HIF-1α pathway: Role, regulation and intervention for cancer therapy

Acta Pharmaceutica Sinica B

Volumn 5, Issue 5, 2015, Pages 378-389

  Masoud, Georgina N ^a   Li, Wei ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Cancer drug discovery and development; HIF 1 ; HIF 1 inhibitors

Indexed keywords

2 METHOXYESTRA 1,3,5(10),16 TETRAENE 3 CARBOXAMIDE; 2 METHOXYESTRADIOL; 2 MORPHOLINO 8 PHENYLCHROMONE; ALVESPIMYCIN; AMINOFLAVONE; ANTISENSE OLIGONUCLEOTIDE; DIGOXIN; ENMD 1200; ENMD 1237; EVEROLIMUS; EZN 2698; FIRTECAN; FIRTECAN PEGOL; FLAVONE DERIVATIVE; GELDANAMYCIN; GROWTH FACTOR; HEAT SHOCK PROTEIN 90; HYPOXIA INDUCIBLE FACTOR 1; IPI 493; IRINOTECAN; MESSENGER RNA; OUABAIN; PROSCILLARIDIN; PROTEIN MDM2; RAPAMYCIN; TEMSIROLIMUS; TOPOTECAN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VON HIPPEL LINDAU PROTEIN; WORTMANNIN;

ADVANCED CANCER; CANCER CELL LINE; CANCER THERAPY; CELL HYPOXIA; CELL STRESS; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG RESPONSE; DRUG TARGETING; HUMAN; HYDROXYLATION; KIDNEY CARCINOMA; LYMPHOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RECTUM CANCER; REGULATORY MECHANISM; REVIEW; SOLID TUMOR;

EID: 84947202428     PISSN: 22113835     EISSN: 22113843     Source Type: Journal    
DOI: 10.1016/j.apsb.2015.05.007     Document Type: Review

References (87)

1. Semenza GL. HIF-1 and human disease: one highly involved factor. Genes Dev 2000, 14:1983-1991.
2. Powis G, Kirkpatrick L. Hypoxia inducible factor-1alpha as a cancer drug target. Mol Cancer Ther 2004, 3:647-654.
3. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 2008, 8:705-713.
4. Ke QD, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006, 70:1469-1480.
5. Patiar S, Harris AL. Role of hypoxia-inducible factor-1alpha as a cancer therapy target. Endocr Relat Cancer 2006, 13(Suppl 1):61-75.
6. Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med 2002, 8:S62-S67.
7. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732.
8. Xia Y, Choi H-K, Lee K. Recent advances in hypoxia-inducible factor (HIF)-1 inhibitors. Eur J Med Chem 2012, 49:24-40.
9. Bárdos JI, Ashcroft M. Negative and positive regulation of HIF-1: a complex network. Biochim Biophys Acta 2005, 1755:107-120.
10. Minet E, Michel G, Mottet D, Raes M, Michiels C. Transduction pathways involved in hypoxia-inducible factor-1 phosphorylation and activation. Free Radic Biol Med 2001, 31:847-855.
11. Semenza GL. HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 2001, 13:167-171.
12. Weinhouse S, Warburg O, Burk D, Schade AL. On respiratory impairment in cancer cells. Science 1956, 124:267-272.
13. Conway EM, Collen D, Carmeliet P. Molecular mechanisms of blood vessel growth. Cardiovasc Res 2001, 49:507-521.
14. Laderoute KR, Calaoagan JM, Gustafson-Brown C, Knapp AM, Li GC, Mendonca HL, et al. The response of c-Jun/AP-1 to chronic hypoxia is hypoxia-inducible factor 1α dependent. Mol Cell Biol 2002, 22:2515-2523.
15. Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE. Hypoxia-inducible nuclear factors bind to an enhancer element located 3[U+02B9] to the human erythropoietin gene. Proc Natl Acad Sci USA 1991, 88:5680-5684.
16. Goldberg MA, Dunning SP, Bunn HF. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 1988, 242:1412-1415.
17. 2 tension. Proc Natl Acad Sci USA 1995, 92:5510-5514.
18. Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 1996, 271:17771-17778.
19. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995, 270:1230-1237.
20. Li H, Ko HP, Whitlock JP. Induction of phosphoglycerate kinase 1 gene expression by hypoxia. Roles of Arnt and HIF1α. J Biol Chem 1996, 271:21262-21267.
21. Yamashita K, Discher DJ, Hu J, Bishopric NH, Webster KA. Molecular regulation of the endothelin-1 gene by hypoxia. Contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2, AND p300/CBP. J Biol Chem 2001, 276:12645-12653.
22. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
23. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 1997, 94:4273-4278.
24. Makino Y, Cao RH, Svensson K, Bertilsson G, Asman M, Tanaka H, et al. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 2001, 414:550-554.
25. Kallio PJ, Pongratz I, Gradin K, McGuire J, Poellinger L. Activation of hypoxia-inducible factor 1α: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc Natl Acad Sci USA 1997, 94:5667-5672.
26. Salceda S, Caro J. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 1997, 272:22642-22647.
27. Iwai K, Yamanaka K, Kamura T, Minato N, Conaway RC, Conaway JW, et al. Identification of the von Hippel-Lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex. Proc Natl Acad Sci USA 1999, 96:12436-12441.
28. Epstein ACR, Gleadle JM, McNeill LA, Hewitson KS, ORourke J, Mole DR, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
29. Jeong J-W, Bae M-K, Ahn M-Y, Kim S-H, Sohn T-K, Bae M-H, et al. Regulation and destabilization of HIF-1α by ARD1-mediated acetylation. Cell 2002, 111:709-720.
30. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
31. Block KM, Wang H, Szabó LZ, Polaske NW, Henchey LK, Dubey R, et al. Direct inhibition of hypoxia-inducible transcription factor complex with designed dimeric epidithiodiketopiperazine. J Am Chem Soc 2009, 131:18078-18088.
32. Dann CE, Bruick RK, Deisenhofer J. Structure of factor-inhibiting hypoxia-inducible factor 1: an asparaginyl hydroxylase involved in the hypoxic response pathway. Proc Natl Acad Sci USA 2002, 99:15351-15356.
33. 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, 16:1466-1471.
34. McNeill LA, Hewitson KS, Claridge TD, Seibel JF, Horsfall LE, Schofield CJ. Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the β-carbon of asparagine-803. Biochem J 2002, 367:571-575.
35. Jiang BH, Jiang G, Zheng JZ, Lu Z, Hunter T, Vogt PK. Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ 2001, 12:363-369.
36. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 2002, 64:993-998.
37. Conrad PW, Freeman TL, Beitner-Johnson D, Millhorn DE. EPAS1 trans-activation during hypoxia requires p42/p44 MAPK. J Biol Chem 1999, 274:33709-33713.
38. Gingras A-C, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001, 15:807-826.
39. Sang N, Stiehl DP, Bohensky J, Leshchinsky I, Srinivas V, Caro J. MAPK signaling up-regulates the activity of hypoxia-inducible factors by its effects on p300. J Biol Chem 2003, 278:14013-14019.
40. Bae M-K, Ahn M-Y, Jeong J-W, Bae M-H, Lee YM, Bae S-K, et al. Jab1 interacts directly with HIF-1α and regulates its stability. J Biol Chem 2002, 277:9-12.
41. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, et al. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev 2000, 14:34-44.
42. Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J Biol Chem 2002, 277:29936-29944.
43. Gradin K, McGuire J, Wenger RH, Kvietikova I, fhitelaw ML, Toftgård R, et al. Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol Cell Biol 1996, 16:5221-5231.
44. Melillo G. Hypoxia-inducible factor 1 inhibitors. Methods Enzymol 2007, 435:385-402.
45. Rapisarda A, Uranchimeg B, Scudiero DA, Selby M, Sausville EA, Shoemaker RH, et al. Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 2002, 62:4316-4324.
46. Chau N-M, Rogers P, Aherne W, Carroll V, Collins I, McDonald E, et al. Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1α induction in response to hypoxic stress and growth factors. Cancer Res 2005, 65:4918-4928.
47. Kaluz S, Kaluzová M, Stanbridge EJ. Proteasomal inhibition attenuates transcriptional activity of hypoxia-inducible factor 1 (HIF-1) via specific effect on the HIF-1α C-terminal activation domain. Mol Cell Biol 2006, 26:5895-5907.
48. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res 2004, 64:1475-1482.
49. Kong DH, Park EJ, Stephen AG, Calvani M, Cardellina JH, Monks A, et al. Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res 2005, 65:9047-9055.
50. Park J-E, Kong DH, Fisher R, Cardellina J, Shoemaker RH, Melillo G. Targeting the PAS-A domain of HIF-1alpha for development of small molecule inhibitors of HIF-1. Cell Cycle 2006, 5:1847-1853.
51. Kung AL, Zabludoff SD, France DS, Freedman SJ, Tanner EA, Vieira A, et al. Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway. Cancer Cell 2004, 6:33-43.
52. Greenberger LM, Horak ID, Filpula D, Sapra P, Westergaard M, Frydenlund HF, et al. A RNA antagonist of hypoxia-inducible factor-1α, EZN-2968, inhibits tumor cell growth. Mol Cancer Ther 2008, 7:3598-3608.
53. Onnis B, Rapisarda A, Melillo G. Development of HIF-1 inhibitors for cancer therapy. J Cell Mol Med 2009, 13:2780-2786.
54. Rapisarda A, Hollingshead M, Uranchimeg B, Bonomi CA, Borgel SD, Carter JP, et al. Increased antitumor activity of bevacizumab in combination with hypoxia inducible factor-1 inhibition. Mol Cancer Ther 2009, 8:1867-1877.
55. Hsiang YH, Hertzberg R, Hecht S, Liu LF. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J Biol Chem 1985, 260:14873-14878.
56. Sapra P, Zhao H, Mehlig M, Malaby J, Kraft P, Longley C, et al. Novel delivery of SN38 markedly inhibits tumor growth in xenografts, including a camptothecin-11-refractory model. Clin Cancer Res 2008, 14:1888-1896.
57. Del Bufalo D, Ciuffreda L, Trisciuoglio D, Desideri M, Cognetti F, Zupi G, et al. Antiangiogenic potential of the mammalian target of rapamycin inhibitor temsirolimus. Cancer Res 2006, 66:5549-5554.
58. Kaelin WG The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res 2007, 13. 680-4s.
59. Ravaud A, Bernhard JC, Gross-Goupil M, Digue L, Ferriere JM. mTOR inhibitors: temsirolimus and everolimus in the treatment of renal cell carcinoma. Bull Cancer 2010, 97:45-51.
60. Zhang HF, Qian DZ, Tan YS, Lee K, Gao P, Ren YR, et al. Digoxin and other cardiac glycosides inhibit HIF-1α synthesis and block tumor growth. Proc Natl Acad Sci USA 2008, 105:19579-19586.
61. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 2003, 3:363-375.
62. LaVallee TM, Burke PA, Swartz GM, Hamel E, Agoston GE, Shah J, et al. Significant antitumor activity in vivo following treatment with the microtubule agent ENMD-1198. Mol Cancer Ther 2008, 7:1472-1482.
63. Hur E, Kim HH, Choi SM, Kim JH, Yim S, Kwon HJ, et al. Reduction of hypoxia-induced transcription through the repression of hypoxia-inducible factor-1α/aryl hydrocarbon receptor nuclear translocator DNA binding by the 90-kDa heat-shock protein inhibitor radicicol. Mol Pharmacol 2002, 62:975-982.
64. Porter JR, Ge J, Lee J, Normant E, West K. Ansamycin inhibitors of Hsp90: nature[U+05F3]s prototype for anti-chaperone therapy. Curr Top Med Chem 2009, 9:1386-1418.
65. Kurebayashi J, Otsuki T, Kurosumi M, Soga S, Akinaga S, Sonoo H. A radicicol derivative, KF58333, inhibits expression of hypoxia-inducible factor-1alpha and vascular endothelial growth factor, angiogenesis and growth of human breast cancer xenografts. Jpn J Cancer Res 2001, 92:1342-1351.
66. Han JY, Oh SH, Morgillo F, Myers JN, Kim E, Hong WK, et al. Hypoxia-inducible factor 1α and antiangiogenic activity of farnesyltransferase inhibitor SCH66336 in human aerodigestive tract cancer. J Natl Cancer Inst 2005, 97:1272-1286.
67. Osada M, Imaoka S, Funae Y. Apigenin suppresses the expression of VEGF, an important factor for angiogenesis, in endothelial cells via degradation of HIF-1α protein. FEBS Lett 2004, 575:59-63.
68. Melstrom LG, Salabat MR, Ding XZ, Strouch MJ, Grippo PJ, Mirzoeva S, et al. Apigenin down-regulates the hypoxia response genes: HIF-1α, GLUT-1, and VEGF in human pancreatic cancer cells. J Surg Res 2011, 167:173-181.
69. Lim JH, Lee YM, Chun YS, Chen JJ, Kim JE, Park JW. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1α. Mol Cell 2010, 38:864-878.
70. Ueda H, Nakajima H, Hori Y, Fujita T, Nishimura M, Goto T, et al. FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968 I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. J Antibiot 1994, 47:301-310.
71. Furumai R, Matsuyama A, Kobashi N, Lee KH, Nishiyama M, Nakajima H, et al. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res 2002, 62:4916-4921.
72. Kong XG, Lin Z, Liang DM, Fath D, Sang NL, Caro J. Histone deacetylase inhibitors induce VHL and ubiquitin-independent proteasomal degradation of hypoxia-inducible factor 1α. Mol Cell Biol 2006, 26:2019-2028.
73. Lee K, Kang JE, Park SK, Jin YL, Chung KS, Kim HM, et al. LW6, a novel HIF-1 inhibitor, promotes proteasomal degradation of HIF-1α via upregulation of VHL in a colon cancer cell line. Biochem Pharmacol 2010, 80:982-989.
74. Lee K, Zhang HF, Qian DZ, Rey S, Liu JO, Semenza GL. Acriflavine inhibits HIF-1 dimerization, tumor growth, and vascularization. Proc Natl Acad Sci USA 2009, 106:17910-17915.
75. Lee K, Qian DZ, Rey S, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci USA 2009, 106:2353-2358.
76. Vergis R, Corbishley CM, Norman AR, Bartlett J, Jhavar S, Borre M, et al. Intrinsic markers of tumour hypoxia and angiogenesis in localised prostate cancer and outcome of radical treatment: a retrospective analysis of two randomised radiotherapy trials and one surgical cohort study. Lancet Oncol 2008, 9:342-351.
77. Staab A, Loeffler J, Said HM, Diehlmann D, Katzer A, Beyer M, et al. Effects of HIF-1 inhibition by chetomin on hypoxia-related transcription and radiosensitivity in HT 1080 human fibrosarcoma cells. BMC Cancer 2007, 7:213.
78. Richardson PG, Hideshima T, Anderson KC. Bortezomib (PS-341): a novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Control 2003, 10:361-369.
79. Befani CD, Vlachostergios PJ, Hatzidaki E, Patrikidou A, Bonanou S, Simos G, et al. Bortezomib represses HIF-1α protein expression and nuclear accumulation by inhibiting both PI3K/Akt/TOR and MAPK pathways in prostate cancer cells. J Mol Med 2012, 90:45-54.
80. Goda AE, Erikson RL, Sakai T, Ahn JS, Kim BY. Preclinical evaluation of bortezomib/dipyridamole novel combination as a potential therapeutic modality for hematologic malignancies. Mol Oncol 2015, 9:309-322.
81. Zhang BL, Gu Y. Bortezomib inhibits gastric carcinoma HGC-27 cells through the phospho-Jun N-terminal kinase (p-JNK) pathway in vitro. Gene 2015, 559:164-171.
82. Huang B, Li J, Xu X, Zheng D, Zhou Z, Liu J. Successful treatment of renal light chain (AL) amyloidosis with bortezomib and dexamethasone (VD). Pathol Biol 2015, 63:17-20.
83. Ko FN, Wu CC, Kuo SC, Lee FY, Teng CM. YC-1, a novel activator of platelet guanylate cyclase. Blood 1994, 84:4226-4233.
84. Li SH, Shin DH, Chun YS, Lee MK, Kim MS, Park JW. A novel mode of action of YC-1 in HIF inhibition: stimulation of FIH-dependent p300 dissociation from HIF-1α. Mol Cancer Ther 2008, 7:3729-3738.
85. Chun YS, Yeo EJ, Choi E, Teng CM, Bae JM, Kim MS, et al. Inhibitory effect of YC-1 on the hypoxic induction of erythropoietin and vascular endothelial growth factor in Hep3B cells. Biochem Pharmacol 2001, 61:947-954.
86. Park JW, Chun Y-G, Bair K, Cho HS, inventors; HIF Bio, Inc., assignee. Compound for treating angiogenesis. US patent 7,226,941. 2007 Jun 5.
87. Koh MY, Spivak-Kroizman T, Venturini S, Welsh S, Williams RR, Kirkpatrick DL, et al. Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1α. Mol Cancer Ther 2008, 7:90-100.