Autocatalysed oxidative modifications to 2-oxoglutarate dependent oxygenases

FEBS Journal

Volumn 279, Issue 9, 2012, Pages 1563-1575

  Mantri, Monica ^a   Zhang, Zhihong ^a   McDonough, Michael A ^a   Schofield, Christopher J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

2 oxoglutarate oxygenase; ACCO; auto oxidation; ethylene; histone demethylases; hypoxia; JMJD6; oxidative fragmentation; reactive oxygen species; RNA splicing; self hydroxylation

Indexed keywords

1 AMINOCYCLOPROPANE 1 CARBOXYLIC ACID OXIDASE; 2 OXOGLUTARIC ACID; 2,4 DICHLOROPHENOXYACETATE OXYGENASE; OXIDOREDUCTASE; OXYGENASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AUTOOXIDATION; CATALYSIS; CHEMICAL REACTION KINETICS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME METABOLISM; ENZYME MODIFICATION; FRAGMENTATION REACTION; HYDROXYLATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEREOSPECIFICITY;

AMINO ACID OXIDOREDUCTASES; FERROUS COMPOUNDS; HYDROXYLATION; KETOGLUTARIC ACIDS; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXYGENASES; REPRESSOR PROTEINS;

EID: 84862819069     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08496.x     Document Type: Review

References (71)

1. Hausinger RP, (2004) Fe(II)/α-ketoglutarate dependent hydroxylases and related enzymes. Crit Rev Biochem Mol Biol 39, 21-68. (Pubitemid 38648162)
2. Flashman E, &, Schofield CJ, (2007) The most versatile of all reactive intermediates? Nat Chem Biol 3, 86-87. (Pubitemid 46134991)
3. Loenarz C, &, Schofield CJ, (2008) Expanding chemical biology of 2oxoglutarate oxygenases. Nat Chem Biol 4, 152-156. (Pubitemid 351264133)
4. Vaillancourt FH, Yin J, &, Walsh CT, (2005) SyrB2 in syringomycin E biosynthesis is a nonheme FeIIα-ketoglutarate- and O2-dependent halogenase. Proc Natl Acad Sci USA 102, 10111-10116. (Pubitemid 41023334)
5. Leung IKH, Krojer TJ, Kochan GT, Henry L, von Delft F, Claridge TDW, Oppermann U, McDonough MA, &, Schofield CJ, (2010) Structural and eechanistic studies on γ-butyrobetaine hydroxylase. Chem Biol 17, 1316-1324.
6. Loenarz C, Coleman ML, Boleininger A, Schierwater B, Holland PWH, Ratcliffe PJ, &, Schofield CJ, (2010) The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep 12, 63-70.
7. Loenarz C, &, Schofield CJ, (2011) Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxoglutarate oxygenases. Trends Biochem Sci 36, 7-18.
8. Baldwin JE, &, Bradley M, (1990) Isopenicillin N synthase: mechanistic studies. Chem Rev 90, 1079-1088.
9. Schofield CJ, &, Baldwin JE, (1992) Chapter 1. The biosynthesis of β-lactams. In The Chemistry of β-Lactam (, Page MI, ed.). Blackie Academic & Professional, London.
10. Baggaley KH, Brown AG, &, Schofield CJ, (1997) Chemistry and biosynthesis of clavulanic acid and other clavams. Nat Prod Rep 14, 309-333. (Pubitemid 27347840)
11. Lange T, Hedden P, &, Graebe JE, (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc Natl Acad Sci USA 91, 8552-8556. (Pubitemid 24273702)
12. Turnbull JJ, Nakajima J, Welford RWD, Yamazaki M, Saito K, &, Schofield CJ, (2004) Mechanistic studies on three 2-oxoglutarate dependent oxygenases of flavonoid biosynthesis. J Biol Chem 279, 1206-1216.
13. Roach PL, Clifton IJ, Fulop V, Harlos K, Barton GJ, Hajdu J, Andersson I, Schofield CJ, &, Baldwin JE, (1995) Crystal structure of isopenicillin N synthase is the first from a new structural family of enzymes. Nature 375, 700-704.
14. John P, (1997) Ethylene biosynthesis: the role of 1-aminocyclopropane- 1carboxylate (ACC) oxidase, and its possible evolutionary origin. Physiol Plant 100, 583-592. (Pubitemid 27340700)
15. Zhang Z, Ren J, Clifton IJ, &, Schofield CJ, (2004) Crystal structure and mechanistic implications of 1-aminocyclopropane-1-carboxylic acid oxidase-the ethylene-forming enzyme. Chem Biol 11, 1383-1394. (Pubitemid 39365164)
16. Rose NR, McDonough MA, King ONF, Kawamura A, &, Schofield CJ, (2011) Inhibition of 2-oxoglutarate dependent oxygenases. Chem Soc Rev 40, 4364-4397.
17. McDonough MA, Loenarz C, Chowdhury R, Clifton IJ, &, Schofield CJ, (2010) Structural studies on human 2-oxoglutarate dependent oxygenases. Curr Opin Struct Biol 20, 659-672.
18. Clifton IJ, McDonough MA, Ehrismann D, Kershaw NJ, Granatino N, &, Schofield CJ, (2006) Structural studies on 2-oxoglutarate oxygenases and related double-stranded β-helix fold proteins. J Inorg Biochem 100, 644-669.
19. Valegård K, van Scheltinga ACT, Lloyd MD, Hara T, Ramaswamy S, Perrakis A, Thompson A, Lee H-J, Baldwin JE, Schofield CJ, et al. (1998) Structure of a cephalosporin synthase. Nature 394, 805-809. (Pubitemid 28391648)
20. Hegg EL, &, Jr LQ, (1997) The 2-his-1-carboxylate facial triad-an emerging structural motif in mononuclear non-heme iron(II) enzymes. Eur J Biochem 250, 625-629. (Pubitemid 28022477)
21. Roach PL, Clifton IJ, Hensgens CMH, Shibata N, Schofield CJ, Hajdu J, &, Baldwin JE, (1997) Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation. Nature 387, 827-830. (Pubitemid 27270911)
22. Blasiak LC, Vaillancourt FH, Walsh CT, &, Drennan CL, (2006) Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis. Nature 440, 368-371.
23. Hewitson KS, Holmes SL, Ehrismann D, Hardy AP, Chowdhury R, Schofield CJ, &, McDonough MA, (2008) Evidence that two enzyme-derived histidine ligands are sufficient for iron binding and catalysis by factor inhibiting HIF (FIH). J Biol Chem 283, 25971-25978.
24. Valegård K, van Scheltinga ACT, Dubus A, Ranghino G, Oster LM, Hajdu J, &, Andersson I, (2004) The structural basis of cephalosporin formation in a mononuclear ferrous enzyme. Nat Struct Mol Biol 11, 95-101. (Pubitemid 38173447)
25. 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.
26. Stubbs CJ, Loenarz C, Mecinović J, Yeoh KK, Hindley N, Liénard BM, Sobott F, Schofield CJ, &, Flashman E, (2009) Application of a proteolysis/mass spectrometry method for investigating the effects of inhibitors on hydroxylase structure. J Med Chem 52, 2799-2805.
27. McDonough MA, McNeill LA, Tilliet M, Papamicaël CA, Chen Q-Y, Banerji B, Hewitson KS, &, Schofield CJ, (2005) Selective inhibition of factor Inhibiting hypoxia-inducible factor. J Am Chem Soc 127, 7680-7681. (Pubitemid 40745948)
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. (Pubitemid 29025230)
29. Zhang Z, Ren JS, 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 centred rearrangements. FEBS Lett 517, 7-12. (Pubitemid 34327621)
30. Krebs C, Galonić Fujimori D, Walsh CT, &, Bollinger JM, (2007) Non-heme Fe(IV)-oxo intermediates. Acc Chem Res 40, 484-492.
31. Proshlyakov DA, Henshaw TF, Monterosso GR, Ryle MJ, &, Hausinger RP, (2004) Direct detection of oxygen intermediates in the non-heme Fe enzyme taurine/α-ketoglutarate dioxygenase. J Am Chem Soc 126, 1022-1023. (Pubitemid 38140723)
32. Shaik S, Kumar D, de Visser SP, Altun A, &, Thiel W, (2005) Theoretical perspective on the structure and mechanism of cytochrome P450 enzymes. Chem Rev 105, 2279-2328. (Pubitemid 40947949)
33. Meunier B, de Visser SP, &, Shaik S, (2004) Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem Rev 104, 3947-3980.
34. 2- and alpha-ketoglutarate-dependent tyrosyl radical formation in TauD, an alpha-keto acid-dependent non-heme iron dioxygenase. Biochemistry 42, 1854-1862. (Pubitemid 36258659)
35. Liu A, Ho RYN, Que L, Ryle MJ, Phinney BS, &, Hausinger RP, (2001) Alternative reactivity of an α-ketoglutarate dependent iron(II) oxygenase: enzyme self-hydroxylation. J Am Chem Soc 123, 5126-5127. (Pubitemid 32905680)
36. Rocklin A, Kato K, Liu H-w, Que L, &, Lipscomb J, (2004) Mechanistic studies of 1-aminocyclopropane-1-carboxylic acid oxidase: single turnover reaction. J Biol Inorg Chem 9, 171-182. (Pubitemid 38327313)
37. Mirica LM, &, Klinman JP, (2008) The nature of O2 activation by the ethylene-forming enzyme 1-aminocyclopropane-1-carboxylic acid oxidase. Proc Natl Acad Sci USA 105, 1814-1819. (Pubitemid 351439420)
38. Ge W, Clifton IJ, Howard-Jones AR, Stok JE, Adlington RM, Baldwin JE, &, Rutledge PJ, (2009) Structural studies on the reaction of isopenicillin N synthase with a sterically demanding depsipeptide substrate analogue. ChemBioChem 10, 2025-2031.
39. Guengerich FP, (1999) Cytochrome P-450 3A4: regulation and role in drug metabolism. Ann Rev Pharmacol Toxicol 39, 1-17. (Pubitemid 29222549)
40. Guengerich FP, (2007) Cytochrome P450 and chemical toxicology. Chem Res Toxicol 21, 70-83. (Pubitemid 351219709)
41. Guengerich FP, (1978) Destruction of heme and hemoproteins mediated by liver microsomal reduced nicotinamide adenine dinucleotide phosphate-cytochrome P-450 reductase. Biochemistry 17, 3633-3639. (Pubitemid 8405395)
42. Chen YH, Comeaux LM, Eyles SJ, &, Knapp MJ, (2008) Auto-hydroxylation of FIH-1: an Fe(II), alpha-ketoglutarate-dependent human hypoxia sensor. Chem Commun 39, 4768-4770.
43. Elkins JM, Hewitson KS, McNeill LA, Seibel JF, Schlemminger I, Pugh CW, Ratcliffe PJ, &, Schofield CJ, (2003) Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF1α. J Biol Chem 278, 1802-1806. (Pubitemid 36801416)
44. Sundheim O, Vagbo CB, Bjoras M, Sousa MML, Talstad V, Aas PA, Drablos F, Krokan HE, Tainer JA, &, Slupphaug G, (2006) Human ABH3 structure and key residues for oxidative demethylation to reverse DNA/RNA damage. EMBO J 25, 3389-3397. (Pubitemid 44144212)
45. Henshaw TF, Feig M, &, Hausinger RP, (2004) Aberrant activity of the DNA repair enzyme AlkB. J Biol Inorg Chem 98, 856-861. (Pubitemid 38595287)
46. Ge Y, Lawhorn BG, ElNaggar M, Sze SK, Begley TP, &, McLafferty FW, (2003) Detection of four oxidation sites in viral prolyl-4-hydroxylase by top-down mass spectrometry. Protein Sci 12, 2320-2326. (Pubitemid 37163366)
47. Müller I, Stückl C, Wakeley J, Kertesz M, &, Usõn I, (2005) Succinate complex crystal structures of the α-ketoglutarate- dependent dioxygenase AtsK. J Biol Chem 280, 5716-5723. (Pubitemid 40280051)
48. Webby CJ, Wolf A, Gromak N, Dreger M, Kramer H, Kessler B, Nielsen ML, Schmitz C, Butler DS, Yates JR III, et al. (2009) Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science 325, 90-93.
49. Mantri M, Webby CJ, Loik ND, Hamed RB, Nielsen ML, McDonough MA, McCullagh JSO, Böttger A, Schofield CJ, &, Wolf A, (2012) Self-hydroxylation of the splicing factor lysyl hydroxylase, JMJD6. Med Chem Commun 3, 80-85.
50. Mantri M, Loik ND, Hamed RB, Claridge TDW, McCullagh JSO, &, Schofield CJ, (2011) The 2-oxoglutarate-dependent oxygenase JMJD6 catalyses oxidation of lysine residues to give 5S-hydroxylysine residues. ChemBioChem 12, 531-534.
51. Grzyska PK, Müller TA, Campbell MG, &, Hausinger RP, (2007) Metal ligand substitution and evidence for quinone formation in taurine/α-ketoglutarate dioxygenase. J Inorg Biochem 101, 797-808. (Pubitemid 46529002)
52. Zhang Z, Schofield CJ, Baldwin JE, Thomas P, &, John P, (1995) Expression, purification and characterization of 1-aminocyclopropane-1- carboxylate oxidase from tomato in Escherichia coli. Biochem J 307, 77-85.
53. Smith JJ, Zhang ZH, Schofield CJ, John P, &, Baldwin JE, (1994) Inactivation of 1-aminocyclopropane-1-carboxylate (ACC) oxidase. J Exp Bot 45, 521-527. (Pubitemid 2099404)
54. Barlow JN, Zhang Z, John P, Baldwin JE, &, Schofield CJ, (1997) Inactivation of 1-aminocyclopropane-1-carboxylate oxidase involves oxidative modifications. Biochemistry 36, 3563-3569. (Pubitemid 27143510)
55. Zhang Z, Barlow JN, Baldwin JE, &, Schofield CJ, (1997) Metal-catalyzed oxidation and mutagenesis studies on the iron(II) binding site of 1aminocyclopropane-1-carboxylate oxidase. Biochemistry 36, 15999-16007. (Pubitemid 28027405)
56. Stadtman ER, &, Oliver CN, (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266, 2005-2008. (Pubitemid 21909019)
57. Stadtman ER, (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62, 797-821. (Pubitemid 23237888)
58. Stadtman E, (1992) Protein oxidation and aging. Science 257, 1220-1224.
59. Wei C-H, Chou W-Y, &, Chang G-G, (1995) Identification of Asp258 as the metal coordinate of pigeon liver malic enzyme by site-specific mutagenesis. Biochemistry 34, 7949-7954.
60. 2+ ascorbate system. J Biol Chem 270, 25935-25941.
61. Nietfeld JJ, &, Kemp A, (1981) The function of ascorbate with respect to prolyl 4-hydroxylase activity. Biochim Biophys Acta 657, 159-167. (Pubitemid 11181775)
62. Blanchard JS, Englard S, &, Kondo A, (1982) γ-Butyrobetaine hydroxylase: a unique protective effect of catalase. Arch Biochem Biophys 219, 327-334.
63. 2+ dehydrogenases. Consensus target sequence between propanediol oxidoreductase of Escherichia coli and alcohol dehydrogenase II of Zymomonas mobilis. J Biol Chem 269, 6592-6597.
64. Levine RL, Oliver CN, Fulks RM, &, Stadtman ER, (1981) Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis. Proc Natl Acad Sci USA 78, 2120-2124.
65. Liaw SH, Villafranca JJ, &, Eisenberg D, (1993) A model for oxidative modification of glutamine synthetase, based on crystal structures of mutant H269N and the oxidized enzyme. Biochemistry 32, 7999-8003. (Pubitemid 23259657)
66. Myllyl R, Majamaa K, Günzler V, Hanauske-Abel HM, &, Kivirikko KI, (1984) Ascorbate is consumed stoichiometrically in the uncoupled reactions catalyzed by prolyl 4-hydroxylase and lysyl hydroxylase. J Biol Chem 259, 5403-5405. (Pubitemid 14144988)
67. De Jong L, Albracht SPJ, &, Kemp A, (1982) Prolyl 4-hydroxylase activity in relation to the oxidation state of enzyme-bound iron: the role of ascorbate in peptidyl proline hydroxylation. Biochim Biophys Acta Protein Struct Mol Enzymol 704, 326-332. (Pubitemid 12010842)
68. 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.
69. Buettner GR, &, Jurkiewicz BA, (1996) Catalytic metals, ascorbate and free radicals: combinations to avoid. Radiat Res 145, 532-541. (Pubitemid 26127160)
70. Welford RWD, 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. (Pubitemid 41319743)
71. 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 Mol Biol 7, 127-133. (Pubitemid 30082510)