 21:5427-5433.
51. Izbicka E, Wheelhouse RT, Raymond E, Davidson KK, Lawrence RA, Sun D, Windle BE, Hurley LH and Von HoffDD. Effects of cationic porphyrins as G-quadruplex interactive agents in human tumor cells. Cancer research. 1999; 59:639-644.
52. Wang Y, Jin TH, Farhana A, Freeman J, Estell K, Zmijewski JW, Gaggar A, Thannickal VJ, Schwiebert LM, Steyn AJ and Deshane JS. Exposure to cigarette smoke impacts myeloid-derived regulatory cell function and exacerbates airway hyper-responsiveness. Laboratory investigation. 2014; 94:1312-1325.
53. Takikawa O, Kuroiwa T, Yamazaki F and Kido R. Mechanism of interferon-gamma action. Characterization of indoleamine 2, 3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. The Journal of biological chemistry. 1988; 263:2041-2048.
54. Jeong YI, Kim SW, Jung ID, Lee JS, Chang JH, Lee CM, Chun SH, Yoon MS, Kim GT, Ryu SW, Kim JS, Shin YK, Lee WS, Shin HK, Lee JD and Park YM. Curcumin suppresses the induction of indoleamine 2, 3-dioxygenase by blocking the Janus-activated kinase-protein kinase Cdelta-STAT1 signaling pathway in interferon-gamma-stimulated murine dendritic cells. The Journal of biological chemistry. 2009; 284:3700-3708.