IOP1, a novel hydrogenase-like protein that modulates hypoxia-inducible factor-1α activity

Biochemical Journal

Volumn 401, Issue 1, 2007, Pages 341-352

  Huang, Jianhe ^a   Song, Daisheng ^a   Flores, Adrian ^a   Zhao, Quan ^a   Mooney, Sharon M ^a   Shaw, Leslie M ^a   Lee, Frank S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Hypoxia inducible factor (HIF); Iron only hydrogenase like protein 1 (IOP1); Nuclear prelamin A recognition factor (Narf); Proline hydroxylase domain containing protein (PHD); Yeast

Indexed keywords

HYPOXIA-INDUCIBLE FACTOR (HIF); IRON-ONLY HYDROGENASE-LIKE PROTEIN 1 (IOP1); NUCLEAR PRELAMIN A RECOGNITION FACTOR (NARF); PROLINE HYDROXYLASE DOMAIN-CONTAINING PROTEIN (PHD);

ACTIVATION ANALYSIS; ANIMAL CELL CULTURE; BIOCHEMISTRY; CELLS; YEAST;

PROTEINS;

HYPOXIA INDUCIBLE FACTOR 1ALPHA; IRON ONLY HYDROGENASE LIKE PROTEIN 1; PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; UPREGULATION;

AMINO ACID SEQUENCE; BLOTTING, NORTHERN; CONSERVED SEQUENCE; HUMANS; HYDROGENASE; KIDNEY; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

MAMMALIA;

EID: 33846298869     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060635     Document Type: Article

References (79)

1. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15, 551-578
2. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
3. 2 tension. Proc. Natl. Acad. Sci. U.S.A. 92, 5510-5514
4. Ema, M., Taya, S., Yokotani, N., Sogawa, K., Matsuda, Y. and Fujii-Kuriyama, Y. (1997) A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. U.S.A. 94, 4273-4278
5. Hogenesch, J. B., Chan, W. K., Jackiw, V. H., Brown, R. C., Gu, Y. Z., Pray-Grant, M., Perdew, G. H. and Bradfield, C. A. (1997) Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272, 8581-8593
6. Gu, Y. Z., Moran, S. M., Hogenesch, J. B., Wartman, L. and Bradfield, C. A. (1998) Molecular characterization and chromosomal localization of a third α-class hypoxia inducible factor subunit, HIF3α. Gene Expr. 7, 205-213
7. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 7987-7992
8. Maynard, M. A., Qi, H., Chung, J., Lee, E. H., Kondo, Y., Hara, S., Conaway, R. C., Conaway, J. W. and Ohh, M. (2003) Multiple splice variants of the human HIF-3 α locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J. Biol. Chem. 278, 11032-11040
9. 2 sensing. Science 292, 464-468
10. 2-regulated prolyl hydroxylation. Science 292, 468-472
11. Yu, F., White, S. B., Zhao, Q. and Lee, F. S. (2001) HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. U.S.A. 98, 9630-9635
12. Masson, N., Willam, C., Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J. (2001) Independent function of two destruction domains in hypoxia-inducible factor-α chains activated by prolyl hydroxylation. EMBO J. 20, 5197-5206
13. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A. et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54
14. Bruick, R. K. and McKnight, S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340
15. Ivan, M., Haberberger, T., Gervasi, D. C., Michelson, K. S., Gunzler, V., Kondo, K., Yang, H., Sorokina, I., Conaway, R. C., Conaway, J. W. et al. (2002) Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc. Natl. Acad. Sci. U.S.A. 99, 13459-13464
16. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R. and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275
17. Salceda, S. and Caro, J. (1997) Hypoxia-inducible factor 1alpha (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, 22642-22647
18. Schofield, C. J. and Ratcliffe, P. J. (2005) Signalling hypoxia by HIF hydroxylases. Biochem. Biophys. Res. Commun. 338, 617-626
19. Kaelin, W. G. (2005) Proline hydroxylation and gene expression. Annu. Rev. Biochem. 74, 115-128
20. Hirota, K. and Semenza, G. L. (2005) Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases. Biochem. Biophys. Res. Commun. 338, 610-616
21. 2-dependent regulators of the hypoxic response pathway. Biochem. Biophys. Res. Commun. 338, 639-647
22. Hu, C. J., Wang, L. Y., Chodosh, L. A., Keith, B. and Simon, M. C. (2003) Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF-2α in hypoxic gene regulation. Mol. Cell. Biol. 23, 9361-9374
23. Vengellur, A., Woods, B. G., Ryan, H. E., Johnson, R. S. and LaPres, J. J. (2003) Gene expression profiling of the hypoxia signaling pathway in hypoxia-inducible factor 1α null mouse embryonic fibroblasts. Gene Expr. 11, 181-197
24. Warnecke, C., Zaborowska, Z., Kurreck, J., Erdmann, V. A., Frei, U., Wiesener, M. and Eckardt, K. U. (2004) Differentiating the functional role of hypoxia-inducible factor (HIF)-1α and HIF-2α (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2α target gene in Hep3B and Kelly cells. FASEB J. 18, 1462-1464
25. Makino, Y., Cao, R., Svensson, K., Bertilsson, G., Asman, M., Tanaka, H., Cao, Y., Berkenstam, A. and Poellinger, L. (2001) Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 414, 550-554
26. Makino, Y., Kanopka, A., Wilson, W. J., Tanaka, H. and Poellinger, L. (2002) Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3α locus. J. Biol. Chem. 277, 32405-32408
27. Mahon, P. C., Hirota, K. and Semenza, G. L. (2001) FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15, 2675-2686
28. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J. and Whitelaw, M. L. (2002) Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295, 858-861
29. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L. and Bruick, R. K. (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471
30. Hewitson, K. S., McNeill, L A., Riordan, M. V., Tian, Y. M., Bullock, A. N., Welford, R. W., Elkins, J. M., Oldham, N.J., Bhattacharya, S., Gleadle, J. M. et al. (2002) 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, 26351-26355
31. Lancaster, D. E., McNeill, L. A., McDonough, M. A., Aplin, R. T., Hewitson, K. S., Pugh, C. W., Ratcliffe, P. J. and Schofield, C. J. (2004) Disruption of dimerization and substrate phospnorylation inhibit factor inhibiting hypoxia-inducible factor (FIH) activity. Biochem. J. 383, 429-437
32. Gradin, K., Takasaki, C., Fujii-Kuriyama, Y. and Sogawa, K. (2002) The transcriptional activation function of the HIF-like factor requires phosphorylation at a conserved threonine. J. Biol. Chem. 277, 23508-23514
33. Laughner, E., Taghavi, P., Chiles, K., Mahon, P. C. and Semenza, G. L. (2001) 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, 3995-4004
34. Baek, J. H., Mahon, P. C., Oh, J., Kelly, B., Krishnamachary, B., Pearson, M., Chan, D. A., Giaccia, A. J. and Semenza, G. L. (2005) OS-9 interacts with hypoxia-inducible factor 1α and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α. Mol. Cell 17, 503-512
35. Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature 340, 245-246
36. Huang, J., Zhao, Q., Mooney, S. M. and Lee, F. S. (2002) Sequence determinants in hypoxia-inducible factor-1α for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J. Biol. Chem. 277, 39792-39800
37. Iyer, N. V., Leung, S. W. and Semenza, G. L. (1998) The human hypoxia-inducible factor 1α gene: HIF1A structure and evolutionary conservation. Genomics 52, 159-165
38. Yu, F., White, S. B., Zhao, Q. and Lee, F. S. (2001) Dynamic, site-specific interaction of hypoxia-inducible factor-1α with the von Hippel-Lindau tumor suppressor protein. Cancer Res. 61, 4136-4142
39. Lee, F. S., Peters, R. T., Dang, L. C. and Maniatis, T. (1998) MEKK1 activates both IκB kinase α and IκB kinase β. Proc. Natl. Acad. Sci. U.S.A. 95, 9319-9324
40. Tu, Z., Kelley, V. R., Collins, T. and Lee, F. S. (2001) IκB kinase is critical for TNF-α-induced VCAM1 gene expression in renal tubular epithelial cells. J. Immunol. 166, 6839-6846
41. Paddison, P. J., Caudy, A. A., Bernstein, E., Hannon, G. J. and Conklin, D. S. (2002) Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16, 948-958
42. Berra, E., Benizri, E., Ginouves, A., Volmat, V., Roux, D. and Pouyssegur, J. (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1a in normoxia. EMBO J. 22, 4082-4090
43. Zhao, Q. and Lee, F. S. (2003) The transcriptional activity of the APP intracellular domain-Fees complex is inhibited by activation of the NF-κB pathway. Biochemistry 42, 3627-3634
44. Horner, D. S., Heil, B., Happe, T. and Embley, T. M. (2002) Iron hydrogenases: ancient enzymes in modern eukaryotes. Trends Biochem. Sci. 27, 148-153
45. Frey, M. (2002) Hydrogenases: hydrogen-activating enzymes. ChemBioChem 3, 153-160
46. Vignais, P. M., Billoud, B. and Meyer, J. (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25, 455-501
47. Barton, R. M. and Worman, H. J. (1999) Prenylated prelamin A interacts with Narf, a novel nuclear protein. J. Biol. Chem. 274, 30008-30018
48. Peters, J. W. (1999) Structure and mechanism of iron-only hydrogenases. Curr. Opin. Struct. Biol. 9, 670-676
49. Nicolet, Y., Lemon, B. J., Fontecilla-Camps, J. C. and Peters, J. W. (2000) A novel FeS cluster in Fe-only hydrogenases. Trends Biochem. Sci. 25, 138-143
50. Rees, D. C. and Howard, J. B. (2003) The interface between the biological and inorganic worlds: iron-sulfur metalloclusters. Science 300, 929-931
51. Freeman, R. S., Hasbani, D. M., Lipscomb, E. A., Straub, J. A. and Xie, L (2003) SM-20, EGL-9, and the EGLN family of hypoxia-inducible factor prolyl hydroxylases. Mol. Cell 16, 1-12
52. Appelholf, R. J., Tian, Y. M., Raval, R. R., Turley, H., Harris, A. L., Pugh, C. W., Ratcliffe, P. J. and Gleadle, J. M. (2004) Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 279, 38458-38465
53. Marxsen, J. H., Stengel, P., Doege, K., Heikkinen, P., Jokilehto, T., Wagner, T., Jelkmann, W., Jaakkola, P. and Metzen, E. (2004) Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-α-prolyl-4- hydroxylases. Biochem. J. 381, 761-767
54. Aprelikova, O., Chandramouli, G. V., Wood, M., Vasselli, J. R., Riss, J., Maranchie, J. K., Linehan, W. M. and Barrett, J. C. (2004) Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 92, 491-501
55. Greijer, A., van der Groep, P., Kemming, D., Shvarts, A., Semenza, G., Meijer, G., van de Wiel, M., Belien, J., van Diest, P. and van der Wall, E. (2005) Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J. Pathol. 206, 291-304
56. Balk, J., Pierik, A. J., Netz, D. J., Muhlenhoff, U. and Lill, R. (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23, 2105-2115
57. Metzen, E., Stiehl, D. P., Doege, K., Marxsen, J. H., Hellwig-Burgel, T. and Jelkmann, W. (2005) Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: identification of a functional hypoxia-responsive element. Biochem. J. 387, 711-717
58. del Peso, L., Castellanos, M. C., Temes, E., Martin-Puig, S., Cuevas, Y., Olmos, G. and Landazuri, M. O. (2003) The von Hippel Lindau/hypoxia-inducible factor (HIF) pathway regulates the transcription of the HIF-proline hydroxylase genes in response to low oxygen. J. Biol. Chem. 278, 48690-48695
59. Pescador, N., Cuevas, Y., Naranjo, S., Alcaide, M., Villar, D., Landazuri, M. O. and Del Peso, L. (2005) Identification of a functional hypoxia-responsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem. J. 390, 189-197
60. Kaelin, Jr, W. G. (2005) The von Hippel-Lindau protein, HIF hydroxylation, and oxygen sensing. Biochem. Biophys. Res. Commun. 338, 627-638
61. Schofield, C. J. and Ratcliffe, P. J. (2004) Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354
62. Nakayama, K., Frew, I. J., Hagensen, M., Skals, M., Habelhah, H., Bhoumik, A., Kadoya, T., Erdjument-Bromage, H., Tempst, P., Frappeli, P. B. et al. (2004) Siah2 regulates stability of prolyl-hydroxylases, controls HIF1α abundance, and modulates physiological responses to hypoxia. Cell 117, 941-952
63. Bae, M. K., Ahn, M. Y., Jeong, J. W., Bae, M. H., Lee, Y. M., Bae, S. K., Park, J. W., Kim, K. R. and Kim, K. W. (2002) Jab1 interacts directly with HIF-1α and regulates its stability. J. Biol. Chem. 277, 9-12
64. Bemis, L., Chan, D. A., Finkielstein, C. V., Qi, L., Sutphin, P. D., Chen, X., Stenmark, K., Giaccia, A. J. and Zundel, W. (2004) Distinct aerobic and hypoxic mechanisms of HIF-α regulation by CSN5. Genes Dev. 18, 739-744
65. Ozer, A., Wu, L. C. and Bruick, R. K. (2005) The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proc. Natl. Acad. Sci. U.S.A. 102, 7481-7486
66. Isaacs, J. S., Jung, Y. J., Mimnaugh, E. G., Martinez, A., Cuttitta, F. and Neckers, L. M. (2002) Hsp90 regulates a von Hippei Lindau-independent hypoxia-inducible factor-1 α-degradative pathway. J. Biol. Chem. 277, 29936-29944
67. Corn, P. G., McDonald, III, E. R., Herman, J. G. and El-Deiry, W. S. (2003) Tat-binding protein-1, a component of the 26S proteasome, contributes to the E3 ubiquitin ligase function of the von Hippel-Lindau protein. Nat. Genet. 35, 229-237
68. Jeong, J. W., Bae, M. K., Ahn, M. Y., Kim, S. H., Sohn, T. K., Bae, M. H., Yoo, M. A., Song, E. J., Lee, K. J. and Kim, K. W. (2002) Regulation and destabilization of HIF-1α by ARD1-mediated acetylation. Cell 111, 709-720
69. Li, Z., Wang, D., Messing, E. M. and Wu, G. (2005) VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1α. EMBO Rep. 6, 373-378
70. An, W. G., Kanekal, M., Simon, M. C., Maltepe, E., Blagosklonny, M. V. and Neckers, L. M. (1998) Stabilization of wild-type p53 by hypoxia-inducible factor 1α. Nature 392, 405-408
71. Bardos, J. I. and Ashcroft, M. (2005) Negative and positive regulation of HIF-1: a complex network. Biochim. Biophys. Acta 1755, 107-120
72. Meyer, J. (2000) Clostridial iron-sulphur proteins. J. Mol. Microbiol. Biotechnol. 2, 9-14
73. Armstrong, F. A. (2004) Hydrogenases: active site puzzles and progress. Curr. Opin. Chem. Biol. 8, 133-140
74. Peters, J. W., Lanzilotta, W. N., Lemon, B. J. and Seefeldt, L C. (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282, 1853-1858
75. Nicolet, Y., Piras, C., Legrand, P., Hatchikian, C. E. and Fontecilla-Camps, J. C. (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7, 13-23
76. Hackstein, J. H., Akhmanova, A., Boxma, B., Harhangi, H. R. and Voncken, F. G. (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol. 7, 441-447
77. Happe, T., Hemschemeier, A., Winkler, M. and Kaminski, A. (2002) Hydrogenases in green algae: do they save the algae's life and solve our energy problems? Trends Plant Sci. 7, 246-250
78. Dyall, S. D., Yan, W., Oelgadillo-Correa, M.G., Lunceford, A., Loo, J. A., Clarke, C. F. and Johnson, P. J. (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103-1107
79. Hrdy, I., Hirt, R. P., Dolezal, P., Bardonova, L., Foster, P. G., Tachezy, J. and Embley, T. M. (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618-622