Molecular pathways: Hypoxia response in immune cells fighting or promoting cancer

Clinical Cancer Research

Volumn 18, Issue 5, 2012, Pages 1207-1213

  Palazón, Asis ^a,b   Aragonés, Julián ^c   Morales Kastresana, Aizea ^a,b   Ortiz De Landázuri, Manuel ^c   Melero, Ignacio ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

^c HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA;

ADAPTIVE IMMUNITY; ARTICLE; CANCER GROWTH; CANCER IMMUNOLOGY; CANCER LOCALIZATION; CANCER PROGNOSIS; CELL HYPOXIA; CELL INFILTRATION; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; HUMAN; HYDROXYLATION; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MACROPHAGE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; TUMOR VASCULARIZATION;

ANIMALS; CELL HYPOXIA; HUMANS; IMMUNOTHERAPY; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84857702419     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1591     Document Type: Article

References (66)

1. Ward JP. Oxygen sensors in context. Biochim Biophys Acta 2008;1777:1-14.
2. Vaupel P. Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol 2004;14:198-206. (Pubitemid 38903223)
3. Caldwell CC, Kojima H, Lukashev D, Armstrong J, Farber M, Apasov SG, et al. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol 2001;167:6140-9. (Pubitemid 33081540)
4. Semenza GL. Oxygen sensing, homeostasis, and disease. N Engl J Med 2011;365:537-47.
5. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992;12:5447-54.
6. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992;359:843-5.
7. Garayoa M, Martínez A, Lee S, Pío R, An WG, Neckers L, et al. Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotionmechanismof carcinogenesis.Mol Endocrinol 2000;14:848-62. (Pubitemid 32260498)
8. Majmundar AJ, Wong WJ, Simon MC. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 2010;40:294-309.
9. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001;292: 468-72. (Pubitemid 32335942)
10. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005;2005:re12.
11. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 1998;17:3005-15. (Pubitemid 28254373)
12. Aragonés J, Fraisl P, Baes M, Carmeliet P. Oxygen sensors at the crossroad of metabolism. Cell Metab 2009;9:11-22.
13. Lando D,Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH- 1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 2002;16:1466-71. (Pubitemid 34686328)
14. Lisy K, Peet DJ. Turn me on: regulating HIF transcriptional activity. Cell Death Differ 2008;15:642-9. (Pubitemid 351405067)
15. Rankin EB, Biju MP, Liu Q, Unger TL, Rha J, Johnson RS, et al. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 2007;117:1068-77. (Pubitemid 46556763)
16. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-KuriyamaY. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A 1997;94:4273-8.
17. Fang HY, Hughes R, Murdoch C, Coffelt SB, Biswas SK, Harris AL, et al. Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 2009;114:844-59.
18. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 1997;11:72-82. (Pubitemid 27043825)
19. Dang EV, Barbi J, Yang HY, Jinasena D, Yu H, Zheng Y, et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 2011;146: 772-84.
20. Laderoute KR. The interaction between HIF-1 and AP-1 transcription factors in response to lowoxygen.Semin Cell Dev Biol 2005;16:502-13. (Pubitemid 41247873)
21. Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, et al. hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin Cancer Res 2008;14:1340-8. (Pubitemid 351413913)
22. Arany Z, Huang LE, Eckner R, Bhattacharya S, Jiang C, Goldberg MA, et al. An essential role for p300/CBPin the cellular response to hypoxia. Proc Natl Acad Sci U S A 1996;93:12969-73. (Pubitemid 26382753)
23. Takeda Y, Costa S, Delamarre E, Roncal C, de Oliveira RL, Squadrito ML, et al. Macrophage skewing by Phd2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature 2011;479:122-6.
24. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, Marti HH, et al. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 2008;453:410-4. (Pubitemid 351693122)
25. Crawford Y, Ferrara N. Tumor and stromal pathways mediating refractoriness/ resistance to anti-angiogenic therapies. Trends Pharmacol Sci 2009;30:624-30.
26. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011;473:298-307.
27. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegué E, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-20. (Pubitemid 351318372)
28. Alfaro C, Suárez N, Martínez-Forero I, Palazón A, Rouzaut A, Solano S, et al. Carcinoma-derived interleukin-8 disorients dendritic cell migration without impairing T-cell stimulation. PLoS ONE 2011;6:e17922.
29. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
30. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, et al. Macrophage polarization in tumour progression. Semin Cancer Biol 2008;18:349-55.
31. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008;13:453-61. (Pubitemid 351599757)
32. Movahedi K, Laoui D, Gysemans C, Baeten M, Stangé G, Van den Bossche J, et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 2010;70:5728-39.
33. Takeda N, O'Dea EL, Doedens A, Kim JW, Weidemann A, Stockmann C, et al. Differential activation and antagonistic function of HIF-alpha isoforms in macrophages are essential for NO homeostasis. Genes Dev 2010;24:491-501.
34. Rodríguez-Prados JC, Través PG, Cuenca J, Rico D, Aragonés J, Martín-Sanz P, et al. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol 2010;185:605-14.
35. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, et al. HIF-1alpha expression regulates the bactericidal capacity of phagocytes. J Clin Invest 2005;115:1806-15. (Pubitemid 40979719)
36. Blouin CC, Pagé EL, Soucy GM, Richard DE. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 2004;103:1124-30. (Pubitemid 38129580)
37. Shirato K, Kizaki T, Sakurai T, Ogasawara JE, Ishibashi Y, Iijima T, et al. Hypoxia-inducible factor-1alpha suppresses the expression of macrophage scavenger receptor 1. Pflugers Arch 2009;459:93-103.
38. Werno C, Menrad H, Weigert A, Dehne N, Goerdt S, Schledzewski K, et al. Knockout of HIF-1a in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis 2010;31:1863-72.
39. Bansal V, Ochoa JB. Arginine availability, arginase, and the immune response. Curr Opin Clin Nutr Metab Care 2003;6:223-8. (Pubitemid 40674527)
40. Imtiyaz HZ, Williams EP, Hickey MM, Patel SA, Durham AC, Yuan LJ, et al. Hypoxia-inducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation. J Clin Invest 2010;120:2699-714.
41. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, et al. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 2000;157:411-21. (Pubitemid 30626905)
42. 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.
43. CorzoCA, Condamine T, Lu L,CotterMJ, 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.
44. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci U S A 2011;108:16369-74.
45. Bosco MC, Pierobon D, Blengio F, Raggi F, Vanni C, Gattorno M, et al. Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mature dendritic cells: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo. Blood 2011;117:2625-39.
46. Olin MR, Andersen BM, Litterman AJ, Grogan PT, Sarver AL, Robertson PT, et al. Oxygen is a master regulator of the immunogenicity of primary human glioma cells. Cancer Res 2011;71: 6583-9.
47. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-74. (Pubitemid 40488632)
48. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 2011;29:610-8.
49. Atkuri KR, Herzenberg LA, Herzenberg LA. Culturing at atmospheric oxygen levels impacts lymphocyte function. Proc Natl Acad Sci U S A 2005;102:3756-9. (Pubitemid 40354684)
50. Atkuri KR, Herzenberg LA, Niemi AK, Cowan T, Herzenberg LA. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc Natl Acad Sci U S A 2007;104:4547-52. (Pubitemid 47186262)
51. Neumann AK, Yang J, Biju MP, Joseph SK, Johnson RS, Haase VH, et al. Hypoxia inducible factor 1 alpha regulates T cell receptor signal transduction. Proc Natl Acad Sci U S A 2005;102:17071-6. (Pubitemid 41692685)
52. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P, et al. Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE 2007;2:e853.
53. Lukashev D, Klebanov B, Kojima H, Grinberg A, Ohta A, Berenfeld L, et al. Cutting edge: hypoxia-inducible factor 1alpha and its activationinducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J Immunol 2006;177:4962-5. (Pubitemid 44527564)
54. Hasmim M, Noman MZ, Lauriol J, Benlalam H, Mallavialle A, Rosselli F, et al. Hypoxia-dependent inhibition of tumor cell susceptibility to CTL-mediated lysis involves NANOG induction in target cells. J Immunol 2011;187:4031-9.
55. Ohta A, Gorelik E, Prasad SJ, Ronchese F, Lukashev D,Wong MK, et al. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci U S A 2006;103:13132-7. (Pubitemid 44338928)
56. Zhang B. CD73: a novel target for cancer immunotherapy. Cancer Res 2010;70:6407-11.
57. Sitkovsky M, Lukashev D. Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors. Nat Rev Immunol 2005;5:712-21. (Pubitemid 43086172)
58. Kono K, Salazar-Onfray F, Petersson M, Hansson J, Masucci G, Wasserman K, et al. Hydrogen peroxide secreted by tumor-derived macrophages down-modulates signal-transducing zeta molecules and inhibits tumor-specific T cell-and natural killer cell-mediated cytotoxicity. Eur J Immunol 1996;26:1308-13.
59. Melero I, Murillo O, Dubrot J, Hervás-Stubbs S, Perez-Gracia JL. Multi-layered action mechanisms of CD137 (4-1BB)-targeted immunotherapies. Trends Pharmacol Sci 2008;29:383-90.
60. Alizadeh AA, Gentles AJ, Alencar AJ, Liu CL, Kohrt HE, Houot R, et al. Prediction of survival in diffuse large B-cell lymphoma based on the expression of 2 genes reflecting tumor and microenvironment. Blood 2011;118:1350-8.
61. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP, et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 2011;475:226-30.
62. Palazón A, Teijeira A, Martínez-Forero I, Hervás-Stubbs S, Roncal C, Peñuelas I, et al. Agonist anti-CD137 mAb act on tumor endothelial cells to enhance recruitment of activated T lymphocytes. Cancer Res 2011;71:801-11.
63. Noman MZ, Janji B, Kaminska B, Van Moer K, Pierson S, Przanowski P, et al. Blocking hypoxia-induced autophagy in tumors restores cytotoxic T-cell activity and promotes regression. Cancer Res 2011;71:5976-86.
64. Kuraishy A, Karin M, Grivennikov SI. Tumor promotion via injury- and death-induced inflammation. Immunity 2011;35:467-77.
65. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
66. Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 2007;7:95-106. (Pubitemid 46160986)