Evidence for the slow reaction of hypoxia-inducible factor prolyl hydroxylase 2 with oxygen

FEBS Journal

Volumn 277, Issue 19, 2010, Pages 4089-4099

  Flashman, Emily ^a   Hoffart, Lee M ^b   Hamed, Refaat B ^a,c   Bollinger Jr , J Martin ^b   Krebs, Carsten ^b   Schofield, Christopher J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c Assiut University   (Egypt)

Author keywords

2 oxoglutarate; hypoxia inducible factor; oxygen; oxygenase; prolyl hydroxylase; spectroscopy

Indexed keywords

2 OXOGLUTARIC ACID; FERROUS ION; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; HIF1A PROTEIN, HUMAN; PEPTIDE; RECOMBINANT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; MOSSBAUER SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; ULTRAVIOLET SPECTROSCOPY; AMINO ACID SEQUENCE; CATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; HUMAN; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ANIMALIA;

AMINO ACID SEQUENCE; CATALYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PEPTIDES; PROCOLLAGEN-PROLINE DIOXYGENASE; RECOMBINANT PROTEINS; SPECTROSCOPY, MOSSBAUER; SUBSTRATE SPECIFICITY;

EID: 77956631879     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07804.x     Document Type: Article

References (63)

1. Semenza GL Wang GL (1992) A nuclear factor induced by hypoxia via denovo protein- synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12, 5447 5454.
2. Kaelin WG Jr. Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30, 393 402.
3. Schofield CJ Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5, 343 354.
4. Semenza GL (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 19, 176 182.
5. Wang GL Semenza GL (1995) Purification and characterization of hypoxia-inducible factor-1. J Biol Chem 270, 1230 1237.
6. 2 sensing. Science 292, 464 468.
7. 2-regulated prolyl hydroxylation. Science 292, 468 472.
8. Lando D, Peet DJ, Whelan DA, Gorman JJ Whitelaw ML (2002) Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295, 858 861.
9. Bruick RK McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337 1340.
10. Epstein ACR, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, 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.
11. Taylor MS (2001) Characterization and comparative analysis of the EGLN gene family. Gene 275, 125 132.
12. Hewitson KS, McNeill LA, Riordan MV, Tian YM, Bullock AN, Welford RWD, Elkins JM, Oldham NJ, Battacharya S, Gleadle J 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.
13. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML Bruick RK (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 16, 1466 1471.
14. Takeda K, Cowan A Fong GH (2007) Essential role for prolyl hydroxylase domain protein 2 in oxygen homeostasis of the adult vascular system. Circulation 116, 774 781.
15. Berra E, Benizri E, Ginouves A, Volmat V, Roux D Pouyssegur J (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J 22, 4082 4090.
16. Clifton IJ, McDonough MA, Ehrismann D, Kershaw NJ, Granatino N Schofield CJ (2006) Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J Inorg Biochem 100, 644 669.
17. Costas M, Mehn MP, Jensen MP Que L (2004) Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates. Chem Rev 104, 939 986.
18. Hausinger RP (2004) Fe(II)/α-ketoglutarate-dependent hydroxylases and related enzymes. Crit Rev Biochem Mol 39, 21 68.
19. Solomon EI, Brunold TC, Davis MI, Kemsley JN, Lee SK, Lehnert N, Neese F, Skulan AJ, Yang YS Zhou J (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem Rev 100, 235 350.
20. Krebs C, Galonić Fujimori D, Walsh CT Bollinger JM Jr. (2007) Non-heme Fe(IV)-oxo intermediates. Acc Chem Res 40, 484 492.
21. Hanauske-Abel HM Günzler V (1982) A stereochemical concept for the catalytic mechanism of prolyl hydroxylase: applicability to classification and design of inhibitors. J Theor Biol 94, 421 455.
22. Bollinger JM Jr. , Price JC, Hoffart LM, Barr EW Krebs C (2005) Mechanism of oxygen activation by taurine: α-ketoglutarate dioxygenase (TauD) from Escherichia coli. Eur J Inorg Chem 2005, 4245 4254. (Pubitemid 41587542)
23. Koehntop KD, Emerson JP Que L Jr. (2005) The 2-His-1-carboxylate facial triad: a versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes. J Biol Inorg Chem 10, 87 93.
24. Que L (2000) One motif - many different reactions. Nat Struct Biol 7, 182 184.
25. Valegård K, van Scheltinga ACT, Lloyd MD, Hara T, Ramaswamy S, Perrakis A, Thompson A, Lee HJ, Baldwin JE, Schofield CJ et al. (1998) Structure of a cephalosporin synthase. Nature 394, 805 809.
26. Zhang Z, Ren J, Stammers DK, Baldwin JE, Harlos K Schofield CJ (2000) Structural origins of the selectivity of the trifunctional oxygenase clavaminic acid synthase. Nat Struct Biol 7, 127 133.
27. Pavel EG, Zhou J, Busby RW, Gunsior M, Townsend CA Solomon EI (1998) Circular dichroism and magnetic circular dichroism spectroscopic studies of the non-heme ferrous active site in clavaminate synthase and its interaction with alpha-ketoglutarate cosubstrate. J Am Chem Soc 120, 743 753.
28. Zhou J, Gunsior M, Bachmann BO, Townsend CA Solomon EI (1998) Substrate binding to the α-ketoglutarate-dependent non-heme iron enzyme clavaminate synthase 2: coupling mechanism of oxidative decarboxylation and hydroxylation. J Am Chem Soc 120, 13539 13540.
29. Whiting AK, Que L, Saari RE, Hausinger RP, Fredrick MA McCracken J (1997) Metal coordination environment of a Cu(II)-substituted α-keto acid-dependent dioxygenase that degrades the herbicide 2,4-D. J Am Chem Soc 119, 3413 3414.
30. Welford RW, Kirkpatrick JM, McNeill LA, Puri M, Oldham NJ Schofield CJ (2005) Incorporation of oxygen into the succinate co-product of iron(II) and 2-oxoglutarate dependent oxygenases from bacteria, plants and humans. FEBS Lett 579, 5170 5174.
31. Price JC, Barr EW, Tirupati B, Bollinger JM Jr. Krebs C (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an alpha-ketoglutarate-dependent dioxygenase: a high-spin FeIV complex in taurine/alpha-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42, 7497 7508.
32. Hoffart LM, Barr EW, Guyer RB, Bollinger JM Jr. Krebs C (2006) Direct spectroscopic detection of a C-H-cleaving high-spin Fe(IV) complex in a prolyl-4-hydroxylase. Proc Natl Acad Sci U S A 103, 14738 14743.
33. Price JC, Barr EW, Glass TE, Krebs C Bollinger JM Jr. (2003) Evidence for hydrogen abstraction from C1 of taurine by the high-spin Fe(IV) intermediate detected during oxygen activation by taurine: alpha-ketoglutarate dioxygenase (TauD). J Am Chem Soc 125, 13008 13009.
34. Groves JT (1985) Key elements of the chemistry of cytochrome P-450. J Chem Educ 62, 928 931.
35. Price JC, Barr EW, Hoffart LM, Krebs C Bollinger JM Jr. (2005) Kinetic dissection of the catalytic mechanism of taurine: alpha-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 44, 8138 8147.
36. McDonough MA, Li V, Flashman E, Chowdhury R, Mohr C, Lienard BM, Zondlo J, Oldham NJ, Clifton IJ, Lewis J et al. (2006) Cellular oxygen sensing: crystal structure of hypoxia-inducible factor prolyl hydroxylase (PHD2). Proc Natl Acad Sci U S A 103, 9814 9819.
37. Chowdhury R, McDonough MA, Mecinovic J, Loenarz C, Flashman E, Hewitson KS, Domene C Schofield CJ (2009) Structural basis for binding of hypoxia-inducible factor to the oxygen-sensing prolyl hydroxylases. Structure 17, 981 989.
38. Bleijlevens B, Shivarattan T, Flashman E, Yang Y, Simpson PJ, Koivisto P, Sedgwick B, Schofield CJ Matthews SJ (2008) Dynamic states of the DNA repair enzyme AlkB regulate product release. EMBO Rep 9, 872 877.
39. McNeill LA, Flashman E, Buck MR, Hewitson KS, Clifton IJ, Jeschke G, Claridge TD, Ehrismann D, Oldham NJ Schofield CJ (2005) Hypoxia-inducible factor prolyl hydroxylase 2 has a high affinity for ferrous iron and 2-oxoglutarate. Mol Biosyst 1, 321 324.
40. Dao JH, Kurzeja RJ, Morachis JM, Veith H, Lewis J, Yu V, Tegley CM Tagari P (2009) Kinetic characterization and identification of a novel inhibitor of hypoxia-inducible factor prolyl hydroxylase 2 using a time-resolved fluorescence resonance energy transfer-based assay technology. Anal Biochem 384, 213 223.
41. Ehrismann D, Flashman E, Genn DN, Mathioudakis N, Hewitson KS, Ratcliffe PJ Schofield CJ (2007) Studies on the activity of the hypoxia-inducible-factor hydroxylases using an oxygen consumption assay. Biochem J 401, 227 234.
42. Flashman E, Bagg EAL, Chowdhury R, Mecinovic J, Loenarz C, McDonough MA, Hewitson KS Schofield CJ (2008) Kinetic rationale for selectivity toward N- and C-terminal oxygen-dependent degradation domain substrates mediated by a loop region of hypoxia-inducible factor prolyl hydroxylases. J Biol Chem 283, 3808 3815.
43. Tuckerman Jr. Zhao Y, Hewitson KS, Tian YM, Pugh CW, Ratcliffe PJ Mole DR (2004) Determination and comparison of specific activity of the HIF-prolyl hydroxylases. FEBS Lett 576, 145 150.
44. Hirsilä M, Koivunen P, Günzler V, Kivirikko KI Myllyharju J (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem 278, 30772 30780.
45. Koivunen P, Hirsilä M, Günzler V, Kivirikko KI Myllyharju J (2004) 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, 9899 9904.
46. Flashman E, Davies SL, Yeoh KK Schofield CJ (2010) Investigating the dependence of the hypoxia-inducible factor hydroxylases (factor inhibiting HIF and prolyl hydroxylase domain 2) on ascorbate and other reducing agents. Biochem J 427, 135 142.
47. Knowles HJ, Raval RR, Harris AL Ratcliffe PJ (2003) Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res 63, 1764 1768.
48. Grzyska PK, Ryle MJ, Monterosso GR, Liu J, Ballou DP Hausinger RP (2005) Steady-state and transient kinetic analyses of taurine/alpha-ketoglutarate dioxygenase: effects of oxygen concentration, alternative sulfonates, and active-site variants on the FeIV-oxo intermediate. Biochemistry 44, 3845 3855.
49. Bollinger JM Jr. Krebs C (2006) Stalking intermediates in oxygen activation by iron enzymes: motivation and method. J Inorg Biochem 100, 586 605.
50. Ryle MJ, Padmakumar R Hausinger RP (1999) Stopped-flow kinetic analysis of Escherichia coli taurine/alpha-ketoglutarate dioxygenase: interactions with alpha-ketoglutarate, taurine, and oxygen. Biochemistry 38, 15278 15286.
51. Neidig ML, Brown CD, Light KM, Fujimori DG, Nolan EM, Price JC, Barr EW, Bollinger JM Jr. , Krebs C, Walsh CT et al. (2007) CD and MCD of CytC3 and taurine dioxygenase: role of the facial triad in alpha-KG-dependent oxygenases. J Am Chem Soc 129, 14224 14231.
52. Galonić DP, Barr EW, Walsh CT, Bollinger JM Jr. Krebs C (2007) Two interconverting Fe(IV) intermediates in aliphatic chlorination by the halogenase CytC3. Nat Chem Biol 3, 113 116.
53. Matthews ML, Krest CM, Barr EW, Vaillancourt FH, Walsh CT, Green MT, Krebs C Bollinger JM (2009) Substrate-triggered formation and remarkable stability of the C-H bond-cleaving chloroferryl intermediate in the aliphatic halogenase, SyrB2. Biochemistry 48, 4331 4343.
54. Koivunen P, Hirsilä M, Kivirikko KI Myllyharju J (2006) The length of peptide substrates has a marked effect on hydroxylation by the hypoxia-inducible factor prolyl 4-hydroxylases. J Biol Chem 281, 28712 28720.
55. Matthews ML, Neumann CS, Miles LA, Grove TL, Booker SJ, Krebs C, Walsh CT Bollinger JM Jr. (2009) Substrate positioning controls the partition between halogenation and hydroxylation in the aliphatic halogenase, SyrB2. Proc Natl Acad Sci USA 106, 17723 17728.
56. Eser BE, Barr EW, Frantom PA, Saleh L, Bollinger JM Jr. , Krebs C Fitzpatrick PF (2007) Direct spectroscopic evidence for a high-spin Fe(IV) intermediate in tyrosine hydroxylase. J Am Chem Soc 129, 11334 11335.
57. Krebs C, Price JC, Baldwin J, Saleh L, Green MT Bollinger JM Jr. (2005) Rapid freeze-quench 57Fe Mössbauer spectroscopy: monitoring changes of an iron-containing active site during a biochemical reaction. Inorg Chem 44, 742 757.
58. Chowdhury R, Hardy A Schofield CJ (2008) The human oxygen sensing machinery and its manipulation. Chem Soc Rev 37, 1308 1319.
59. Hirota K Semenza GL (2005) Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases. Biochem Biophys Res Commun 338, 610 616.
60. Schofield CJ Ratcliffe PJ (2005) Signalling hypoxia by HIF hydroxylases. Biochem Biophys Res Commun 338, 617 626.
61. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ Harris AL (2000) The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 157, 411 421.
62. Zhang Z, Ren J, Harlos K, McKinnon CH, Clifton IJ Schofield CJ (2002) Crystal structure of a clavaminate synthase.Fe(II).2-oxoglutarate.substrate.NO complex: evidence for metal centered rearrangements. FEBS Lett 517, 7 12.
63. Leung IKH, Flashman E, Yeoh KK, Schofield CJ Claridge TD (2010) Using NMR solvent water relaxation to investigate metalloenzyme-ligand binding interactions. J Med Chem 53, 867 875.