Molecular responses to hypoxia-inducible factor 1α and beyond

Molecular Pharmacology

Volumn 85, Issue 5, 2014, Pages 651-657

  Brocato, Jason ^a   Chervona, Yana ^a   Costa, Max ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; 4 [BIS(2 CHLOROETHYL)OXIDOAMINO]PHENYLALANINE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; DACTOLISIB; DEFERASIROX; DIOXYGENASE; HISTONE DEMETHYLASE; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIFICIGUAT; MAGNOLOL; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; METFORMIN; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PYRUVATE KINASE; SORAFENIB; TOPOTECAN; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR RUNX3;

CANCER PROGNOSIS; DRUG TARGETING; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL HYPOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TRANSCRIPTION FACTORS;

EID: 84897382168     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.089623     Document Type: Review

References (81)

1. Agani F and Jiang BH (2013) Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets 13: 245-251.
2. Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, and Xavier RJ (2009) An integrative genomics approach identifies hypoxia inducible factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37:4587-4602.
3. Birner P, Schindl M, Obermair A, Plank C, Breitenecker G, and Oberhuber G (2000) Over expression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res 60:4693-4696.
4. Cao D, Hou M, Guan YS, Jiang M, Yang Y, and Gou HF (2009) Expression of HIF-1alpha and VEGF in colorectal cancer: association with clinical outcomes and prognostic implications. BMC Cancer 9:432.
5. Chai DM, Bao ZQ, Hu JG, Ma L, Feng ZZ, and Tao YS (2013) Vasculogenic mimicry and aberrant expression of HIF-la/E-cad are associated with worse prognosis of esophageal squamous cell carcinoma. J Huazhong Univ Sci Technolog Med Sci 33: 385-391.
6. Chen H and Costa M (2009) Iron-and 2-oxoglutarate-dependent dioxygenases: an emerging group of molecular targets for nickel toxicity and carcinogenicity. Biometals 22:191-196.
7. Chen MC, Lee CF, Huang WH, and Chou TC (2013) Magnolol suppresses hypoxia induced angiogenesis via inhibition of HIF-1α/VEGF signaling pathway in human bladder cancer cells. Biochem Pharmacol 85:1278-1287.
8. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, and Cantley LC (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-233.
9. Daponte A, Ioannou M, Mylonis I, Simos G, Minas M, Messinis IE, and Koukoulis G (2008) Prognostic significance of hypoxia-inducible factor 1 alpha(HIF-1 alpha) expression in serous ovarian cancer: an immunohistochemical study. BMC Cancer 8:335.
10. Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, and Mazure NM (2006) The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxiainducible factor-1alpha. Cancer Res 66:3688-3698.
11. Demidenko ZN and Blagosklonny MV (2011) The purpose of the HIF-1/PHD feedback loop: to limit mTOR-induced HIF-1α. Cell Cycle 10:1557-1562.
12. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, and Gleadle JM (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1α, HIF-2αlpha, and other pathways. J Biol Chem 281:15215-15226.
13. Favaro E, Ramachandran A, McCormick R, Gee H, Blancher C, Crosby M, Devlin C, Blick C, Buffa F, and Li JL et al. (2010) MicroRNA-210 regulates mitochondrial free radical response to hypoxia and krebs cycle in cancer cells by targeting iron sulfur cluster protein ISCU. PLoS One 5:e10345.
14. Fillies T, Werkmeister R, van Diest PJ, Brandt B, Joos U, and Buerger H (2005) HIF1-alpha overexpression indicates a good prognosis in early stage squamous cell carcinomas of the oral floor. BMC Cancer 5:84.
15. Finlay DK, Rosenzweig E, Sinclair LV, Feijoo-Carnero C, Hukelmann JL, Rolf J, Panteleyev AA, Okkenhaug K, and Cantrell DA (2012) PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+ T cells. J Exp Med 209:2441-2453.
16. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285: 1182-1186.
17. Giatromanolaki A (2001) Prognostic role of angiogenesis in non-small cell lung cancer. Anticancer Res 21:4373-4382.
18. Giatromanolaki A, Koukourakis MI, Sivridis E, Turley H, Talks K, Pezzella F, Gatter KC, and Harris AL (2001) Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 85:881-890.
19. Giatromanolaki A, Sivridis E, Kouskoukis C, Gatter KC, Harris AL, and Koukourakis MI (2003) Hypoxia-inducible factors 1alpha and 2alpha are related to vascular endothelial growth factor expression and a poorer prognosis in nodular malignant melanomas of the skin. Melanoma Res 13:493-501.
20. Greer SN, Metcalf JL, Wang Y, and Ohh M (2012) The updated biology of hypoxiainducible factor. EMBO J 31:2448-2460.
21. Guo X, Lu J, Wang Y, Gui Y, Duan X, and Cai Z (2012) Ascorbate antagonizes nickel ion to regulate JMJD1A expression in kidney cancer cells. Acta Biochim Biophys Sin (Shanghai) 44:330-338.
22. Horak P, Crawford AR, Vadysirisack DD, Nash ZM, DeYoung MP, Sgroi D, and Ellisen LW (2010) Negative feedback control of HIF-1 through REDD+-regulated ROS suppresses tumorigenesis. Proc Natl Acad Sci USA 107:4675-4680.
23. Hu Y, Liu J, and Huang H (2013) Recent agents targeting HIF-1α for cancer therapy. J Cell Biochem 114:498-509.
24. Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, Chung YL, Merino M, Trepel J, Zbar B, and Toro J et al. (2005) HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8:143-153.
25. Ito Y (2004) Oncogenic potential of the RUNX gene family: 'overview.' Oncogene 23: 4198-4208.
26. Jin HO, Seo SK, Woo SH, Kim ES, Lee HC, Yoo DH, Choe TB, Hong SI, Kim JI, and Park IC (2009) SP600125 negatively regulates the mammalian target of rapamycin via ATF4-induced Redd1 expression. FEBS Lett 583:123-127.
27. Kaelin WG, Jr and Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393-402.
28. Karar J, Cerniglia GJ, Lindsten T, Koumenis C, and Maity A (2012) Dual PI3K/mTOR inhibitor NVP-BEZ235 suppresses hypoxia-inducible factor (HIF)-1alpha expression by blocking protein translation and increases cell death under hypoxia. Cancer Biol Ther 13:1102-1111.
29. Ke Q and Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70: 1469-1480.
30. Klatte T, Seligson DB, Riggs SB, Leppert JT, Berkman MK, Kleid MD, Yu H, Kabbinavar FF, Pantuck AJ, and Belldegrun AS (2007) Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin Cancer Res 13:7388-7393.
31. Klose RJ, Kallin EM, and Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7:715-727.
32. Koh MY, Darnay BG, and Powis G (2008) Hypoxia-associated factor, a novel E3-ubiquitin ligase, binds and ubiquitinates hypoxia-inducible factor 1alpha, leading to its oxygen-independent degradation. Mol Cell Biol 28:7081-7095.
33. Koivunen P, Hirsilä M, Remes AM, Hassinen IE, Kivirikko KI, and Myllyharju J (2007) Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 282:4524-4532.
34. Kolamunne RT, Clare M, and Griffiths HR (2011) Mitochondrial superoxide anion radicals mediate induction of apoptosis in cardiac myoblasts exposed to chronic hypoxia. Arch Biochem Biophys 505:256-265.
35. Koukourakis MI, Giatromanolaki A, Sivridis E, Simopoulos C, Turley H, Talks K, Gatter KC, and Harris AL (2002) Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer. Int J Radiat Oncol Biol Phys 53:1192-1202.
36. Krieg AJ, Rankin EB, Chan D, Razorenova O, Fernandez S, and Giaccia AJ (2010) Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth. Mol Cell Biol 30: 344-353.
37. Kucejova B, Peña-Llopis S, Yamasaki T, Sivanand S, Tran TA, Alexander S, Wolff NC, Lotan Y, Xie XJ, and Kabbani W et al. (2011) Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol Cancer Res 9: 1255-1265.
38. Lang KJ, Kappel A, and Goodall GJ (2002) Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 13:1792-1801.
39. Lee K and Kim HM (2011) A novel approach to cancer therapy using PX-478 as a HIF-1α inhibitor. Arch Pharm Res 34:1583-1585.
40. Lee SH, Bae SC, Kim KW, and Lee YM (2013) RUNX3 inhibits hypoxia-inducible factor-1a protein stability by interacting with prolyl hydroxylases in gastric cancer cells [published ahead of print]. Oncogene DOI: 10.1038/onc.2013.76.
41. Lee SH, Che X, Jeong JH, Choi JY, Lee YJ, Lee YH, Bae SC, and Lee YM (2012) Runx2 protein stabilizes hypoxia-inducible factor-1a through competition with von Hippel-Lindau protein (pVHL) and stimulates angiogenesis in growth plate hypertrophic chondrocytes. J Biol Chem 287:14760-14771.
42. Lidgren A, Hedberg Y, Grankvist K, Rasmuson T, Bergh A, and Ljungberg B (2006) Hypoxia-inducible factor 1alpha expression in renal cell carcinoma analyzed by tissue microarray. Eur Urol 50:1272-1277.
43. Liu LP, Ho RL, Chen GG, and Lai PB (2012) Sorafenib inhibits hypoxia-inducible factor-1alpha synthesis: implications for antiangiogenic activity in hepatocellular carcinoma. Clin Cancer Res 18:5662-5671.
44. Liu YV, Baek JH, Zhang H, Diez R, Cole RN, and Semenza GL (2007) RACK1 competes with HSP90 for binding to HIF-1α and is required for O(2)-independent and HSP90 inhibitor-induced degradation of HIF-1α. Mol Cell 25: 207-217.
45. Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, Cole RN, Pandey A, and Semenza GL (2011) Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145:732-744.
46. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, and Semenza GL (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669.
47. Mazurek S (2011) Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. Int J Biochem Cell Biol 43:969-980.
48. Melvin A and Rocha S (2012) Chromatin as an oxygen sensor and active player in the hypoxia response. Cell Signal 24:35-43.
49. Myllyharju J and Koivunen P (2013) Hypoxia-inducible factor prolyl 4-hydroxylases: common and specific roles. Biol Chem 394:435-448.
50. Ohyashiki JH, Kobayashi C, Hamamura R, Okabe S, Tauchi T, and Ohyashiki K (2009) The oral iron chelator deferasirox represses signaling through the mTOR in myeloid leukemia cells by enhancing expression of REDD1. Cancer Sci 100: 970-977.
51. Peng H, Hamanaka RB, Katsnelson J, Hao LL, Yang W, Chandel NS, and Lavker RM (2012a) MicroRNA-31 targets FIH-1 to positively regulate corneal epithelial glycogen metabolism. FASEB J 26:3140-3147.
52. Peng H, Kaplan N, Hamanaka RB, Katsnelson J, Blatt H, Yang W, Hao L, Bryar PJ, Johnson RS, and Getsios S et al. (2012b) microRNA-31/factor-inhibiting hypoxiainducible factor 1 nexus regulates keratinocyte differentiation. Proc Natl Acad Sci USA 109:14030-14034.
53. Peng ZG, Zhou MY, Huang Y, Qiu JH, Wang LS, Liao SH, Dong S, and Chen GQ (2008) Physical and functional interaction of Runt-related protein 1 with hypoxiainducible factor-1alpha. Oncogene 27:839-847.
54. Pollard PJ, Loenarz C, Mole DR, McDonough MA, Gleadle JM, Schofield CJ, and Ratcliffe PJ (2008) Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha. Biochem J 416:387-394.
55. Poyton RO, Ball KA, and Castello PR (2009) Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol Metab 20:332-340.
56. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, and Melillo G (2004) Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res 64:1475-1482.
57. Ruas JL, Poellinger L, and Pereira T (2005) Role of CBP in regulating HIF-1-mediated activation of transcription. J Cell Sci 118:301-311.
58. Sar A, Ponjevic D, Nguyen M, Box AH, and Demetrick DJ (2009) Identification and characterization of demethylase JMJD1A as a gene upregulated in the human cellular response to hypoxia. Cell Tissue Res 337:223-234.
59. Schödel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, and Mole DR (2011) High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 117:e207-e217.
60. Schofield CJ and Zhang Z (1999) Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr Opin Struct Biol 9: 722-731.
61. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, SimonMC, Thompson CB, and Gottlieb E (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7:77-85.
62. Selivanov VA, Votyakova TV, Pivtoraiko VN, Zeak J, Sukhomlin T, Trucco M, Roca J, and Cascante M (2011) Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain. PLOS Comput Biol 7: e1001115.
63. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408.
64. Shibaji T, Nagao M, Ikeda N, Kanehiro H, Hisanaga M, Ko S, Fukumoto A, and Nakajima Y (2003) Prognostic significance of HIF-1 alpha overexpression in human pancreatic cancer. Anticancer Res 23:4721-4727.
65. Shimomura M, Hinoi T, Kuroda S, Adachi T, Kawaguchi Y, Sasada T, Takakura Y, Egi H, Okajima M, Tashiro H et al. (2013) Overexpression of hypoxia inducible factor-1 alpha is an independent risk factor for recurrence after curative resection of colorectal liver metastases. Ann Surg Oncol 20(Suppl 3):S527-S536.
66. Simon MC and Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9:285-296.
67. Sun HC, Qiu ZJ, Liu J, Sun J, Jiang T, Huang KJ, Yao M, and Huang C (2007a) Expression of hypoxia-inducible factor-1 alpha and associated proteins in pancreatic ductal adenocarcinoma and their impact on prognosis. Int J Oncol 30: 1359-1367.
68. Sun HL, Liu YN, Huang YT, Pan SL, Huang DY, Guh JH, Lee FY, Kuo SC, and Teng CM (2007b) YC-1 inhibits HIF-1 expression in prostate cancer cells: contribution of Akt/NF-kappaB signaling to HIF-1α accumulation during hypoxia. Oncogene 26:3941-3951.
69. Takahashi R, Tanaka S, Hiyama T, Ito M, Kitadai Y, Sumii M, Haruma K, and Chayama K (2003) Hypoxia-inducible factor-1alpha expression and angiogenesis in gastrointestinal stromal tumor of the stomach. Oncol Rep 10:797-802.
70. Tang CM and Yu J (2013) Hypoxia-inducible factor-1 as a therapeutic target in cancer. J Gastroenterol Hepatol 28:401-405.
71. Tanimoto K, Tsuchihara K, Kanai A, Arauchi T, Esumi H, Suzuki Y, and Sugano S (2010) Genome-wide identification and annotation of HIF-1α binding sites in two cell lines using massively parallel sequencing. Hugo J 4:35-48.
72. Theodoropoulos VE, Lazaris ACh, Sofras F, Gerzelis I, Tsoukala V, Ghikonti I, Manikas K, and Kastriotis I (2004) Hypoxia-inducible factor 1 alpha expression correlates with angiogenesis and unfavorable prognosis in bladder cancer. Eur Urol 46:200-208.
73. Vleugel MM, Greijer AE, Shvarts A, van der Groep P, van Berkel M, Aarbodem Y, van Tinteren H, Harris AL, van Diest PJ, and van der Wall E (2005) Differential prognostic impact of hypoxia induced and diffuse HIF-1α expression in invasive breast cancer. J Clin Pathol 58:172-177.
74. Winter SC, Shah KA, Han C, Campo L, Turley H, Leek R, Corbridge RJ, Cox GJ, and Harris AL (2006) The relation between hypoxia-inducible factor (HIF)-1alpha and HIF-2αlpha expression with anemia and outcome in surgically treated head and neck cancer. Cancer 107:757-766.
75. Xia X, Lemieux ME, Li W, Carroll JS, Brown M, Liu XS, and Kung AL (2009a) Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc Natl Acad Sci USA 106: 4260-4265.
76. Xia X, Lemieux ME, Li W, Carroll JS, Brown M, Liu XS, and Kung AL (2009b) Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis. Proc Natl Acad Sci USA 106:4260-4265.
77. Xia Y, Choi HK, and Lee K (2012) Recent advances in hypoxia-inducible factor (HIF)-1 inhibitors. Eur J Med Chem 49:24-40.
78. Yamamoto Y, Ibusuki M, Okumura Y, Kawasoe T, Kai K, Iyama K, and Iwase H (2008) Hypoxia-inducible factor 1alpha is closely linked to an aggressive phenotype in breast cancer. Breast Cancer Res Treat 110:465-475.
79. Yang J, Ledaki I, Turley H, Gatter KC, Montero JC, Li JL, and Harris AL (2009) Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases. Ann N Y Acad Sci 1177:185-197.
80. Zhang N, Fu Z, Linke S, Chicher J, Gorman JJ, Visk D, Haddad GG, Poellinger L, Peet DJ, and Powell F et al. (2010) The asparaginyl hydroxylase factor inhibiting HIF-1α is an essential regulator of metabolism. Cell Metab 11:364-378.
81. Zheng SS, Chen XH, Yin X, and Zhang BH (2013) Prognostic significance of HIF-1α expression in hepatocellular carcinoma: a meta-analysis. PLoS One 8:e65753.