The emerging "Hallmarks" of metabolic reprogramming and immune evasion: Distinct or linked?

Cancer Research

Volumn 73, Issue 9, 2013, Pages 2737-2742

  Kareva, Irina ^a   Hahnfeldt, Philip ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ACIDIFICATION; AEROBIC METABOLISM; ANTIGEN PRESENTING CELL; CELL EXPANSION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; PH; PRIORITY JOURNAL; REVIEW; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; UPREGULATION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, NEOPLASM; GLYCOLYSIS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOTHERAPY; INTERFERON-GAMMA; NEOPLASMS; TUMOR ESCAPE; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877728919     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3696     Document Type: Review

References (60)

1. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
2. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23: 549-55.
3. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009;27:451-83.
4. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
5. Ruffell B, DeNardo DG, Affara NI, Coussens LM. Lymphocytes in cancer development: polarization towards pro-tumor immunity. Cytokine Growth Factor Rev 2010;21:3-10.
6. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006;6: 24-37.
7. Murphy K, Travers P, Walport M. Janeway's immunobiology. 7th ed. New York and London: Garland Science, Taylor & Francis Group; 2007.
8. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 2001;166:678-89.
9. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin- cyclophosphamide chemotherapy. Cancer Immunol Immunother 2009;58:49-59.
10. Weinberg F, Chandel NS. Mitochondrial metabolism and cancer. Ann N Y Acad Sci 2009;1177:66-73.
11. Fox CJ, Hammerman PS, Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 2005;5:844-52.
12. Greiner EF, Guppy M, Brand K. Glucose is essential for proliferation and the glycolytic enzyme induction that provokes a transition to glycolytic energy production. J Biol Chem 1994;269:31484-90.
13. Brand K, Aichinger S, Forster S, Kupper S, Neumann B, Nürnberg W, et al. Cell-cycle-related metabolic and enzymatic events in proliferating rat thymocytes. Eur J Biochem 1988;172:695-702.
14. MacIver NJ, Jacobs SR, Wieman HL, Wofford JA, Coloff JL, Rathmell JC. Glucose metabolism in lymphocytes is a regulated process with significant effects on immune cell function and survival. J Leukoc Biol 2008;84:949-57.
15. Ganapathy V, Thangaraju M, Prasad PD. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol Ther 2009;121:29-40.
16. Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ, et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010;115:4742-9.
17. Semenza GL. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin Cancer Biol 2009;19:12-6.
18. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010;29:625-34.
19. Harris AL. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47.
20. Mekhail K, Gunaratnam L, Bonicalzi ME, Lee S. HIF activation by pHdependent nucleolar sequestration of VHL. Nat Cell Biol 2004;6:642-7.
21. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891-9.
22. Norian LA, Rodriguez PC, O'Mara LA, Zabaleta J, Ochoa AC, Cella M, et al. Tumor-infiltrating regulatory dendritic cells inhibit CD8? T cell function via L-arginine metabolism. Cancer Res 2009;69:3086-94.
23. Harari O, Liao JK. Inhibition ofMHC II gene transcription by nitric oxide and antioxidants. Curr Pharm Des 2004;10:893-8.
24. Bogdan C. Regulation of lymphocytes by nitric oxide. Methods Mol Biol 2011;677:375-93.
25. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8?T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol 2004;172:989-99.
26. Erratum in: J Immunol. 2004 Apr 1;172:4647.
27. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, et al. HIF- 1a regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 2010;207: 2439-53.
28. Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res 2010;70:7465-75.
29. Kim WY, KaelinWG.Role ofVHL gene mutation in human cancer. J Clin Oncol 2004;22:4991-5004.
30. Schoenborn JR, Wilson CB. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 2007;96:41-101.
31. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferon- gamma: implications for immune responses and autoimmune diseases. Immunity 2009;31:539-50.
32. Enzler T, Gillessen S, Manis JP, Ferguson D, Fleming J, Alt FW, Mihm M, Dranoff G. Deficiencies of GM-CSF and interferon gamma link inflammation and cancer. J Exp Med 2003;197:1213-9.
33. Raes G, Beschin A, Ghassabeh GH, De Baetselier P. Alternatively activated macrophages in protozoan infections. Curr Opin Immunol 2007;19:454-9.
34. Nathan I, Groopman JE, Quan SG, Bersch N, Golde DW. Immune (gamma) interferon produced by a human T-lymphoblast cell line. Nature 1981;292:842-4.
35. Barth RJ Jr, Mule JJ, Spiess PJ, Rosenberg SA. Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8? tumor-infiltrating lymphocytes. J Exp Med 1991;173: 647-58.
36. Heming TA, Dave SK, Tuazon DM, Chopra AK, Peterson JW, Bidani A. Effects of extracellular pH on tumour necrosis factor-alpha production by resident alveolar macrophages. Clin Sci (Lond) 2001;101:267-74.
37. Lardner A. The effects of extracellular pH on immune function. J Leukoc Biol 2001;69:522-30.
38. Lopez DH, Trevani AS, Salamone G, Andonegui G, Raiden S, Giordano M, et al. Acidic pH increases the avidity of FcgammaR for immune complexes. Immunology 1999;98:450-5.
39. Hammer CH, Hänsch G, Gresham HD, Shin ML. Activation of the fifth and sixth components of the human complement system: C6-dependent cleavage of C5 in acid and the formation of a bimolecular lytic complex, C5b,6a. J Immunol 1983;131:892-8.
40. Fishelson Z, Horstmann RD, Müller-Eberhard HJ. Regulation of the alternative pathway of complement by pH. J Immunol 1987;138: 3392-5.
41. Emeis M, Sonntag J, Willam C, Strauss E, Walka MM, Obladen M. Acidosis activates complement system in vitro. Mediators Inflamm 1998;7:417-20.
42. Sonntag J, Emeis M, Strauss E, Obladen M. In vitro activation of complement and contact systemby lactic acidosis. Mediators Inflamm 1998;7:49-51.
43. Martínez D, Vermeulen M, Trevani A, Ceballos A, Sabatte J, Gamberale R, et al. Extracellular acidosis induces neutrophil activation by a mechanism dependent on activation of phosphatidylinositol 3- kinase/Akt and ERK pathways. J Immunol 2006;176:1163-71.
44. Zhang J, Koh J, Lu J, Thiel S, Leong BS, Sethi S, et al. Local inflammation induces complement crosstalk which amplifies the antimicrobial response. PLoS Pathog 2009;5:e1000282.
45. Trevani AS, Andonegui G, Giordano M, Lopez DH, Gamberale R, Minucci F, et al. Extracellular acidification induces human neutrophil activation. J Immunol 1999;162:4849-57.
46. Tong J, Wu WN, Kong X, Wu PF, Tian L, Du W, et al. Acid-sensing ion channels contribute to the effect of acidosis on the function of dendritic cells. J Immunol 2011;186:3686-92.
47. Vermeulen M, Giordano M, Trevani AS, Sedlik C, Gamberale R, Fernandez-Calotti P, et al. Acidosis improves uptake of antigens and MHC class I-restricted presentation by dendritic cells. J Immunol 2004;172:3196-204.
48. Martínez D, Vermeulen M, von Euw E, Sabatte J, Maggíni J, Ceballos A, et al. Extracellular acidosis triggers the maturation of human dendritic cells and the production of IL-12. J Immunol 2007;179:1950-9.
49. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
50. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 2006;66:8927-30.
51. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
52. Warburg O. On the origin of cancer cells. Science 1956;123:309-14.
53. Almog N. Molecular mechanisms underlying tumor dormancy. Cancer Lett 2010;294:139-46.
54. Bragado P, Sosa MS, Keely P, Condeelis J, Aguirre-Ghiso JA. Microenvironments dictating tumor cell dormancy. Recent Results Cancer Res 2012;195:25-39.
55. Thompson ED, Enriquez HL, Fu YX, Engelhard VH. Tumor masses support naive T cell infiltration, activation, and differentiation into effectors. J Exp Med 2010;207:1791-804.
56. Gillies RJ, Robey I, Gatenby RA. Causes and consequences of increased glucose metabolism of cancers. J Nucl Med 2008;49 Suppl 2:24S-42S.
57. Lesterhuis WJ, Haanen JB, Punt CJ. Cancer immunotherapy-revisited. Nat Rev Drug Discov 2011;10:591-600.
58. Melief CJ. Cancer immunotherapy by dendritic cells. Immunity 2008;29:372-83.
59. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006;314:126-9.
60. Nowak AK, Robinson BW, Lake RA. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res 2003;63:4490-6.