Hypoxia-inducible factors and hypoxic cell death in tumour physiology

Annals of Medicine

Volumn 36, Issue 7, 2004, Pages 530-539

  Bacon, Andrea L ^a   Harris, Adrian L ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Apoptosis; BNIP3; Hypoxia inducible factor; Necrosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYPOXIA INDUCIBLE FACTOR 1;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO; FIBROSARCOMA; HYPOXIA; HYPOXIC CELL; MOUSE; NECROSIS; NONHUMAN; PRIORITY JOURNAL; REOXYGENATION; REVIEW; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL HYPOXIA; DNA-BINDING PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NECROSIS; NEOPLASMS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS;

EID: 8544271638     PISSN: 07853890     EISSN: None     Source Type: Journal    
DOI: 10.1080/07853890410018231     Document Type: Review

References (73)

1. Hockel M, Schienger K, Hockel S, Aral B, Schaffer U, Vaupel P. Tumor hypoxia in pelvic recurrences of cervical cancer. Int J Cancer 1998;79:365-9.
2. Stadler P, Becker A, Feldmann HJ, Hansgen G, Dunst J, Wurschmidt F, et al. Influence of the hypoxic subvolume on the survival of patients with head and neck cancer. Int J Radiat Oncol Biol Phys 1999;44:749-54.
3. Knowles HJ, Harris AL. Hypoxia and oxidative stress in breast cancer. Hypoxia and tumourigenesis. Breast Cancer Res 2001;3:318-22.
4. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47.
5. Dang CV, Semenza GL. Oncogenic alterations of metabolism. Trends Biochem Sci 1999;24:68-72.
6. Gatenby RA, Gawlinski ET. The glycolytic phenotype in carcinogenesis and tumor invasion: insights through mathematical models. Cancer Res 2003;63:3847-54.
7. Kajstura J, Cheng W, Sarangarajan R, Li P, Li B, Nitahara JA, et al. Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am J Physiol 1996;271:H1215-28.
8. Webster KA, Discher DJ, Kaiser S, Hernandez O, Sato B, Bishopric NH. Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J Clin Invest 1999;104:239-52.
9. Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 2001;93:266-76.
10. Beasley NJ, Leek R, Alam M, Turley H, Cox GJ, Gatter K, et al. Hypoxia-inducible factors HIF-1alpha and HIF-2alpha in head and neck cancer: relationship to tumor biology and treatment outcome in surgically resected patients. Cancer Res 2002;62:2493-7.
11. Tomes L, Emberley E, Niu Y, Troup S, Pastorek J, Strange K, et al. Necrosis and hypoxia in invasive breast carcinoma. Breast Cancer Res Treat 2003;81:61-9.
12. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 1999;15:551-78.
13. Maynard MA, Qi H, Chung J, Lee EH, Kondo Y, Hara S, et al. Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem 2003;278:11032-40.
14. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL, et al. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 1998;92:2260-8.
15. 2 tension. Proc Natl Acad Sci USA 1995;92:5510-4.
16. 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.
17. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294:1337-40.
18. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke 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.
19. O'Rourke JF, Dachs GU, Gleadle JM, Maxwell PH, Pugh CW, Stratford IJ, et al. Hypoxia response elements. Oncol Res 1997;9:327-32.
20. Sowter HM, Ferguson M, Pym C, Watson P, Fox SB, Han C, et al. Expression of the cell death genes BNip3 and NIX in ductal carcinoma in situ of the breast; correlation of BNip3 levels with necrosis and grade. J Pathol 2003;201:573-80.
21. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 1998;17:3005-15.
22. Kotch LE, Iyer NV, Laughner E, Semenza GL. Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev Biol 1999;209:254-67.
23. Peng J, Zhang L, Drysdale L, Fong GH. The transcription factor EPAS-1/hypoxia-inducible factor 2alpha plays an important role in vascular remodeling. Proc Natl Acad Sci USA 2000;97:8386-91.
24. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, et al. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002;8:702-10.
25. Tian H, Hammer RE, Matsumoto AM, Russell DW, McKnight SL. The fresponsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 1998;12:3320-4.
26. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1 alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003;23:9361-74.
27. Hara S, Hamada J, Kobayashi C, Kondo Y, Imura N. Expression and characterization of hypoxia-inducible factor (HIF)-3alpha in human kidney: suppression of HIF-mediated gene expression by HIF-3alpha. Biochem Biophys Res Commun 2001;287:808-13.
28. Makino Y, Cao R, 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;414:550-4.
29. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003;9:677-84.
30. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-61.
31. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, et al. Hypoxia inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res 2000;60:4010-5.
32. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ, et al. Hypoxia-inducible factor-1 modulates gène expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci USA 1997;94:8104-9.
33. Erez N, Milyavsky M, Eilam R, Shats I, Goldfinger N, Rotter V. Expression of prolyl-hydroxylase-1 (PHD1/EGLN2) suppresses hypoxia-inducible factor-1alpha activation and inhibits tumor growth. Cancer Res 2003;63:8777-83.
34. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998;394:485-90.
35. Halterman MW, Miller CC, Federoff HJ. Hypoxia-inducible factor-lalpha mediates hypoxia-induced delayed neuronal death that involves p53. J Neurosci 1999;19:6818-24.
36. Mack FA, Rathmell WK, Arsham AM, Gnarra J, Keith B, Simon MC. Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth. Cancer Cell 2003;3:75-88.
37. Blouw B, Song H, Tihan T, Bosze J, Ferrara N, Gerber HP, et al. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003;4:133-46.
38. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res 2001;61:6669-73.
39. Wykoff CC, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. Identification of novel hypoxia-dependent and independent target genes of the von Hippel-Lindau (VHL) tumour suppressor by mRNA differential expression profiling. Oncogene 2000;19:6297-305.
40. Koong AC, Denko NC, Hudson KM, Schindler C, Swiersz L, Koch C, et al. Candidate genes for the hypoxic tumor phenotype. Cancer Res 2000;60:883-7.
41. Denko NC, Fontana LA, Hudson KM, Sutphin PD, Raychaudhuri S, Altman R, et al. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 2003;22:5907-14.
42. Rajah R, Valentinis B, Cohen P. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-beta1 on programmed cell death through a p53- and IGF-independent mechanism. J Biol Chem 1997;272:12181-8.
43. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996;379:88-91.
44. Graeber TG, Peterson JF, Tsai M, Monica K, Fornace AJ, Jr, Giaccia AJ. Hypoxia induces accumulation of p53 protein, but activation of a G1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 1994;14:6264-77.
45. Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem Soc Trans 2001;29:684-8.
46. An WG, Kanekal M, Simon MC, Maltepe E, Blagosklonny MV, Neckers LM. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 1998;392:405-8.
47. Suzuki H, Tomida A, Tsuruo T. Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia. Oncogene 2001;20:5779-88.
48. Wenger RH, Camenisch G, Desbaillets I, Chilov D, Gassmann M. Up-regulation of hypoxia-inducible factor-1alpha is not sufficient for hypoxic/anoxic p53 induction. Cancer Res 1998;58:5678-80.
49. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, et al. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Ceil Biol 2000;20:5454-68.
50. Ray R, Chen G, Vande Velde C, Cizeau J, Park JH, Reed JC, et al. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J Biol Chem 2000;275:1439-48.
51. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 ptotein is induced by hypoxia. Proc Natl Acad Sci USA 2000;97:9082-7.
52. Kothan S, Cizeau J, McMillan-Ward E, Israels SJ, Bailes M, Ens K, et al. BNIP3 plays a role in hypoxic cell death in human epithelial cells that is inhibited by growth factors EGF and IGF. Oncogene 2003;22:4734-44.
53. Kim JY, Park JH. ROS-dependent caspase-9 activation in hypoxic cell death. FEBS Lett 2003;549:94-8.
54. Chen G, Ray R, Dubik D, Shi L, Cizeau J, Bleackley RC, et al. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 1997;186:1975-83.
55. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000;288:1053-8.
56. Lal A, Peters H, St Croix B, Haroon ZA, Dewhirst MW, Strausberg RL, et al. Transcriptional response to hypoxia in human tumors. J Natl Cancer Inst 2001;93:1337-43.
57. Tazuke SI, Mazure NM, Sugawara J, Garland G, Faessen GH, Suen LF, et al. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc Natl Acad Sci USA 1998;95:10188-93.
58. Chang YS, Wang L, Liu D, Mao L, Hong WK, Khuri FR, et al. Correlation between insulin-like growth factor-binding protein-3 promoter methylation and prognosis of patients with stage I non-small cell lung cancer. Clin Cancer Res 2002;8:3669-75.
59. Parkkila S, Rajaniemi H, Parkkila AK, Kivela J, Waheed A, Pastorekova S, et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci USA 2000;97:2220-4.
60. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 2002;99:12825-30.
61. Saitoh Y, Ouchida R, Miwa N. Bcl-2 prevents hypoxia/ reoxygenation- induced cell death through suppressed generation of reactive oxygen species and upregulation of Bcl-2 proteins. J Cell Biochem 2003;90:914-24.
62. Zhivotovsky B. Apoptosis, necrosis and between. Cell Cycle 2004;3:64-6.
63. Shimizu S, Eguchi Y, Kamiike W, Itoh Y, Hasegawa J, Yamabe K, et al. Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-XL. Cancer Res 1996;56:2161-6.
64. Stembach JP, Wolburg H, Klumpp A, Probst H, Weller M. Hypoxia induced cell death in human malignant glioma cells: energy deprivation promotes decoupling of mitochondrial cytochrome c release from caspase processing and necrotic cell death. Cell Death Differ 2003;10:823-32.
65. Tatsumi T, Shiraishi J, Keira N, Akashi K, Mano A, Yamanaka S, et al. Intracellular ATP is required for mitochondrial apoptotic pathways in isolated hypoxic rat cardiac myocytes. Cardiovasc Res 2003;59:428-40.
66. Nowell PC. The clonal evolution of tumor cell populations. Science 1976;194:23-8.
67. Yuan J, Narayanan L, Rockwell S, Glazer PM. Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Res 2000;60:4372-6.
68. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997;88:323-31.
69. Yu JL, Rak JW, Coomber BL, Hicklin DJ, Kerbel RS. Effect of p53 status on tumor response to antiangiogenic therapy. Science 2002;295:1526-8.
70. Hanafusa T, Yumoto Y, Nouso K, Nakatsukasa H, Onishi T, Fujikawa T, et al. Reduced expression of insulin-like growth factor binding protein-3 and its promoter hypermethylation in human hepatocellular carcinoma. Cancer Lett 2002;176:149-58.
71. Kumar CC. Signaling by integrin receptors. Oncogene 1998;17:1365-73.
72. Furstenberger G, Senn HJ. Insulin-like growth factors and cancer. Lancet Oncol 2002;3:298-302.
73. Oehler MK, Norbury C, Hague S, Rees MC, Bicknell R. Adrenomedullin inhibits hypoxic cell death by upregulation of Bcl-2 in endometrial cancer cells; a possible promotion mechanism for tumour growth. Oncogene 2001;20:2937-45.