The HIF pathway in cancer

Seminars in Cell and Developmental Biology

Volumn 16, Issue 4-5, 2005, Pages 523-530

  Maxwell, Patrick H ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Angiogenesis; Cancer; HIF; Hypoxia; VHL

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOPROTEIN; OXYGEN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TUMOR SUPPRESSOR PROTEIN; VON HIPPEL LINDAU PROTEIN;

ANGIOGENESIS; CANCER; CANCER GENETICS; CANCER THERAPY; CARCINOGENESIS; CELL SPECIFICITY; CELL TYPE; CLEAR CELL CARCINOMA; CONCENTRATION (PARAMETERS); DRUG TARGETING; GENE EXPRESSION; KIDNEY CARCINOMA; KIDNEY EPITHELIUM; ONCOGENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 24344488419     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2005.03.001     Document Type: Review

References (66)

1. 2 tension Proc Natl Acad Sci USA 92 1995 5510 5514
2. P.H. Maxwell, M.S. Wiesener, G.-W. Chang, S.C. Clifford, E.C. Vaux, and M.E. Cockman The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 1999 271 275
3. W.G. Kaelin Molecular basis of the VHL hereditary cancer syndrome Nat Rev Cancer 2 2002 673 682
4. A.L. Harris Hypoxia - a key regulatory factor in tumour growth Nat Rev Cancer 2 2002 38 47
5. D. Shweiki, A. Itin, D. Soffer, and E. Keshet Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis Nature 359 1992 843 845
6. M.S. Wiesener, P.M. Munchenhagen, I. Berger, N.V. Morgan, J. Roigas, and A. Schwiertz Constitutive activation of hypoxia-inducible genes related to overexpression of hypoxia-inducible factor-1alpha in clear cell renal carcinomas Cancer Res 61 2001 5215 5222
7. P. Carmeliet, Y. Dor, J.-M. Herbert, D. Fukumura, K. Brusselmans, and M. Dewerchin Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis Nature 394 1998 485 490
8. B. Blouw, H. Song, T. Tihan, J. Bosze, N. Ferrara, and H.P. Gerber The hypoxic response of tumors is dependent on their microenvironment Cancer Cell 4 2003 133 146
9. F.A. Mack, W.K. Rathmell, A.M. Arsham, J. Gnarra, B. Keith, and M.C. Simon Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth Cancer Cell 3 2003 75 88
10. K.M. Comerford, T.J. Wallace, J. Karhausen, N.A. Louis, M.C. Montalto, and S.P. Colgan Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene Cancer Res 62 2002 3387 3394
11. D. Feldser, F. Agani, N.V. Iyer, B. Pak, G. Ferreira, and G.L. Semenza Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2 Cancer Res 59 1999 3915 3918
12. H. Nishi, T. Nakada, S. Kyo, M. Inoue, J.W. Shay, and K. Isaka Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT) Mol Cell Biol 24 2004 6076 6083
13. D.J. Ceradini, A.R. Kulkarni, M.J. Callaghan, O.M. Tepper, N. Bastidas, and M.E. Kleinman Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 Nat Med 10 2004 858 864
14. P. Staller, J. Sulitkova, J. Lisztwan, H. Moch, E.J. Oakeley, and W. Krek Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL Nature 425 2003 307 311
15. H.M. Sowter, P.J. Ratcliffe, P. Watson, A.H. Greenberg, and A.L. Harris HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors Cancer Res 61 2001 6669 6673
16. R.K. Bruick Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci USA 97 2000 9082 9087
17. M.P. Biju, A.K. Neumann, S.J. Bensinger, R.S. Johnson, L.A. Turka, and V.H. Haase Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes Mol Cell Biol 24 2004 9038 9047
18. E. Schipani, H.E. Ryan, S. Didrickson, T. Kobayashi, M. Knight, and R.S. Johnson Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival Genes Dev 15 2001 2865 2876
19. N. Goda, H.E. Ryan, B. Khadivi, W. McNulty, R.C. Rickert, and R.S. Johnson Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia Mol Cell Biol 23 2003 359 369
20. 2-regulated prolyl hydroxylation Science 292 2001 468 472
21. D. Lando, D.J. Peet, D.A. Whelan, J.J. Gorman, and M.L. Whitelaw Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch Science 295 2002 858 861 [reports]
22. 2 sensing Science 292 2001 464 468
23. T.N. Seagroves, D. Hadsell, J. McManaman, C. Palmer, D. Liao, and W. McNulty HIF1alpha is a critical regulator of secretory differentiation and activation, but not vascular expansion, in the mouse mammary gland Development 130 2003 1713 1724
24. T.N. Seagroves, H.E. Ryan, H. Lu, B.G. Wouters, M. Knapp, and P. Thibault Transcription factor HIF-1 is a necessary mediator of the Pasteur effect in mammalian cells Mol Cellular Biol 21 2001 3436 3444
25. T. Cramer, Y. Yamanishi, B.E. Clausen, I. Forster, R. Pawlinski, and N. Mackman HIF-1alpha is essential for myeloid cell-mediated inflammation Cell 112 2003 645 657
26. Wiesener MS, Jurgensen JS, Rosenberger C, Scholze C, Horstrup JH, Warnecke C et al., Widespread, hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J 2002:02-0445fje.
27. M. Scortegagna, M.A. Morris, Y. Oktay, M. Bennett, and J.A. Garcia The HIF family member EPAS1/HIF-2alpha is required for normal hematopoiesis in mice Blood 102 2003 1634 1640
28. M. Scortegagna, K. Ding, Y. Oktay, A. Gaur, F. Thurmond, and L.J. Yan Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice Nat Genet 35 2003 331 340
29. V. Compernolle, K. Brusselmans, T. Acker, P. Hoet, M. Tjwa, and H. Beck 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 8 2002 702 710
30. H. Tian, R.E. Hammer, A.M. Matsumoto, D.W. Russell, and S.L. McKnight The hypoxia responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development Genes Dev 12 1998 3320 3324
31. M. Morita, O. Ohneda, T. Yamashita, S. Takahashi, N. Suzuki, and O. Nakajima HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin EMBO J 22 2003 1134 1146
32. M.A. Maynard, H. Qi, J. Chung, E.H. Lee, Y. Kondo, and S. Hara Multiple splice variants of the human HIF-3alpha locus are targets of the VHL E3 ubiquitin ligase complex J Biol Chem 278 2003 11032 11040
33. Y. Makino, R. Cao, K. Svensson, G. Bertilsson, M. Asman, and H. Tanaka Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression [letters] Nature 414 2001 550 554
34. S.J. Mandriota, K.J. Turner, D.R. Davies, P.G. Murray, N.V. Morgan, and H.M. Sowter HIF activation identifies early lesions in VHL kidneys. Evidence for site-specific tumor suppressor function in the nephron Cancer Cell 1 2002 459 468
35. C.A. Thrash-Bingham, and K.D. Tartof aHIF: a natural antisense transcript overexpressed in human renal cancer and during hypoxia J Natl Cancer Inst 91 1999 143 151
36. S.L. Madden, E.A. Galella, D. Riley, A.H. Bertelsen, and G.A. Beaudry Induction of cell growth regulatory genes by p53 Cancer Res 56 1996 5384 5390
37. S.D. Wax, C.L. Rosenfield, and M.B. Taubman Identification of a novel growth factor-responsive gene in vascular smooth muscle cells J Biol Chem 269 1994 13041 13047
38. R.J. Appelhoff, Y.M. Tian, R.R. Raval, H. Turley, A.L. Harris, and C.W. Pugh Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor J Biol Chem 279 2004 38458 38465
39. E. Berra, E. Benizri, A. Ginouves, V. Volmat, D. Roux, and J. Pouyssegur HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia EMBO J 22 2003 4082 4090
40. A.C.R. Epstein, J.M. Gleadle, L.A. McNeill, K.S. Hewitson, J. O'Rourke, and D.R. Mole C. elegans EGL-9 and mammalian homologues define a family of dioxygenases that regulate HIF by prolyl hydroxylation Cell 107 2001 43 54
41. K. Nakayama, I.J. Frew, M. Hagensen, M. Skals, H. Habelhah, and A. Bhoumik Siah2 regulates stability of prolyl-hydroxylases, controls HIF1alpha abundance, and modulates physiological responses to hypoxia Cell 117 2004 941 952
42. D.A. Chan, P.D. Sutphin, N.C. Denko, and A.J. Giaccia Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1alpha J Biol Chem 277 2002 40112 40117
43. H.J. Knowles, R.R. Raval, A.L. Harris, and P.J. Ratcliffe Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells Cancer Res 63 2003 1764 1768
44. P.K. Majumder, P.G. Febbo, R. Bikoff, R. Berger, Q. Xue, and L.M. McMahon mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways Nat Med 10 2004 594 601
45. J. Brugarolas, K. Lei, R.L. Hurley, B.D. Manning, J.H. Reiling, and E. Hafen Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex Genes Dev 18 2004 2893 2904
46. J.H. Reiling, and E. Hafen The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila Genes Dev 18 2004 2879 2892
47. O. Iliopoulos, A. Kibel, S. Gray, and W.G. Kaelin Jr. Tumour supression by the human von Hippel-Lindau gene product Nat Med 1 1995 822 826
48. K. Kondo, W. Kim, M. Lechpammer, and W. Kaelin Inhibition of HIF2a is sufficient to suppress pVHL-defective tumor growth PLoS Biol 1 2003 439 444
49. T. Bishop, K.W. Lau, A.C. Epstein, S.K. Kim, M. Jiang, and D. O'Rourke Genetic analysis of pathways regulated by the von hippel-lindau tumor suppressor in Caenorhabditis elegans PLoS Biol 2 2004 e289
50. M. Ohh, R.L. Yauch, K.M. Lonergan, J.M. Whaley, A.O. Stemmer-Rachamimov, and D.N. Louis The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix Mol Cell 1 1998 959 968
51. N.H. Stickle, J. Chung, J.M. Klco, R.P. Hill, W.G. Kaelin Jr., and M. Ohh pVHL modification by NEDD8 is required for fibronectin matrix assembly and suppression of tumor development Mol Cell Biol 24 2004 3251 3261
52. M.A. Hoffman, M. Ohh, H. Yang, J.M. Klco, M. Ivan, and W.G.J. Kaelin von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF Hum Mol Genet 10 2001 1019 1027
53. S.C. Clifford, M.E. Cockman, A.C. Smallwood, D.R. Mole, E.R. Woodward, and P.H. Maxwell Contrasting effects on HIF-1a regulation by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease Hum Mol Genet 10 2001 1029 1038
54. V.H. Haase, J.N. Glickman, M. Socolovsky, and R. Jaenisch Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor Proc Natl Acad Sci USA 98 2001 1583 1588
55. E.C. Vaux, S.M. Wood, M.E. Cockman, L.G. Nicholls, K.M. Yeates, and C.W. Pugh Selection of mutant CHO cells with constitutive activation of the HIF system and inactivation of the von Hippel-Lindau tumor suppressor J Biol Chem 12 2001 12
56. Y. Cao, U. Karsten, H. Zerban, and P. Bannasch Expression of MUC1, Thomsen-Friedenreich-related antigens, and cytokeratin 19 in human renal cell carcinomas and tubular clear cell lesions Virchows Arch 436 2000 119 126
57. C. Rosenberger, S. Mandriota, J.S. Jurgensen, M.S. Wiesener, J.H. Horstrup, and U. Frei Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys J Am Soc Nephrol 13 2002 1721 1732
58. R.S. Yeung, G.H. Xiao, F. Jin, W.C. Lee, J.R. Testa, and A.G. Knudson Predisposition to renal carcinoma in the Eker rat is determined by germ-line mutation of the tuberous sclerosis 2 (TSC2) gene Proc Natl Acad Sci USA 91 1994 11413 11416
59. E.P. Henske The genetic basis of kidney cancer: why is tuberous sclerosis complex often overlooked? Curr Mol Med 4 2004 825 831
60. J.B. Brugarolas, F. Vazquez, A. Reddy, W.R. Sellers, and W.G. Kaelin Jr. TSC2 regulates VEGF through mTOR-dependent and -independent pathways Cancer Cell 4 2003 147 158
61. S. Vanharanta, M. Buchta, S.R. McWhinney, S.K. Virta, M. Peczkowska, and C.D. Morrison Early-onset renal cell carcinoma as a novel extraparaganglial component of SDHB-associated heritable paraganglioma Am J Hum Genet 74 2004 153 159
62. M.A. Selak, S.M. Armour, E.D. Mackenzie, H. Boulahbel, D.G. Watson, and K.D. Mansfield Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase Cancer Cell 7 2005 77 85
63. A. Unruh, A. Ressel, H.G. Mohamed, R.S. Johnson, R. Nadrowitz, and E. Richter The hypoxia-inducible factor-1 alpha is a negative factor for tumor therapy Oncogene 22 2003 3213 3220
64. A.L. Kung, S.D. Zabludoff, D.S. France, S.J. Freedman, E.A. Tanner, and A. Vieira Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway Cancer Cell 6 2004 33 43
65. N. Erez, M. Milyavsky, R. Eilam, I. Shats, N. Goldfinger, and V. Rotter Expression of prolyl-hydroxylase-1 (PHD1/EGLN2) suppresses hypoxia inducible factor-1alpha activation and inhibits tumor growth Cancer Res 63 2003 8777 8783
66. A. Rapisarda, B. Uranchimeg, D.A. Scudiero, M. Selby, E.A. Sausville, and R.H. Shoemaker Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway Cancer Res 62 2002 4316 4324