Hypoxia-inducible factors in cancer stem cells and inflammation

Trends in Pharmacological Sciences

Volumn 36, Issue 6, 2015, Pages 374-383

  Peng, Gong ^a   Liu, Yang ^a,b  

^a JILIN UNIVERSITY   (China)

^b CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

Cancer immunotherapy; Dendritic cells; Leukemia initiating cells; Myeloid derived suppressor cells; Tumor microenvironment; Tumor associated macrophages

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MULTIDRUG RESISTANCE PROTEIN 1; ONCOPROTEIN; PKM2 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; HYPOXIA INDUCIBLE FACTOR 1;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ADAPTIVE IMMUNITY; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CHRONIC MYELOID LEUKEMIA; CROSS FERTILIZATION; DENDRITIC CELL; GENETIC ASSOCIATION; GLIOMA; HUMAN; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; TH17 CELL; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; GENETIC EPIGENESIS; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INFLAMMATION; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 84934974754     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2015.03.003     Document Type: Review

References (119)

1. Hanahan, D. and Weinberg, R.A. (2000) The hallmarks of cancer. Cell 100, 57-70
2. Hanahan, D. and Weinberg, R.A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
3. Al-Hajj, M. et al. (2003) Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 100, 3983-3988
4. Lapidot, T. et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648
5. Bao, S. et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760
6. Terpstra, W. et al. (1996) Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice and in culture. Blood 88, 1944-1950
7. Wicha, M.S. et al. (2006) Cancer stem cells: an old idea-a paradigm shift. Cancer Res. 66, 1883-1890 discussion 1895-1886
8. Li, Z. et al. (2009) Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15, 501-513
9. Wang, Y. et al. (2011) Targeting HIF1alpha eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 8, 399-411
10. Wang, Y.H. et al. (2014) Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis. Cell 158, 1309-1323
11. Palazon, A. et al. (2014) HIF transcription factors, inflammation, and immunity. Immunity 41, 518-528
12. Cheng, S.C. et al. (2014) mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345, 1250684
13. Saeed, S. et al. (2014) Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345, 1251086
14. Keith, B. et al. (2012) HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 12, 9-22
15. Semenza, G.L. (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408
16. Wang, G.L. et al. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U.S.A. 92, 5510-5514
17. Luo, W. et al. (2011) Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145, 732-744
18. Zhang, P. et al. (2014) Hypoxia-inducible factor 3 is an oxygen-dependent transcription activator and regulates a distinct transcriptional response to hypoxia. Cell Rep. 6, 1110-1121
19. Kondo, K. et al. (2002) Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1, 237-246
20. Latif, F. et al. (1993) Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 260, 1317-1320
21. Maranchie, J.K. et al. (2002) The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1, 247-255
22. Pereira, T. et al. (2003) Identification of residues critical for regulation of protein stability and the transactivation function of the hypoxia-inducible factor-1alpha by the von Hippel-Lindau tumor suppressor gene product. J. Biol. Chem. 278, 6816-6823
23. Zbar, B. (1995) Von Hippel-Lindau disease and sporadic renal cell carcinoma. Cancer Surv. 25, 219-232
24. Semenza, G.L. (2010) HIF-1: upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev. 20, 51-56
25. Xu, W. et al. (2011) Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17-30
26. Zhao, S. et al. (2009) Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 324, 261-265
27. Ward, P.S. et al. (2010) The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 17, 225-234
28. Pardanani, A. et al. (2010) IDH1 and IDH2 mutation analysis in chronic- and blast-phase myeloproliferative neoplasms. Leukemia 24, 1146-1151
29. Abbas, S. et al. (2010) Acquired mutations in the genes encoding IDH1 and IDH2 both are recurrent aberrations in acute myeloid leukemia: prevalence and prognostic value. Blood 116, 2122-2126
30. Paschka, P. et al. (2010) IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication. J. Clin. Oncol. 28, 3636-3643
31. Yan, H. et al. (2009) IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765-773
32. Koivunen, P. et al. (2012) Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature 483, 484-488
33. Bertout, J.A. et al. (2009) Heterozygosity for hypoxia inducible factor 1alpha decreases the incidence of thymic lymphomas in a p53 mutant mouse model. Cancer Res. 69, 3213-3220
34. Lidgren, A. et al. (2005) The expression of hypoxia-inducible factor 1alpha is a favorable independent prognostic factor in renal cell carcinoma. Clin. Cancer Res. 11, 1129-1135
35. Klatte, T. et al. (2007) Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin. Cancer Res. 13, 7388-7393
36. Mazumdar, J. et al. (2010) HIF-2alpha deletion promotes Kras-driven lung tumor development. Proc. Natl. Acad. Sci. U.S.A. 107, 14182-14187
37. Velasco-Hernandez, T. et al. (2014) HIF-1alpha can act as a tumor suppressor gene in murine acute myeloid leukemia. Blood 124, 3597-3607
38. Zhang, H. et al. (2007) HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11, 407-420
39. Mazure, N.M. et al. (1996) Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res. 56, 3436-3440
40. Arany, Z. et al. (1996) An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. U.S.A. 93, 12969-12973
41. Forsythe, J.A. et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4604-4613
42. Kong, D. et al. (2005) Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res. 65, 9047-9055
43. Comerford, K.M. et al. (2002) Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 62, 3387-3394
44. Ricker, J.L. et al. (2004) 2-methoxyestradiol inhibits hypoxia-inducible factor 1alpha, tumor growth, and angiogenesis and augments paclitaxel efficacy in head and neck squamous cell carcinoma. Clin. Cancer Res. 10, 8665-8673
45. Zhang, H. et al. (2014) Kruppel-like factor 8 contributes to hypoxia-induced MDR in gastric cancer cells. Cancer Sci. 105, 1109-1115
46. Ria, R. et al. (2014) HIF-1alpha of bone marrow endothelial cells implies relapse and drug resistance in patients with multiple myeloma and may act as a therapeutic target. Clin. Cancer Res. 20, 847-858
47. Li, D.W. et al. (2013) Hypoxia induced multidrug resistance of laryngeal cancer cells via hypoxia-inducible factor-1alpha. Asian Pac. J. Cancer Prev. 14, 4853-4858
48. Wang, H. et al. (2014) Wogonin reverses hypoxia resistance of human colon cancer HCT116 cells via downregulation of HIF-1alpha and glycolysis, by inhibiting PI3K/Akt signaling pathway. Mol. Carcinog. 53 (Suppl. 1), E107-E118
49. Cui, X.Y. et al. (2013) Hypoxia influences stem cell-like properties in multidrug resistant K562 leukemic cells. Blood Cells. Mol. Dis. 51, 177-184
50. Ji, Z. et al. (2010) Expression of MDR1, HIF-1alpha and MRP1 in sacral chordoma and chordoma cell line CM-319. J. Exp. Clin. Cancer Res. 29, 158
51. Ding, Z. et al. (2010) Expression and significance of hypoxia-inducible factor-1 alpha and MDR1/P-glycoprotein in human colon carcinoma tissue and cells. J. Cancer Res. Clin. Oncol. 136, 1697-1707
52. An, W.G. et al. (1998) Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 392, 405-408
53. Shoshani, T. et al. (2002) Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 22, 2283-2293
54. Bruick, R.K. (2000) Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. U.S.A. 97, 9082-9087
55. Sowter, H.M. et al. (2001) HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61, 6669-6673
56. Koshiji, M. et al. (2004) HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J. 23, 1949-1956
57. Jin, L. et al. (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat. Med. 12, 1167-1174
58. Jin, L. et al. (2009) Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 5, 31-42
59. Kikushige, Y. et al. (2010) TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 7, 708-717
60. Guzman, M.L. et al. (2007) An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 110, 4427-4435
61. Kelly, P.N. et al. (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317, 337
62. Wang, L. et al. (2013) FISH+CD34+CD38- cells detected in newly diagnosed acute myeloid leukemia patients can predict the clinical outcome. J. Hematol. Oncol. 6, 85
63. Witte, K.E. et al. (2011) High proportion of leukemic stem cells at diagnosis is correlated with unfavorable prognosis in childhood acute myeloid leukemia. Pediatr. Hematol. Oncol. 28, 91-99
64. van Rhenen, A. et al. (2005) High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin. Cancer Res. 11, 6520-6527
65. Gentles, A.J. et al. (2010) Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 304, 2706-2715
66. (2014) NIH Clinical Center open to coll-aboration. Cancer Discovery 4, 752
67. Wang, Y. et al. (2014) Echinomycin protects mice against relapsed acute myeloid leukemia without adverse effect on hematopoietic stem cells. Blood 124, 1127-1135
68. Bernot, K.M. et al. (2013) Toward personalized therapy in AML: in vivo benefit of targeting aberrant epigenetics in MLL-PTD-associated AML. Leukemia 27, 2379-2382
69. Sloma, I. et al. (2010) Insights into the stem cells of chronic myeloid leukemia. Leukemia 24, 1823-1833
70. Mayerhofer, M. et al. (2002) BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor-1alpha, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood 100, 3767-3775
71. Zhao, F. et al. (2010) Imatinib resistance associated with BCR-ABL upregulation is dependent on HIF-1alpha-induced metabolic reprograming. Oncogene 29, 2962-2972
72. Zhang, H. et al. (2012) HIF1alpha is required for survival maintenance of chronic myeloid leukemia stem cells. Blood 119, 2595-2607
73. Ng, K.P. et al. (2014) Physiologic hypoxia promotes maintenance of CML stem cells despite effective BCR-ABL1 inhibition. Blood 123, 3316-3326
74. Conley, S.J. et al. (2012) Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc. Natl. Acad. Sci. U.S.A. 109, 2784-2789
75. Schwab, L.P. et al. (2012) Hypoxia-inducible factor 1alpha promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 14, R6
76. Cordenonsi, M. et al. (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147, 759-772
77. Xiang, L. et al. (2014) Hypoxia-inducible factor 1 mediates TAZ expression and nuclear localization to induce the breast cancer stem cell phenotype. Oncotarget 5, 12509-12527
78. Chaturvedi, P. et al. (2014) Hypoxia-inducible factor-dependent signaling between triple-negative breast cancer cells and mesenchymal stem cells promotes macrophage recruitment. Proc. Natl. Acad. Sci. U.S.A. 111, E2120-E2129
79. Lukashev, D. et al. (2001) Differential regulation of two alternatively spliced isoforms of hypoxia-inducible factor-1 alpha in activated T lymphocytes. J. Biol. Chem. 276, 48754-48763
80. Lukashev, D. et al. (2006) Cutting edge: hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J. Immunol. 177, 4962-4965
81. Dang, E.V. et al. (2011) Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 146, 772-784
82. Shi, L.Z. et al. (2011) HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208, 1367-1376
83. Kryczek, I. et al. (2011) Human TH17 cells are long-lived effector memory cells. Sci. Transl. Med. 3, 104ra100
84. Ben-Shoshan, J. et al. (2008) Hypoxia controls CD4+CD25+ regulatory T-cell homeostasis via hypoxia-inducible factor-1alpha. Eur. J. Immunol. 38, 2412-2418
85. Facciabene, A. et al. (2011) Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475, 226-230
86. Finlay, D.K. et al. (2012) PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+ T cells. J. Exp. Med. 209, 2441-2453
87. Doedens, A.L. et al. (2013) Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen. Nat. Immunol. 14, 1173-1182
88. Thiel, M. et al. (2007) Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS ONE 2, e853
89. Jantsch, J. et al. (2008) Hypoxia and hypoxia-inducible factor-1 alpha modulate lipopolysaccharide-induced dendritic cell activation and function. J. Immunol. 180, 4697-4705
90. Noman, M.Z. et al. (2014) 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, 781-790
91. Barsoum, I.B. et al. (2014) A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res. 74, 665-674
92. Curiel, T.J. et al. (2003) Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 9, 562-567
93. Gabrilovich, D.I. and Nagaraj, S. (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174
94. Talmadge, J.E. and Gabrilovich, D.I. (2013) History of myeloid-derived suppressor cells. Nat. Rev. Cancer 13, 739-752
95. Corzo, C.A. et al. (2010) HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453
96. Doedens, A.L. et al. (2010) Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 70, 7465-7475
97. Chen, W. et al. (2010) mTOR signaling is activated by FLT3 kinase and promotes survival of FLT3-mutated acute myeloid leukemia cells. Mol. Cancer 9, 292
98. Gilliland, D.G. and Griffin, J.D. (2002) The roles of FLT3 in hematopoiesis and leukemia. Blood 100, 1532-1542
99. Sathaliyawala, T. et al. (2010) Mammalian target of rapamycin controls dendritic cell development downstream of Flt3 ligand signaling. Immunity 33, 597-606
100. Brugarolas, J. et al. (2004) Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18, 2893-2904
101. Brugarolas, J.B. et al. (2003) TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4, 147-158
102. Hudson, C.C. et al. (2002) Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol. Cell. Biol. 22, 7004-7014
103. Van de Velde, S. et al. (2011) mTOR links incretin signaling to HIF induction in pancreatic beta cells. Proc. Natl. Acad. Sci. U.S.A. 108, 16876-16882
104. Huang, J. et al. (2009) Pivotal role for glycogen synthase kinase-3 in hematopoietic stem cell homeostasis in mice. J. Clin. Invest. 119, 3519-3529
105. Parkin, B. et al. (2010) Acquired genomic copy number aberrations and survival in adult acute myelogenous leukemia. Blood 116, 4958-4967
106. Joshi, S. et al. (2014) MDM2 regulates hypoxic hypoxia-inducible factor 1alpha stability in an E3 ligase, proteasome, and PTEN-phosphatidylinositol 3-kinase-AKT-dependent manner. J. Biol. Chem. 289, 22785-22797
107. Ravi, R. et al. (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev. 14, 34-44
108. Falini, B. et al. (2005) Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med. 352, 254-266
109. Grisendi, S. and Pandolfi, P.P. (2005) NPM mutations in acute myelogenous leukemia. N. Engl. J. Med. 352, 291-292
110. Chen, D. et al. (2010) Transcription-independent ARF regulation in oncogenic stress-mediated p53 responses. Nature 464, 624-627
111. Fatyol, K. and Szalay, A.A. (2001) The p14ARF tumor suppressor protein facilitates nucleolar sequestration of hypoxia-inducible factor-1alpha (HIF-1alpha) and inhibits HIF-1-mediated transcription. J. Biol. Chem. 276, 28421-28429
112. Wang, H. et al. (2014) Negative regulation of Hif1a expression and TH17 differentiation by the hypoxia-regulated microRNA miR-210. Nat. Immunol. 15, 393-401
113. Blouin, C.C. et al. (2004) Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 103, 1124-1130
114. Laughner, E. et al. (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21, 3995-4004
115. Cui, T.X. et al. (2013) Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity 39, 611-621
116. Kryczek, I. et al. (2014) IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L. Immunity 40, 772-784
117. Lin, E.Y. et al. (2006) Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66, 11238-11246
118. Ben-Neriah, Y. and Karin, M. (2011) Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat. Immunol. 12, 715-723
119. Lin, E.Y. and Pollard, J.W. (2007) Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res. 67, 5064-5066