Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases

Biochemical and Biophysical Research Communications

Volumn 338, Issue 1, 2005, Pages 610-616

  Hirota, Kiichi ^a   Semenza, Gregg L ^b  

^a KYOTO UNIVERSITY HOSPITAL   (Japan)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dioxygenase; Hydroxylation; Hypoxia; Hypoxia inducible factor 1; Oxygen sensing; Transcriptional regulation

Indexed keywords

ASPARAGINYL HYDROXYLASE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; HYPOXIA INDUCIBLE FACTOR 1; N CARBOBENZYLOXYLEUCYLLEUCYLNORVALINAL; NITROPRUSSIDE SODIUM; OXYGEN; OXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG;

ENZYME ACTIVITY; ENZYME SPECIFICITY; HOMEOSTASIS; HUMAN; HYPOXIA; NONHUMAN; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; VON HIPPEL LINDAU DISEASE;

ANIMALS; ANOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MIXED FUNCTION OXYGENASES; PROCOLLAGEN-PROLINE DIOXYGENASE; SIGNAL TRANSDUCTION;

EID: 27544504817     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.193     Document Type: Review

References (66)

1. B.L. Taylor, and I.B. Zhulin PAS domains: internal sensors of oxygen, redox potential, and light Microbiol. Mol. Biol. Rev. 63 1999 479 506
2. R. Poyton Models for oxygen sensing in yeast: implications for oxygen-regulated gene expression in higher eucaryotes Respir. Physiol. 115 1999 119 133
3. M.A. Gilles-Gonzalez Oxygen signal transduction IUBMB Life 51 2001 165 173
4. K. Hirota Hypoxia-inducible factor 1, a master transcription factor of cellular hypoxic gene expression J. Anesth. 16 2002 150 159
5. G.L. Semenza, and G.L. Wang A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation Mol. Cell. Biol 12 1992 5447 5454
6. G.L. Wang, and G.L. Semenza Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia J. Biol. Chem. 268 1993 21513 21518
7. 2 homeostasis by hypoxia-inducible factor 1α Genes Dev. 12 1998 149 162
8. P. Carmeliet, Y. Dor, J.M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, P. Maxwell, C.J. Koch, P. Ratcliffe, L. Moons, R.K. Jain, D. Collen, and E. Keshet Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis Nature 394 1998 485 490
9. H. Reyes, S. Reisz-Porszasz, and O. Hankinson Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor Science 256 1992 1193 1195
10. B.H. Jiang, E. Rue, G.L. Wang, R. Roe, and G.L. Semenza Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1 J. Biol. Chem. 271 1996 17771 17778
11. H. Tian, S.L. McKnight, and D.W. Russel Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells Genes Dev. 11 1997 72 82
12. Y.Z. Gu, S.M. Moran, J.B. Hogenesch, L. Wartman, and C.A. Bradfield Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3α Gene Expr. 7 1998 205 213
13. G.L. Wang, and G.L. Semenza Purification and characterization of hypoxia-inducible factor 1 J. Biol. Chem. 270 1995 1230 1237
14. 2 tension Proc. Natl. Acad. Sci. USA 92 1995 5510 5514
15. 2-dependent degradation domain via the ubiquitin-proteasome pathway Proc. Natl. Acad. Sci. USA 95 1998 7987 7992
16. P.J. Kallio, W.J. Wilson, S. O'Brien, Y. Makino, and L. Poellinger Regulation of the hypoxia-inducible transcription factor 1α by the ubiquitin-proteasome pathway J. Biol. Chem. 274 1999 6519 6525
17. S. Salceda, and J. Caro 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. 272 1997 22642 22647
18. C.H. Sutter, E. Laughner, and G.L. Semenza Hypoxia-inducible factor 1 protein expression is controlled by oxygen-regulated ubiquitination that is disrupted by deletions and missense mutations Proc. Natl. Acad. Sci. USA 97 2000 4748 4753
19. P.H. Maxwell, M.S. Wiesener, G.W. Chang, S.C. Clifford, E.C. Vaux, M.E. Cockman, C.C. Wykoff, C.W. Pugh, E.R. Maher, and P.J. Ratcliffe The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 1999 271 275
20. M. Ohh, C.W. Park, M. Ivan, M.A. Hoffman, T.Y. Kim, L.E. Huang, N. Pavletich, V. Chau, and W.G. Kaelin Ubiquitination of hypoxia-inducible factor requires direct binding to the β-domain of the von Hippel-Lindau protein Nat. Cell Biol. 2 2000 423 427
21. T. Kamura, S. Sato, K. Iwai, M. Czyzyk-Krzeska, R.C. Conaway, and J.W. Conaway Activation of HIF-1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex Proc. Natl. Acad. Sci. USA 97 2000 10430 10435
22. 2-regulated prolyl hydroxylation Science 292 2001 468 472
23. 2 sensing Science 292 2001 464 468
24. F. Yu, S.B. White, Q. Zhao, and F.S. Lee HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation Proc. Natl. Acad. Sci. USA 98 2001 9630 9635
25. A.C. Epstein, J.M. Gleadle, L.A. McNeill, K.S. Hewitson, J. O'Rourke, D.R. Mole, M. Mukherji, E. Metzen, M.I. Wilson, A. Dhanda, Y.M. Tian, N. Masson, D.L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P.H. Maxwell, C.W. Pugh, C.J. Schofield, and P.J. Ratcliffe C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation Cell 107 2001 43 54
26. R.K. Bruick, and S.L. McKnight A conserved family of prolyl-4- hydroxylases that modify HIF Science 294 2001 1337 1340
27. 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
28. B.H. Jiang, J.Z. Zheng, S.W. Leung, R. Roe, and G.L. Semenza Transactivation and inhibitory domains of hypoxia-inducible factor 1α: modulation of transcriptional activity by oxygen tension J. Biol. Chem. 272 1997 19253 19260
29. C.W. Pugh, J.F. O'Rourke, M. Nagao, J.M. Gleadle, and P.J. Ratcliffe Activation of hypoxia-inducible factor-1; definition of regulatory domains within the α-subunit J. Biol. Chem. 272 1997 11205 11214
30. P.J. Kallio, K. Okamoto, S. O'Brien, P. Carrero, Y. Makino, H. Tanaka, and L. Poellinger Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1α EMBO J. 17 1998 6573 6586
31. P.C. Mahon, K. Hirota, and G.L. Semenza FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity Genes Dev. 15 2001 2675 2685
32. 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
33. D. Lando, D.J. Peet, J.J. Gorman, D.A. Whelan, M.L. Whitelaw, and R.K. Bruick FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor Genes Dev. 16 2002 1466 1471
34. K.S. Hewitson, L.A. McNeill, M.V. Riordan, Y.M. Tian, A.N. Bullock, R.W. Welford, J.M. Elkins, N.J. Oldham, S. Bhattacharya, J.M. Gleadle, P.J. Ratcliffe, C.W. Pugh, and C.J. Schofield Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family J. Biol. Chem. 277 2002 26351 26355
35. N. Sang, J. Fang, V. Srinivas, I. Leshchinsky, and J. Caro Carboxyl-terminal transactivation activity of hypoxia-inducible factor 1α is governed by a von Hippel-Lindau protein-independent, hydroxylation-regulated association with p300/CBP Mol. Cell. Biol. 22 2002 2984 2992
36. C.J. Schofield, and Z. Zhang Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes Curr. Opin. Struct. Biol. 9 1999 722 731
37. L.A. McNeill, K.S. Hewitson, J.M. Gleadle, L.E. Horsfall, N.J. Oldham, P.H. Maxwell, C.W. Pugh, P.J. Ratcliffe, and C.J. Schofield The use of dioxygen by HIF prolyl hydroxylase (PHD1) Bioorg. Med. Chem. Lett. 12 2002 1547 1550
38. J. Myllyharju, and K.I. Kivirikko Characterization of the iron- and 2-oxoglutarate-binding sites of human prolyl 4-hydroxylase EMBO J. 16 1997 1173 1180
39. M. Hirsilä, P. Koivunen, V. Gunzler, K.I. Kivirikko, and J. Myllyharju Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor J. Biol. Chem. 278 2003 30772 30780
40. P. Koivunen, M. Hirsilä, V. Gunzler, K.I. Kivirikko, and J. Myllyharju Catalytic properties of the asparaginyl hydroxylase (FIH) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases J. Biol. Chem. 279 2004 9899 9904
41. C.E. Dann III, R.K. Bruick, and J. Deisenhofer Structure of factor inhibiting hypoxia-inducible factor 1: an asparaginyl hydroxylase involved in the hypoxic response Proc. Natl. Acad. Sci. USA. 99 2002 15351 15356
42. N. Masson, C. Willam, P.H. Maxwell, C.W. Pugh, and P.J. Ratcliffe Independent function of two destruction domain in hypoxia-inducible factor-α chains activated by prolyl hydroxylation EMBO J. 20 2001 5197 5206
43. M. Hirsila, P. Koivunen, L. Xu, T. Seeley, K.I. Kivirikko, and J. Myllyharju Effect of desferrioxamine and metals on the hydroxylases in the oxygen sensing pathway FASEB J. 2005
44. J.M. Elkins, K.S. Hewitson, L.A. McNeill, J.F. Seibel, I. Schlemminger, C.W. Pugh, P.J. Ratcliffe, and C.J. Schofield Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1α J. Biol. Chem. 278 2003 1802 1806
45. C. Lee, S.J. Kim, D.G. Jeong, S.M. Lee, and S.E. Ryu Structure of human FIH-1 reveals a unique active site pocket and interaction sites for HIF-1 and von Hippel-Lindau J. Biol. Chem. 278 2003 7558 7563
46. J. Huang, Q. Zhao, S.M. Mooney, and F.S. Lee Sequence determinants in hypoxia-inducible factor-1α for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3 J. Biol. Chem. 277 2002 39792 39800
47. E. Metzen, U. Berchner-Pfannschmidt, P. Stengel, J.H. Marxsen, I. Stolze, M. Klinger, W.Q. Huang, C. Wotzlaw, T. Hellwig-Burgel, W. Jelkmann, H. Acker, and J. Fandrey Intracellular localisation of human HIF-1α hydroxylases: implications for oxygen sensing J. Cell Sci. 116 2003 1319 1326
48. K. Kasuno, S. Takabuchi, K. Fukuda, S. Kizaka-Kondoh, J. Yodoi, T. Adachi, G.L. Semenza, and K. Hirota Nitric oxide induces hypoxia-inducible factor 1 activation that is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling J. Biol. Chem. 279 2004 2550 2558
49. L.A. Palmer, B. Gaston, and R.A. Johns Normoxic stabilization of hypoxia-inducible factor 1 expression and activity: redox-dependent effect of nitrogen oxides Mol. Pharmacol. 58 2000 1197 1203
50. S. Takabuchi, K. Hirota, K. Nishi, S. Oda, T. Oda, T. Shingu, A. Takabayashi, T. Adachi, G.L. Semenza, and K. Fukuda The inhibitory effect of sodium nitroprusside on HIF-1 activation is not dependent on nitric oxide- soluble guanylyl cyclase pathway Biochem. Biophys. Res. Commun. 324 2004 417 423
51. M. Callapina, J. Zhou, S. Schnitzer, E. Metzen, C. Lohr, J.W. Deitmer, and B. Brune Nitric oxide reverses desferrioxamine- and hypoxia-induced HIF-1α accumulation: implications for prolyl hydroxylase activity and iron Exp. Cell Res. 306 2005 274 284
52. T. Hagen, C.T. Taylor, F. Lam, and S. Moncada Redistribution of intracellular oxygen in hypoxia by nitric oxide effect on HIF-1α Science 302 2003 1975 1978
53. F.H. Agani, M. Puchowicz, J.C. Chavez, P. Pichiule, and J. LaManna Role of nitric oxide in the regulation of HIF-1α expression during hypoxia Am. J. Physiol. 283 2002 C178 C186
54. K. Sogawa, K. Numayama-Tsuruta, M. Ema, M. Abe, and Y. Fujii-Kuriyama Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia Proc. Natl. Acad. Sci. USA 95 1998 7368 7373
55. G.L. Semenza HIF-1 and tumor progression: pathophysiology and therapeutics Trends Mol. Med. 8 2002 1983 1991
56. E. Laughner, P. Taghavi, K. Chiles, P.C. Mahon, and G.L. Semenza HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression Mol. Cell. Biol. 21 2001 3995 4004
57. R. Fukuda, K. Hirota, F. Fan, Y.D. Jung, L.M. Ellis, and G.L. Semenza Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells J. Biol. Chem. 277 2002 38205 38211
58. D.A. Chan, P.D. Sutphin, N.C. Denko, and A.J. Giaccia Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1α J. Biol. Chem. 277 2002 40112 40117
59. R. Karni, Y. Dor, E. Keshet, O. Meyuhas, and A. Levitzki Activated pp60c-Src leads to elevated hypoxia-inducible factor (HIF)-1α expression under normoxia J. Biol. Chem. 277 2002 42919 42925
60. K. Nakayama, I. Frew, M. Hagensen, M. Skals, H. Habelhah, A. Bhoumik, T. Kadoya, H. Erdjument-Bromage, P. Tempst, P. Frappell, D. Bowtell, and Z. Ronai Siah2 regulates stability of prolyl-hydroxylases, controls HIF-1α abundance, and modulates physiological responses to hypoxia Cell 117 2004 941 952
61. K. Nakayama, and Z. Ronai Siah: new players in the cellular response to hypoxia Cell Cycle 3 2004 1345 1347
62. A. Ozer, L.C. Wu, and R.K. Bruick The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF) Proc. Natl. Acad. Sci. USA 102 2005 7481 7486
63. N.S. Chandel, E. Maltepe, E. Goldwasser, C.E. Mathieu, M.C. Simon, and P.T. Schumacker Mitochondrial reactive oxygen species trigger hypoxia-induced transcription Proc. Natl. Acad. Sci. USA 95 1998 11715 11720
64. R.D. Guzy, B. Hoyos, E. Robin, H. Chen, L. Liu, K.D. Mansfield, M.C. Simon, U. Hammerling, and P.T. Schumacker Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing Cell Metab. 1 2005 401 408
65. J.K. Brunelle, E.L. Bell, N.M. Quesada, K. Vercauteren, V. Tiranti, M. Zeviani, R.C. Scarpulla, and N.S. Chandel Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation Cell Metab. 1 2005 409 414
66. K.D. Mansfield, R.D. Guzy, Y. Pan, R.M. Young, T.P. Cash, P.T. Schumacker, and M.C. Simon Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-α activation Cell Metab. 1 2005 393 399