Intermittent induction of HIF-1α produces lasting effects on malignant progression independent of its continued expression

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Choi, Hyunsung ^a   Gillespie, David L ^a   Berg, Shauna ^a   Rice, Christopher ^a   Couldwell, Sandrine ^a   Gu, Jie ^a   Colman, Howard ^a   Jensen, Randy L ^a   Huang, L Eric ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; TETRACYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENICITY; CELL INVASION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; BRAIN; CARCINOGENESIS; CELL TRANSFORMATION; DISEASE COURSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PATHOLOGY; TRANSGENE; TUMOR CELL LINE; TUMOR INVASION;

MUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CARCINOGENESIS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MUTATION; NEOPLASM INVASIVENESS; TETRACYCLINE; TRANSGENES;

EID: 84928804016     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125125     Document Type: Article

References (64)

1. Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE. Hypoxia-inducible nuclear factors bind to an enhancer element located 3' to the human erythropoietin gene. Proc Natl Acad Sci USA 1991; 88:5680-4. PMID: 2062846
2. Maxwell PH, Pugh CW, Ratcliffe PJ. Activation of the HIF pathway in cancer. Curr Opin Genet Dev 2001; 11:293-9. PMID: 11377966
3. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002; 2:38-47. PMID: 11902584
4. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3:721-32. PMID: 13130303
5. Giaccia A, Siim BG, Johnson RS. HIF-1 as a target for drug development. Nat Rev Drug Discov 2003; 2:803-11. PMID: 14526383
6. Pouysségur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006; 441:437-43. PMID: 16724055
7. Bertout JA, Patel SA, Simon MC. The impact of O2 availability on human cancer. Nat Rev Cancer 2008; 8:967-75. doi: 10.1038/nrc2540 PMID: 18987634
8. Rice C, Huang LE. From antiangiogenesis to hypoxia: current research and future directions. Cancer Manag Res 2010; 3:9-16. doi: 10.2147/CMR.S14812 PMID: 21407995
9. Tiburcio PD, Choi H, Huang LE. Complex role of HIF in cancer: the known, the unknown, and the unexpected. Hypoxia 2014; 2:59-70.
10. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995; 92:5510-4. PMID: 7539918
11. Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 1996; 271:32253-9. PMID: 8943284
12. Pugh CW, O'Rourke JF, Nagao M, Gleadle JM, Ratcliffe PJ. Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit. J Biol Chem 1997; 272:11205-14. PMID: 9111021
13. Salceda S, Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) 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; 272:22642-7. PMID: 9278421
14. Huang LE, Gu J, Schau M, Bunn HF. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 1998; 95:7987-92. PMID: 9653127
15. 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; 399:271-5. PMID: 10353251
16. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, et al. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2000; 2:423-7. PMID: 10878807
17. Tanimoto K, Makino Y, Pereira T, Poellinger L. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J 2000; 19:4298-309. PMID: 10944113
18. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001; 292:464-8. PMID: 11292862
19. 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. PMID: 11292861
20. Yu F, White SB, Zhao Q, Lee FS. HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 2001; 98:9630-5. PMID: 11504942
21. 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. PMID: 9000051
22. Ema M, Hirota K, Mimura J, Abe H, Yodoi J, Sogawa K, et al. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 1999; 18:1905-14. PMID: 10202154
23. Rankin EB, Giaccia AJ. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ 2008; 15:678-85. doi: 10.1038/cdd.2008.21 PMID: 18259193
24. Hu C-J, Wang L-Y, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003; 23:9361-74. PMID: 14645546
25. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. Differential gene up-regulation by hypoxiainducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res 2005; 65:3299-306. PMID: 15833863
26. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2011; 12:9-22. doi: 10.1038/nrc3183 PMID: 22169972
27. Huang LE. Carrot and stick: HIF-alpha engages c-Myc in hypoxic adaptation. Cell Death Differ 2008; 15:672-7. doi: 10.1038/sj.cdd.4402302 PMID: 18188166
28. Huang LE. How HIF-1α Handles Stress. Science 2013; 339:1285-6. doi: 10.1126/science.1236966 PMID: 23493703
29. Acker T, Diez-Juan A, Aragonés J, Tjwa M, Brusselmans K, Moons L, et al. Genetic evidence for a tumor suppressor role of HIF-2alpha. Cancer Cell 2005; 8:131-41. PMID: 16098466
30. Mazumdar J, Hickey MM, Pant DK, Durham AC, Sweet-Cordero A, Vachani A, et al. HIF-2alpha deletion promotes Kras-driven lung tumor development. Proc Natl Acad Sci USA 2010; 107:14182-7. doi: 10.1073/pnas.1001296107 PMID: 20660313
31. Sun H-X, Xu Y, Yang X-R, Wang W-M, Bai H, Shi R-Y, et al. Hypoxia inducible factor 2 alpha inhibits hepatocellular carcinoma growth through the transcription factor dimerization partner 3/ E2F transcription factor 1-dependent apoptotic pathway. Hepatology 2013; 57:1088-97. doi: 10.1002/hep.26188 PMID: 23212661
32. Kaelin WG. Von Hippel-Lindau disease. Annu Rev Pathol Mech Dis 2007; 2:145-73. PMID: 18039096
33. Purdue MP, Johansson M, Zelenika D, Toro JR, Scelo G, Moore LE, et al. Genome-wide association study of renal cell carcinoma identifies two susceptibility loci on 2p21 and 11q13.3. Nat Genet 2011; 43:60-5. doi: 10.1038/ng.723 PMID: 21131975
34. Zhuang Z, Yang C, Lorenzo F, Merino M, Fojo T, Kebebew E, et al. Somatic HIF2AGain-of-Function Mutations in Paraganglioma with Polycythemia. N Engl J Med 2012; 367:922-30. doi: 10.1056/ NEJMoa1205119 PMID: 22931260
35. Shen C, Beroukhim R, Schumacher SE, Zhou J, Chang M, Signoretti S, et al. Genetic and functional studies implicate HIF1α as a 14q kidney cancer suppressor gene. Cancer Discov 2011; 1:222-35. doi: 10.1158/2159-8290.CD-11-0098 PMID: 22037472
36. Kageyama Y, Koshiji M, To KK-W, Tian Y-M, Ratcliffe PJ, Huang LE. Leu-574 of human HIF-1alpha is a molecular determinant of prolyl hydroxylation. FASEB J 2004; 18:1028-30. PMID: 15084514
37. Hayashi M, Yoo Y-G, Christensen J, Huang LE. Requirement of evading apoptosis for HIF-1alphainduced malignant progression in mouse cells. Cell Cycle 2011; 10:1-9. PMID: 21191187
38. Bhat KPL, Salazar KL, Balasubramaniyan V, Wani K, Heathcock L, Hollingsworth F, et al. The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma. Genes Dev 2011; 25:2594-609. doi: 10.1101/gad.176800.111 PMID: 22190458
39. Dayan F, Roux D, Brahimi-Horn MC, Pouysségur J, Mazure NM. The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1alpha. Cancer Res 2006; 66:3688-98. PMID: 16585195
40. Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 1994; 269:23757-63. PMID: 8089148
41. Mazure NM, Chen EY, Yeh P, Laderoute KR, Giaccia AJ. Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res 1996; 56:3436-40. PMID: 8758908
42. Erler JT, Bennewith KL, Nicolau M, Dornhöfer N, Kong C, Le Q-T, et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006; 440:1222-6. PMID: 16642001
43. Young SD, Marshall RS, Hill RP. Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc Natl Acad Sci USA 1988; 85:9533-7. PMID: 3200838
44. Rofstad EK, Danielsen T. Hypoxia-induced metastasis of human melanoma cells: involvement of vascular endothelial growth factor-mediated angiogenesis. Br J Cancer 1999; 80:1697-707. PMID: 10468285
45. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 2001; 61:8903-8. PMID: 11751415
46. Toffoli S, Michiels C. Intermittent hypoxia is a key regulator of cancer cell and endothelial cell interplay in tumours. FEBS J 2008; 275:2991-3002. doi: 10.1111/j.1742-4658.2008.06454.x PMID: 18445039
47. Martinive P, Defresne F, Bouzin C, Saliez J, Lair F, Grégoire V, et al. Preconditioning of the tumor vasculature and tumor cells by intermittent hypoxia: implications for anticancer therapies. Cancer Res 2006; 66:11736-44. PMID: 17178869
48. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114:97-109. PMID: 17618441
49. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 2004; 23:1949-56. PMID: 15071503
50. Hubbi ME, Kshitiz, Gilkes DM, Rey S, Wong CC, Luo W, et al. A Nontranscriptional Role for HIF-1 as a Direct Inhibitor of DNA Replication. Sci Signal 2013; 6:ra10. doi: 10.1126/scisignal.2003417 PMID: 23405012
51. Gordan JD, Bertout JA, Hu C-J, Diehl JA, Simon MC. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007; 11:335-47. PMID: 17418410
52. Raval RR, Lau KW, Tran MGB, Sowter HM, Mandriota SJ, Li J-L, et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 2005; 25:5675-86. PMID: 15964822
53. Mack FA, Patel JH, Biju MP, Haase VH, Simon MC. Decreased growth of Vhl-/- fibrosarcomas is associated with elevated levels of cyclin kinase inhibitors p21 and p27. Mol Cell Biol 2005; 25:4565-78. PMID: 15899860
54. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol Mech Dis 2006; 1:97-117. PMID: 18039109
55. Carro MS, Lim WK, Alvarez MJ, Bollo RJ, Zhao X, Snyder EY, et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010; 463:318-25. doi: 10.1038/nature08712 PMID: 20032975
56. Lee CG, Da Silva CA, Cruz Dela CS, Ahangari F, Ma B, Kang M-J, et al. Role of chitin and chitinase/ chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 2011; 73:479-501. doi: 10.1146/annurev-physiol-012110-142250 PMID: 21054166
57. Nigro JM, Misra A, Zhang L, Smirnov I, Colman H, Griffin C, et al. Integrated array-comparative genomic hybridization and expression array profiles identify clinically relevant molecular subtypes of glioblastoma. Cancer Res 2005; 65:1678-86. PMID: 15753362
58. Ku BM, Lee YK, Ryu J, Jeong JY, Choi J, Eun KM, et al. CHI3L1 (YKL-40) is expressed in human gliomas and regulates the invasion, growth and survival of glioma cells. Int J Cancer 2011; 128:1316-26. doi: 10.1002/ijc.25466 PMID: 20506295
59. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9:157-73. PMID: 16530701
60. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17:98-110. doi: 10.1016/j.ccr.2009.12.020 PMID: 20129251
61. Jensen RL. Hypoxia in the tumorigenesis of gliomas and as a potential target for therapeutic measures. Neurosurg Focus 2006; 20:E24. PMID: 16709030
62. Rapisarda A, Melillo G. Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia. Nat Rev Clin Oncol 2012; 9:378-90. doi: 10.1038/nrclinonc.2012.64 PMID: 22525710
63. Young RM, Simon MC. Untuning the tumor metabolic machine: HIF-α: pro- and antitumorigenic? Nat Med 2012; 18:1024-5. doi: 10.1038/nm.2865 PMID: 22772556
64. Huang LE. Targeting HIF-α: when a magic arrow hits the bull's eye. Drug Discov Today 2004; 9:869. PMID: 15493075