Immune response regulation in the tumor microenvironment by hypoxia

Seminars in Oncology

Volumn 42, Issue 3, 2015, Pages 378-386

  Labiano, Sara ^a   Palazon, Asis ^b   Melero, Ignacio ^a  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD137 ANTIGEN; OXYGEN; PROGRAMMED DEATH 1 LIGAND 1; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER IMMUNOTHERAPY; DENDRITIC CELL; HUMAN; HYPOXIA; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MACROPHAGE; METABOLISM; MONOCYTE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; CELL HYPOXIA; IMMUNOLOGY; NEOPLASM;

ADAPTIVE IMMUNITY; ANIMALS; CELL HYPOXIA; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; NEOPLASMS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84929145736     PISSN: 00937754     EISSN: 15328708     Source Type: Journal    
DOI: 10.1053/j.seminoncol.2015.02.009     Document Type: Review

References (88)

1. C.C. Caldwell, H. Kojima, and D. Lukashev Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions J Immunol 167 11 2001 6140 6149
2. C. Nombela-Arrieta, G. Pivarnik, and B. Winkel Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment Nat Cell Biol 15 5 2013 533 543
3. L.P. Hale, R.D. Braun, and W.M. Gwinn Hypoxia in the thymus: role of oxygen tension in thymocyte survival Am J Physiol Heart Circ Physiol 282 4 2002 H1467 H1477
4. M.P. Biju, A.K. Neumann, and S.J. Bensinger Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes Mol Cell Biol 24 20 2004 9038 9047
5. L.E. Kandalaft, G.T. Motz, and J. Busch Angiogenesis and the tumor vasculature as anti-tumor immune modulators: the role of vascular endothelial growth factor and endothelin Curr Top Microbiol Immunol 344 2011 129 148
6. P. Berraondo, V. Umansky, and I. Melero Changing the tumor microenvironment: new strategies for immunotherapy Cancer Res 72 20 2012 5159 5164
7. R. Wang, C.P. Dillon, and L.Z. Shi The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation Immunity 35 6 2011 871 882
8. K.A. Frauwirth, J.L. Riley, and M.H. Harris The CD28 signaling pathway regulates glucose metabolism Immunity 16 6 2002 769 777
9. G.L. Semenza Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology Annu Rev Pathol 9 2014 47 71
10. D. Lando, D.J. Peet, and J.J. Gorman FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor Genes Dev 16 12 2002 1466 1471
11. Z. Arany, L.E. Huang, and R. Eckner An essential role for p300/CBP in the cellular response to hypoxia Proc Natl Acad Sci U S A 93 23 1996 12969 12973
12. R.H. Wenger, D.P. Stiehl, and G. Camenisch Integration of oxygen signaling at the consensus HRE Sci STKE 2005 306 2005 re12
13. G.L. Semenza, B.H. Jiang, and S.W. Leung Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1 J Biol Chem 271 51 1996 32529 32537
14. G.L. Semenza, and G.L. Wang 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 12 12 1992 5447 5454
15. J.A. Forsythe, B.H. Jiang, and N.V. Iyer Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1 Mol Cell Biol 16 9 1996 4604 4613
16. M. Garayoa, A. Martinez, and S. Lee Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis Mol Endocrinol 14 6 2000 848 862
17. C. Peyssonnaux, V. Datta, and T. Cramer HIF-1alpha expression regulates the bactericidal capacity of phagocytes J Clin Invest 115 7 2005 1806 1815
18. G.M. Tannahill, A.M. Curtis, and J. Adamik Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha Nature 496 7444 2013 238 242
19. C.C. Blouin, E.L. Page, and G.M. Soucy Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha Blood 103 3 2004 1124 1130
20. J. Rius, M. Guma, and C. Schachtrup NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha Nature 453 7196 2008 807 811
21. H. Nakamura, Y. Makino, and K. Okamoto TCR engagement increases hypoxia-inducible factor-1 alpha protein synthesis via rapamycin-sensitive pathway under hypoxic conditions in human peripheral T cells J Immunol 174 12 2005 7592 7599
22. N.S. Chandel, W.C. Trzyna, and D.S. McClintock Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin J Immunol 165 2 2000 1013 1021
23. R.M. Steinman Decisions about dendritic cells: past, present, and future Annu Rev Immunol 30 2012 1 22
24. K. Palucka, and J. Banchereau Cancer immunotherapy via dendritic cells Nat Rev Cancer 12 4 2012 265 277
25. M.B. Fuertes, A.K. Kacha, and J. Kline Host type I IFN signals are required for anti-tumor CD8+T cell responses through CD8{alpha}+dendritic cells J Exp Med 208 10 2011 2005 2016
26. F. Wimmers, G. Schreibelt, and A.E. Skold Paradigm shift in dendritic cell-based immunotherapy: from in vitro generated monocyte-derived DCs to naturally circulating DC subsets Front Immunol 5 2014 165
27. J. Jantsch, M. Wiese, and J. Schodel Toll-like receptor activation and hypoxia use distinct signaling pathways to stabilize hypoxia-inducible factor 1alpha (HIF1A) and result in differential HIF1A-dependent gene expression J Leukoc Biol 90 3 2011 551 562
28. A. Mancino, T. Schioppa, and P. Larghi Divergent effects of hypoxia on dendritic cell functions Blood 112 9 2008 3723 3734
29. T. Bhandari, J. Olson, and R.S. Johnson HIF-1alpha influences myeloid cell antigen presentation and response to subcutaneous OVA vaccination J Mol Med (Berl) 91 10 2013 1199 1205
30. T. Kohler, B. Reizis, and R.S. Johnson Influence of hypoxia-inducible factor 1alpha on dendritic cell differentiation and migration Eur J Immunol 42 5 2012 1226 1236
31. W. Zhao, S. Darmanin, and Q. Fu Hypoxia suppresses the production of matrix metalloproteinases and the migration of human monocyte-derived dendritic cells Eur J Immunol 35 12 2005 3468 3477
32. X. Qu, M.X. Yang, and B.H. Kong Hypoxia inhibits the migratory capacity of human monocyte-derived dendritic cells Immunol Cell Biol 83 6 2005 668 673
33. A. Ricciardi, A.R. Elia, and P. Cappello Transcriptome of hypoxic immature dendritic cells: modulation of chemokine/receptor expression Mol Cancer Res 6 2 2008 175 185
34. K. Shortman, and Y.J. Liu Mouse and human dendritic cell subtypes Nat Rev Immunol 2 3 2002 151 161
35. M. Yang, C. Ma, and S. Liu Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin Immunology 128 1 Suppl 2009 e237 e249
36. A. Weigert, B. Weichand, and D. Sekar HIF-1alpha is a negative regulator of plasmacytoid DC development in vitro and in vivo Blood 120 15 2012 3001 3006
37. R. Noy, and J.W. Pollard Tumor-associated macrophages: from mechanisms to therapy Immunity 41 1 2014 49 61
38. A. Mantovani, S. Sozzani, and M. Locati Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes Trends Immunol 23 11 2002 549 555
39. C. Murdoch, A. Giannoudis, and C.E. Lewis Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues Blood 104 8 2004 2224 2234
40. A. Casazza, D. Laoui, and M. Wenes Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores anti-tumor immunity Cancer Cell 24 6 2013 695 709
41. T. Cramer, Y. Yamanishi, and B.E. Clausen HIF-1alpha is essential for myeloid cell-mediated inflammation Cell 112 5 2003 645 657
42. J.S. Lewis, R.J. Landers, and J.C. Underwood Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas J Pathol 192 2 2000 150 158
43. M. De Palma, M.A. Venneri, and R. Galli Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors Cancer Cell 8 3 2005 211 226
44. C.E. Lewis, M. De Palma, and L. Naldini Tie2-expressing monocytes and tumor angiogenesis: regulation by hypoxia and angiopoietin-2 Cancer Res 67 18 2007 8429 8432
45. A.L. Doedens, C. Stockmann, and M.P. Rubinstein Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression Cancer Res 70 19 2010 7465 7475
46. C.A. Corzo, T. Condamine, and L. Lu HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment J Exp Med 207 11 2010 2439 2453
47. M.Z. Noman, G. Desantis, and B. Janji PD-L1 is a novel direct target of HIF-1alpha, and its blockade under hypoxia enhanced MDSC-mediated T cell activation J Exp Med 211 5 2014 781 790
48. H.Z. Imtiyaz, E.P. Williams, and M.M. Hickey Hypoxia-inducible factor 2alpha regulates macrophage function in mouse models of acute and tumor inflammation J Clin Invest 120 8 2010 2699 2714
49. K.L. Talks, H. Turley, and K.C. Gatter 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 157 2 2000 411 421
50. N. Takeda, E.L. O'Dea, and A. Doedens Differential activation and antagonistic function of HIF-{alpha} isoforms in macrophages are essential for NO homeostasis Genes Dev 24 5 2010 491 501
51. D. Laoui, E. Van Overmeire, and G. Di Conza Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population Cancer Res 74 1 2014 24 30
52. K. Movahedi, D. Laoui, and C. Gysemans Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes Cancer Res 70 14 2010 5728 5739
53. A.D. Gregory, and A.M. Houghton Tumor-associated neutrophils: new targets for cancer therapy Cancer Res 71 7 2011 2411 2416
54. M. Shen, P. Hu, and F. Donskov Tumor-associated neutrophils as a new prognostic factor in cancer: a systematic review and meta-analysis PLoS One 9 6 2014 e98259
55. S. Hannah, K. Mecklenburgh, and I. Rahman Hypoxia prolongs neutrophil survival in vitro FEBS Lett 372 2-3 1995 233 237
56. S.R. Walmsley, C. Print, and N. Farahi Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity J Exp Med 201 1 2005 105 115
57. S.R. Walmsley, E.R. Chilvers, and A.A. Thompson Prolyl hydroxylase 3 (PHD3) is essential for hypoxic regulation of neutrophilic inflammation in humans and mice J Clin Invest 121 3 2011 1053 1063
58. Z.G. Fridlender, J. Sun, and S. Kim Polarization of tumor-associated neutrophil phenotype by TGF-beta: «N1» versus «N2» TAN Cancer Cell 16 3 2009 183 194
59. M. Thiel, C.C. Caldwell, and S. Kreth Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival PLoS One 2 9 2007 e853
60. J. Roman, T. Rangasamy, and J. Guo T-cell activation under hypoxic conditions enhances IFN-gamma secretion Am J Respir Cell Mol Biol 42 1 2010 123 128
61. E.T. Clambey, E.N. McNamee, and J.A. Westrich Hypoxia-inducible factor-1 alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa Proc Natl Acad Sci U S A 109 41 2012 E2784 E2793
62. E.V. Dang, J. Barbi, and H.Y. Yang Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1 Cell 146 5 2011 772 784
63. A. Facciabene, X. Peng, and I.S. Hagemann Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells Nature 475 7355 2011 226 230
64. M. Hasmim, M.Z. Noman, and J. Lauriol Hypoxia-dependent inhibition of tumor cell susceptibility to CTL-mediated lysis involves NANOG induction in target cells J Immunol 187 8 2011 4031 4039
65. B. Deng, J.M. Zhu, and Y. Wang Intratumor hypoxia promotes immune tolerance by inducing regulatory T cells via TGF-beta1 in gastric cancer PLoS One 8 5 2013 e63777
66. M. Hasmim, M.Z. Noman, and Y. Messai Cutting edge: hypoxia-induced Nanog favors the intratumoral infiltration of regulatory T cells and macrophages via direct regulation of TGF-beta1 J Immunol 191 12 2013 5802 5806
67. A. Ohta, E. Gorelik, and S.J. Prasad A2A adenosine receptor protects tumors from anti-tumor T cells Proc Natl Acad Sci U S A 103 35 2006 13132 13137
68. B. Zhang CD73: a novel target for cancer immunotherapy Cancer Res 70 16 2010 6407 6411
69. M.V. Sitkovsky, J. Kjaergaard, and D. Lukashev Hypoxia-adenosinergic immunosuppression: tumor protection by T regulatory cells and cancerous tissue hypoxia Clin Cancer Res 14 19 2008 5947 5952
70. A.L. Doedens, A.T. Phan, and M.H. Stradner Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen Nat Immunol 14 11 2013 1173 1182
71. A. Palazon, I. Martinez-Forero, and A. Teijeira The HIF-1alpha hypoxia response in tumor-infiltrating T lymphocytes induces functional CD137 (4-1BB) for immunotherapy Cancer Discov 2 7 2012 608 623
72. H. Wang, H. Flach, and M. Onizawa Negative regulation of Hif1a expression and TH17 differentiation by the hypoxia-regulated microRNA miR-210 Nat Immunol 15 4 2014 393 401
73. L. Senovilla, E. Vacchelli, and J. Galon Trial watch: prognostic and predictive value of the immune infiltrate in cancer Oncoimmunology 1 8 2012 1323 1343
74. I.B. Barsoum, T.K. Hamilton, and X. Li Hypoxia induces escape from innate immunity in cancer cells via increased expression of ADAM10: role of nitric oxide Cancer Res 71 24 2011 7433 7441
75. M. Balsamo, C. Manzini, and G. Pietra Hypoxia downregulates the expression of activating receptors involved in NK-cell-mediated target cell killing without affecting ADCC Eur J Immunol 43 10 2013 2756 2764
76. S. Sarkar, W.T. Germeraad, and K.M. Rouschop Hypoxia induced impairment of NK cell cytotoxicity against multiple myeloma can be overcome by IL-2 activation of the NK cells PLoS One 8 5 2013 e64835
77. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 5 2011 646 674
78. R.A. Cairns, I.S. Harris, and T.W. Mak Regulation of cancer cell metabolism Nat Rev Cancer 11 2 2011 85 95
79. L.A. Sena, S. Li, and A. Jairaman Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling Immunity 38 2 2013 225 236
80. C.H. Chang, J.D. Curtis, and L.B. Maggi Jr. Posttranscriptional control of T cell effector function by aerobic glycolysis Cell 153 6 2013 1239 1251
81. J.W. Kim, I. Tchernyshyov, and G.L. Semenza HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia Cell Metab 3 3 2006 177 185
82. D.K. Finlay, E. Rosenzweig, and L.V. Sinclair PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+T cells J Exp Med 209 13 2012 2441 2453
83. P. Correale, M.S. Rotundo, and C. Botta Tumor infiltration by T lymphocytes expressing chemokine receptor 7 (CCR7) is predictive of favorable outcome in patients with advanced colorectal carcinoma Clin Cancer Res 18 3 2012 850 857
84. G.J. van der Windt, and E.L. Pearce Metabolic switching and fuel choice during T-cell differentiation and memory development Immunol Rev 249 1 2012 27 42
85. M. Sukumar, J. Liu, and Y. Ji Inhibiting glycolytic metabolism enhances CD8+T cell memory and anti-tumor function J Clin Invest 123 10 2013 4479 4488
86. R.D. Michalek, V.A. Gerriets, and S.R. Jacobs Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+T cell subsets J Immunol 186 6 2011 3299 3303
87. L.Z. Shi, R. Wang, and G. Huang HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells J Exp Med 208 7 2011 1367 1376
88. A. Haschemi, P. Kosma, and L. Gille The sedoheptulose kinase CARKL directs macrophage polarization through control of glucose metabolism Cell Metab 15 6 2012 813 826