Genetic evidence for a tumor suppressor role of HIF-2α

Cancer Cell

Volumn 8, Issue 2, 2005, Pages 131-141

  Acker, Till ^a   Diez Juan, Antonio ^b   Aragones, Julian ^b   Tjwa, Marc ^b   Brusselmans, Koen ^b   Moons, Lieve ^b   Fukumura, Dai ^c   Moreno Murciano, Maria Paz ^b   Herbert, Jean Marc ^d   Burger, Angelika ^e,h   Riedel, Johanna ^a   Elvert, Gerd ^f,i   Flamme, Ingo ^f,i   Maxwell, Patrick H ^g   Collen, Désiré ^b   Dewerchin, Mieke ^b   Jain, Rakesh K ^c   Plate, Karl H ^a   Carmeliet, Peter ^b  

^a GOETHE UNIVERSITY   (Germany)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SANOFI   (France)

^e TUMOR BIOLOGY CENTER   (Germany)

^f UNIVERSITY OF COLOGNE   (Germany)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

ⁱ BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; LENTIVIRUS VECTOR; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GENETICS; CANCER INHIBITION; CONTROLLED STUDY; GLIOBLASTOMA; GLIOMA; KNOCKOUT GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TERATOMA; TRANSGENE; TUMOR CELL; TUMOR GROWTH; TUMOR VASCULARIZATION;

EID: 23644435597     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2005.07.003     Document Type: Article

References (72)

1. T. Acker, and H. Acker Cellular oxygen sensing need in CNS function: physiological and pathological implications J. Exp. Biol. 207 2004 3171 3188
2. O. Amellem, and E.O. Pettersen Cell inactivation and cell cycle inhibition as induced by extreme hypoxia: the possible role of cell cycle arrest as a protection against hypoxia-induced lethal damage Cell Prolif. 24 1991 127 141
3. B. Bachtiary, M. Schindl, R. Potter, B. Dreier, T.H. Knocke, J.A. Hainfellner, R. Horvat, and P. Birner Overexpression of hypoxia-inducible factor 1α indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer Clin. Cancer Res. 9 2003 2234 2240
4. N.J. Beasley, R. Leek, M. Alam, H. Turley, G.J. Cox, K. Gatter, P. Millard, S. Fuggle, and A.L. Harris Hypoxia-inducible factors HIF-1α and HIF-2α in head and neck cancer: relationship to tumor biology and treatment outcome in surgically resected patients Cancer Res. 62 2002 2493 2497
5. 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-1α in normoxia EMBO J. 22 2003 4082 4090
6. 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
7. C. Blancher, J.W. Moore, K.L. Talks, S. Houlbrook, and A.L. Harris Relationship of hypoxia-inducible factor (HIF)-1α and HIF-2α expression to vascular endothelial growth factor induction and hypoxia survival in human breast cancer cell lines Cancer Res. 60 2000 7106 7113
8. B. Blouw, H. Song, T. Tihan, J. Bosze, N. Ferrara, H.P. Gerber, R.S. Johnson, and G. Bergers The hypoxic response of tumors is dependent on their microenvironment Cancer Cell 4 2003 133 146
9. E.B. Brown, R.B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R.K. Jain In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy Nat. Med. 7 2001 864 868
10. K. Brusselmans, F. Bono, P. Maxwell, Y. Dor, M. Dewerchin, D. Collen, J.M. Herbert, and P. Carmeliet Hypoxia-inducible factor-2α (HIF-2α) is involved in the apoptotic response to hypoglycemia but not to hypoxia J. Biol. Chem. 276 2001 39192 39196
11. P. Carmeliet, V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, and C. Eberhardt Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele Nature 380 1996 435 439
12. P. Carmeliet, Y. Dor, J.M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, and P. Maxwell Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis Nature 394 1998 485 490
13. C. Chen, N. Pore, A. Behrooz, F. Ismail-Beigi, and A. Maity Regulation of glut1 mRNA by HIF-1: Interaction between H-ras and hypoxia J. Biol. Chem. 276 2000 9519 9525
14. J. Chen, S. Zhao, K. Nakada, Y. Kuge, N. Tamaki, F. Okada, J. Wang, M. Shindo, F. Higashino, and K. Takeda Dominant-negative hypoxia-inducible factor-1α reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism Am. J. Pathol. 162 2003 1283 1291
15. G.G. Chen, F.L. Sin, B.C. Leung, H.K. Ng, and W.S. Poon Glioblastoma cells deficient in DNA-dependent protein kinase are resistant to cell death J. Cell. Physiol. 203 2005 127 132
16. V. Compernolle, K. Brusselmans, T. Acker, P. Hoet, M. Tjwa, H. Beck, S. Plaisance, Y. Dor, E. Keshet, and F. Lupu Loss of HIF-2α 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
17. V. Compernolle, K. Brusselmans, D. Franco, A. Moorman, M. Dewerchin, D. Collen, and P. Carmeliet Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1α Cardiovasc. Res. 60 2003 569 579
18. K.L. Covello, M.C. Simon, and B. Keith Targeted replacement of hypoxia-inducible factor-1α by a hypoxia-inducible factor-2α knock-in allele promotes tumor growth Cancer Res. 65 2005 2277 2286
19. J.P. Dales, S. Garcia, S. Meunier-Carpentier, L. Andrac-Meyer, O. Haddad, M.N. Lavaut, C. Allasia, P. Bonnier, and C. Charpin Overexpression of hypoxia-inducible factor HIF-1α predicts early relapse in breast cancer: Retrospective study in a series of 745 patients Int. J. Cancer 116 2005 734 739
20. A. Damert, E. Ikeda, and W. Risau Activator-protein-1 binding potentiates the hypoxia-inducible factor-1-mediated hypoxia-induced transcriptional activation of vascular-endothelial growth factor expression in C6 glioma cells Biochem. J. 327 1997 419 423
21. G. Elvert, A. Kappel, R. Heidenreich, U. Englmeier, S. Lanz, T. Acker, M. Rauter, K. Plate, M. Sieweke, G. Breier, and I. Flamme Cooperative interaction of hypoxia-inducible factor-2α (HIF-2α) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1) J. Biol. Chem. 278 2003 7520 7530
22. I. Flamme, M. Krieg, and K.H. Plate Up-regulation of vascular endothelial growth factor in stromal cells of hemangioblastomas is correlated with up-regulation of the transcription factor HRF/HIF-2α Am. J. Pathol. 153 1998 25 29
23. A. Giaccia, B.G. Siim, and R.S. Johnson HIF-1 as a target for drug development Nat. Rev. Drug Discov. 2 2003 803 811
24. A. Giatromanolaki, M.I. Koukourakis, E. Sivridis, H. Turley, K. Talks, F. Pezzella, K.C. Gatter, and A.L. Harris Relation of hypoxia inducible factor 1α and 2α in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival Br. J. Cancer 85 2001 881 890
25. T.G. Graeber, C. Osmanian, T. Jacks, D.E. Housman, C.J. Koch, S.W. Lowe, and A.J. Giaccia Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours Nature 379 1996 88 91
26. A.E. Greijer, and E. van der Wall The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis J. Clin. Pathol. 57 2004 1009 1014
27. N.V. Iyer, L.E. Kotch, F. Agani, S.W. Leung, E. Laughner, R.H. Wenger, M. Gassmann, J.D. Gearhart, A.M. Lawler, A.Y. Yu, and G.L. Semenza Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α Genes Dev. 12 1998 149 162
28. A. Jones, C. Fujiyama, C. Blanche, J.W. Moore, S. Fuggle, D. Cranston, R. Bicknell, and A.L. Harris Relation of vascular endothelial growth factor production to expression and regulation of hypoxia-inducible factor-1α and hypoxia-inducible factor-2α in human bladder tumors and cell lines Clin. Cancer Res. 7 2001 1263 1272
29. W.G. Kaelin Jr. Proline hydroxylation and gene expression Annu. Rev. Biochem. Annu. Rev. Biochem. 74 2004 115 128
30. K. Kondo, J. Klco, E. Nakamura, M. Lechpammer, and W.G. Kaelin Jr. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein Cancer Cell 1 2002 237 246
31. K. Kondo, W.Y. Kim, M. Lechpammer, and W.G. Kaelin Jr. Inhibition of HIF2α is sufficient to suppress pVHL-defective tumor growth PLoS Biol. 1 2003 e83 10.1371/journal.pbio.0000083
32. M. Koshiji, and L.E. Huang Dynamic balancing of the dual nature of HIF-1α for cell survival Cell Cycle 3 2004 853 854
33. M. Koshiji, Y. Kageyama, E.A. Pete, I. Horikawa, J.C. Barrett, and L.E. Huang HIF-1α induces cell cycle arrest by functionally counteracting Myc EMBO J. 23 2004 1949 1956
34. M. Koshiji, K.K. To, S. Hammer, K. Kumamoto, A.L. Harris, P. Modrich, and L.E. Huang HIF-1α induces genetic instability by transcriptionally downregulating MutSα expression Mol. Cell 17 2005 793 803
35. M. Krieg, R. Haas, H. Brauch, T. Acker, I. Flamme, and K.H. Plate Up-regulation of hypoxia-inducible factors HIF-1α and HIF-2α under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function Oncogene 19 2000 5435 5443
36. A.L. Kung, S. Wang, J.M. Klco, W.G. Kaelin, and D.M. Livingston Suppression of tumor growth through disruption of hypoxia-inducible transcription Nat. Med. 6 2000 1335 1340
37. A.L. Kung, S.D. Zabludoff, D.S. France, S.J. Freedman, E.A. Tanner, A. Vieira, S. Cornell-Kennon, J. Lee, B. Wang, and J. Wang Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway Cancer Cell 6 2004 33 43
38. R.D. Leek, I. Stratford, and A.L. Harris The role of hypoxia-inducible factor-1 in three-dimensional tumor growth, apoptosis, and regulation by the insulin-signaling pathway Cancer Res. 65 2005 4147 4152
39. L. Liu, and M.C. Simon Regulation of transcription and translation by hypoxia Cancer Biol. Ther. 3 2004 492 497
40. N.J. Mabjeesh, D. Escuin, T.M. LaVallee, V.S. Pribluda, G.M. Swartz, M.S. Johnson, M.T. Willard, H. Zhong, J.W. Simons, and P. Giannakakou 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF Cancer Cell 3 2003 363 375
41. 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
42. F.A. Mack, J.H. Patel, M.P. Biju, V.H. Haase, and M.C. Simon Decreased growth of Vhl-/- fibrosarcomas is associated with elevated levels of cyclin kinase inhibitors p21 and p27 Mol. Cell. Biol. 25 2005 4565 4578
43. E. Maltepe, J.V. Schmidt, D. Baunoch, C.A. Bradfield, and M.C. Simon Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT Nature 386 1997 403 407
44. J.K. Maranchie, J.R. Vasselli, J. Riss, J.S. Bonifacino, W.M. Linehan, and R.D. Klausner The contribution of VHL substrate binding and HIF1-α to the phenotype of VHL loss in renal cell carcinoma Cancer Cell 1 2002 247 255
45. P. Maxwell, and K. Salnikow HIF-1: An oxygen and metal responsive transcription factor Cancer Biol. Ther. 3 2004 29 35
46. K. Mekhail, L. Gunaratnam, M.E. Bonicalzi, and S. Lee HIF activation by pH-dependent nucleolar sequestration of VHL Nat. Cell Biol. 6 2004 642 647
47. Y. Pan, P.R. Oprysko, A.M. Asham, C.J. Koch, and M.C. Simon p53 cannot be induced by hypoxia alone but responds to the hypoxic microenvironment Oncogene 23 2004 4975 4983
48. J. Peng, L. Zhang, L. Drysdale, and G.H. Fong The transcription factor EPAS-1/hypoxia-inducible factor 2α plays an important role in vascular remodeling Proc. Natl. Acad. Sci. USA 97 2000 8386 8391
49. L. Poellinger, and R.S. Johnson HIF-1 and hypoxic response: the plot thickens Curr. Opin. Genet. Dev. 14 2004 81 85
50. A. Rapisarda, J. Zalek, M. Hollingshead, T. Braunschweig, B. Uranchimeg, C.A. Bonomi, S.D. Borgel, J.P. Carter, S.M. Hewitt, R.H. Shoemaker, and G. Melillo Schedule-dependent inhibition of hypoxia-inducible factor-1α protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts Cancer Res. 64 2004 6845 6848
51. P.J. Ratcliffe, C.W. Pugh, and P.H. Maxwell Targeting tumors through the HIF system Nat. Med. 6 2000 1315 1316
52. R.R. Raval, K.W. Lau, M.G. Tran, H.M. Sowter, S.J. Mandriota, J.L. Li, C.W. Pugh, P.H. Maxwell, A.L. Harris, and P.J. Ratcliffe Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma Mol. Cell. Biol. 25 2005 5675 5686
53. H.E. Ryan, J. Lo, and R.S. Johnson HIF-1α is required for solid tumor formation and embryonic vascularization EMBO J. 17 1998 3005 3015
54. H.E. Ryan, M. Poloni, W. McNulty, D. Elson, M. Gassmann, J.M. Arbeit, and R.S. Johnson Hypoxia-inducible factor-1α is a positive factor in solid tumor growth Cancer Res. 60 2000 4010 4015
55. E. Schipani, H.E. Ryan, S. Didrickson, T. Kobayashi, M. Knight, and R.S. Johnson Hypoxia in cartilage: HIF-1α is essential for chondrocyte growth arrest and survival Genes Dev. 15 2001 2865 2876
56. C. Schmaltz, P.H. Hardenbergh, A. Wells, and D.E. Fisher Regulation of proliferation-survival decisions during tumor cell hypoxia Mol. Cell. Biol. 18 1998 2845 2854
57. C.J. Schofield, and P.J. Ratcliffe Oxygen sensing by HIF hydroxylases Nat. Rev. Mol. Cell Biol. 5 2004 343 354
58. M. Scortegagna, K. Ding, Y. Oktay, A. Gaur, F. Thurmond, L.J. Yan, B.T. Marck, A.M. Matsumoto, J.M. Shelton, and J.A. Richardson Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice Nat. Genet. 35 2003 331 340
59. G.L. Semenza HIF-1 and tumor progression: pathophysiology and therapeutics Trends Mol. Med. 8 2002 S62 S67
60. G.L. Semenza Targeting HIF-1 for cancer therapy Nat. Rev. Cancer 3 2003 721 732
61. H.M. Sowter, R.R. Raval, J.W. Moore, P.J. Ratcliffe, and A.L. Harris Predominant role of hypoxia-inducible transcription factor (Hif)-1α versus Hif-2α in regulation of the transcriptional response to hypoxia Cancer Res. 63 2003 6130 6134
62. O. Stoeltzing, M.F. McCarty, J.S. Wey, F. Fan, W. Liu, A. Belcheva, C.D. Bucana, G.L. Semenza, and L.M. Ellis Role of hypoxia-inducible factor 1α in gastric cancer cell growth, angiogenesis, and vessel maturation J. Natl. Cancer Inst. 96 2004 946 956
63. K.L. Talks, H. Turley, K.C. Gatter, P.H. Maxwell, C.W. Pugh, P.J. Ratcliffe, and A.L. Harris The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers, and tumor-associated macrophages Am. J. Pathol. 157 2000 411 421
64. 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
65. Y. Tsuzuki, D. Fukumura, B. Oosthuyse, C. Koike, P. Carmeliet, and R.K. Jain Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1α→ hypoxia response element→ VEGF cascade differentially regulates vascular response and growth rate in tumors Cancer Res. 60 2000 6248 6252
66. M. Volm, and R. Koomagi Hypoxia-inducible factor (HIF-1) and its relationship to apoptosis and proliferation in lung cancer Anticancer Res. 20 2000 1527 1533
67. M.S. Wiesener, H. Turley, W.E. Allen, C. Willam, K.U. Eckardt, K.L. Talks, S.M. Wood, K.C. Gatter, A.L. Harris, and C.W. Pugh Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1α Blood 92 1998 2260 2268
68. G. Xia, Y. Kageyama, T. Hayashi, S. Kawakami, M. Yoshida, and K. Kihara Regulation of vascular endothelial growth factor transcription by endothelial PAS domain protein 1 (EPAS1) and possible involvement of EPAS1 in the angiogenesis of renal cell carcinoma Cancer 91 2001 1429 1436
69. H. Yoshimura, D.K. Dhar, H. Kohno, H. Kubota, T. Fujii, S. Ueda, S. Kinugasa, M. Tachibana, and N. Nagasue Prognostic impact of hypoxia-inducible factors 1α and 2α in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression Clin. Cancer Res. 10 2004 8554 8560
70. J.L. Yu, J.W. Rak, P. Carmeliet, A. Nagy, R.S. Kerbel, and B.L. Coomber Heterogeneous vascular dependence of tumor cell populations Am. J. Pathol. 158 2001 1325 1334
71. H. Zhong, K. Chiles, D. Feldser, E. Laughner, C. Hanrahan, M.M. Georgescu, J.W. Simons, and G.L. Semenza Modulation of hypoxia-inducible factor 1α expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics Cancer Res. 60 2000 1541 1545
72. M. Zimmer, D. Doucette, N. Siddiqui, and O. Iliopoulos Inhibition of hypoxia-inducible factor is sufficient for growth suppression of VHL-/- tumors Mol. Cancer Res. 2 2004 89 95