Evidence that oxidative dephosphorylation by the nonheme Fe(II), α-ketoglutarate:UMP oxygenase occurs by stereospecific hydroxylation

FEBS Letters

Volumn 591, Issue 3, 2017, Pages 468-478

  Goswami, Anwesha ^a   Liu, Xiaodong ^a   Cai, Wenlong ^a   Wyche, Thomas P ^b   Bugni, Tim S ^b   Meurillon, Maïa ^c   Peyrottes, Suzanne ^c   Perigaud, Christian ^c   Nonaka, Koichi ^d   Rohr, Jürgen ^a   Van Lanen, Steven G ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIV MONTPELLIER   (France)

^d DAIICHI SANKYO CO   (Japan)

Author keywords

antibiotic; biosynthesis; nonheme iron; nucleoside; oxygenase; translocase I

Indexed keywords

2 OXOGLUTARIC ACID; IRON; OXYGENASE; UNCLASSIFIED DRUG; URIDINE MONOPHOSPHATE OXYGENASE; ALPHA-KETOGLUTARIC ACID; HEME; HYDROGEN; URIDINE PHOSPHATE;

BIOCHEMISTRY; CATALYST; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HYDROXYLATION; LETTER; MOLECULAR PROBE; OXIDATIVE PHOSPHORYLATION; PROTEIN SYNTHESIS; BIOCATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; STEREOISOMERISM;

BIOCATALYSIS; HEME; HYDROGEN; HYDROXYLATION; IRON; KETOGLUTARIC ACIDS; OXIDATION-REDUCTION; OXYGENASES; PHOSPHORYLATION; STEREOISOMERISM; SUBSTRATE SPECIFICITY; URIDINE MONOPHOSPHATE;

EID: 85012982886     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12554     Document Type: Article

References (47)

1. Hausinger RP (2004) Fe(II)/α-ketoglutarate-dependent hydroxylases and related enzymes. Crit Rev Biochem Mol Biol 39, 21–68.
2. Wu LF, Meng S and Tang GL (2016) Ferrous iron and α-ketoglutarate-dependent dioxygenases in the biosynthesis of microbial natural products. Biochim Biophys Acta 1864, 453–470.
3. Schofield C and Hausinger R (2015) RSC Metatallobiology: 2-Oxoglutarate-Dependent Oxygenases, Royal Society of Chemistry.
4. Martinex S and Hausinger RP (2015) Catalytic mechanisms of Fe(II)- and 2-oxoglutarate-dependent oxygenases. J Biol Chem 290, 20702–20711.
5. Bollinger JM and Krebs C (2006) Stalking intermediates in oxygen activation by iron enzymes: motivation and method. J Inorg Biochem 100, 586–605.
6. Hangasky JA, Taabazuiing CY, Valliere MA and Knapp JA (2013) Imposing function down a (cupin)-barrel: secondary structure and metal stereochemistry in the αKG-dependent oxygenases. Metallomics 5, 287–301.
7. Schofield CJ and Zhang Z (1999) Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr Opin Struct Biol 9, 722–731.
8. Srnec M, Wong SD, Matthews ML, Krebs C, Bollinger JM and Solomon EI (2016) Electronic structure of the ferryl intermediate in the α-ketoglutarate dependent non-heme iron halogenase SyrB2: contributions to H atom abstraction reactivity. J Am Chem Soc 138, 5110–5122.
9. Matthews ML, Neumann CS, Miles LA, Grove TL, Booker SJ, Krebs C, Walsh CT and Bollinger JM (2009) Substrate positioning controls the partition between halogenation and hydroxylation in the aliphatic halogenase, SyrB2. Proc Natl Acad Sci USA 42, 17723–17728.
10. Usharani D, Janardanan D and Shaik S (2010) Does the TauD enzyme always hydroxylate alkanes, while an analogous synthetic non-heme reagent always desaturates them? J Am Chem Soc 133, 176–179.
11. Kulik HJ and Drennan CL (2013) Substrate placement influences reactivity in non-heme halogenases and hydroxylases. J Biol Chem 288, 11233–11241.
12. Solomon EI, Light KM, Liu LV, Srnec M and Wong SD (2013) Geometric and electronic structure contributions to function in non-heme iron enzymes. Acc Chem Res 46, 2725–2739.
13. Yang Z, Chi X, Funabashi M, Baba S, Nonaka K, Pahari P, Unrine J, Jacobsen JM, Elliott GI, Rohr J et al. (2011) Characterization of LipL as a non-heme, Fe (II)-dependent α-ketoglutarate: UMP dioxygenase that generates uridine-5′-aldehyde during A-90289 biosynthesis. J Biol Chem 286, 7885–7892.
14. Yang Z, Unrine J, Nonaka K and Van Lanen SG (2012) Fe(II)-dependent, uridine-5′-monophosphate: α-ketoglutarate dioxygenases in the synthesis of 5′-modified nucleosides. Methods Enzymol 516, 153–168.
15. Cai W, Goswami A, Yang Z, Liu X, Green KD, Barnard-Britson S, Baba S, Funabashi M, Nonaka K, Sunkara M et al. (2015) The biosynthesis of capuramycin-type antibiotics: identification of the A-102395 biosynthetic gene cluster, mechanism of self-resistance, and formation of uridine-5′-carboxamide. J Biol Chem 290, 13710–13724.
16. Winn M, Goss RJ, Kimura KI and Bugg TD (2010) Antimicrobial nucleoside antibiotics targeting cell wall assembly: recent advances in structure–function studies and nucleoside biosynthesis. Nat Prod Rep 27, 279–304.
17. Salowe SP, Marsh EN and Townsend CA (1990) Purification and characterization of clavaminate synthase from Streptomyces clavuligerus: An unusual oxidative enzyme in natural product biosynthesis. Biochemistry 29, 6499–6508.
18. Busby RW and Townsend CA (1996) A single monomeric iron center catalyzes three nonsuccessive oxidative transformations. Bioorg Med Chem 4, 1059–1064.
19. Zhang Z, Ren J, Stammers DK, Baldwin JE, Harlos K and Schofield CJ (2000) Structural origins of the selectivity of the trifunctional oxygenase clavaminic acid synthase. Nat Struct Biol 7, 127–133.
20. Zhang Z, Ren JS, Harlos K, McKinnon CH, Clifton IJ and 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.
21. Eichhorn E, van der Ploeg JR, Kertesz MA and Leisinger T (1997) Characterization of α-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J Biol Chem 272, 23031–23036.
22. Price JC, Barr EW, Tirupati B, Bollinger JM Jr and Krebs C (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an α-ketoglutarate-dependent dioxygenase: a high-spin Fe (IV) complex in taurine/α-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42, 7497–7508.
23. Proshlyakov DA, Henshaw TF, Monterosso GR, Ryle MJ and 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.
24. Riggs-Gelasco PJ, Price JC, Guyer RB, Brehm JH, Barr EW, Bollinger JM and Krebs C (2004) EXAFS spectroscopic evidence for an Fe O unit in the Fe (IV) intermediate observed during oxygen activation by taurine:α-ketoglutarate dioxygenase. J Am Chem Soc 126, 8108–8109.
25. Grzyska PK, Appelman EH, Hausinger RP and Proshlyakov DA (2010) Insight into the mechanism of an iron dioxygenase by resolution of steps following the FeIV═ O species. Proc Natl Acad Sci 107, 3982–3987.
26. Kahnert A and Kertesz MA (2000) Characterization of a sulfur-regulated oxygenative alkylsulfatase from Pseudomonas putida S-313. J Biol Chem 275, 31661–31667.
27. Müller I, Kahnert A, Pape T, Sheldrick GM, Meyer-Klaucke W, Dierks T, Kertesz M and Usón I (2004) Crystal structure of the alkylsulfatase AtsK: insights into the catalytic mechanism of the Fe(II) α-ketoglutarate-dependent dioxygenase superfamily. Biochemistry 43, 3075–3088.
28. Meurillon M, Chaloin L, Périgaud C and Peyrottes S (2011) Synthesis of pyrimidine-containing nucleoside β-(R/S)-hydroxyphosphonate analogues. Eur J Org Chem 00, 3794–3802.
29. Parkin DW, Leung HB and Schramm VL (1984) Synthesis of nucleotides with specific radiolabels in ribose. Primary 14C and secondary 3H kinetic isotope effects on acid-catalyzed glycosidic bond hydrolysis of AMP, dAMP, and inosine. J Biol Chem 259, 9411–9417.
30. Lienhard GE and Rose IA (1964) The mechanism of action of 6-phosphogluconate dehydrogenase. Biochemistry 3, 190–195.
31. Malaisse W, Zahner D, Malaisse Lagae F, Verbruggen I, Kayser F, Biesemans M and Willem R (1994) Diastereotopic specificity of phosphoriboisomerase. Med Sci Res 22, 247–249.
32. Xu Y, Flavin MT and Xu ZQ (1996) Preparation of new Wittig reagents and their application to the synthesis of α, β-unsaturated phosphonates. J Org Chem 61, 7697–7701.
33. Yengoyan L and Rammler DH (1966) Nucleoside phosphonic acids. I. The synthesis of 5′-deoxyuridine 5′-phosphonic acids and derivatives. Biochemistry 5, 3629–3638.
34. Price JC, Barr EW, Glass TE, Krebs C and 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:α-ketoglutarate dioxygenase (TauD). J Am Chem Soc 125, 13008–13009.
35. Price JC, Barr EW, Hoffart LM, Krebs C and Bollinger JM (2005) Kinetic dissection of the catalytic mechanism of taurine: α-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 44, 8138–8147.
36. McCusker KP and Klinman JP (2009) Modular behavior of TauD provides insight into the origin of specificity in α-ketoglutarate-dependent nonheme iron oxygenases. Proc Natl Acad Sci USA 106, 19791–19795.
37. McCusker KP and Klinman JP (2009) Facile synthesis of 1, 1-[2 H 2]-2-methylaminoethane-1-sulfonic acid as a substrate for taurine α ketoglutarate dioxygenase (TauD). Tetrahedron Lett 50, 611–613.
38. Muthukumaran RB, Grzyska PK, Hausinger RP and McCracken J (2007) Probing the iron-substrate orientation for taurine/α-ketoglutarate dioxygenase using deuterium electron spin echo envelope modulation spectroscopy. Biochemistry 46, 5951–5959.
39. Casey TM, Grzyska PK, Hausinger RP and McCracken J (2013) Measuring the orientation of taurine in the active site of the non-heme Fe (II)/α-ketoglutarate-dependent taurine hydroxylase (TauD) using electron spin echo envelope modulation (ESEEM) spectroscopy. J Phys Chem 117, 10384–10394.
40. Yi C, Jia G, Hou G, Dai Q, Zhang W, Zheng G, Jian X, Yang C-G, Cui Q and He C (2010) Iron-catalyzed oxidation intermediates captured in a DNA repair dioxygenase. Nature 468, 330–333.
41. Chang WC, Guo Y, Wang C, Butch SE, Rosenzweig AC, Boal AK, Krebs C and Bollinger JM (2014) Mechanism of the C5 stereoinversion reaction in the biosynthesis of carbapenem antibiotics. Science 343, 1140–1144.
42. Clifton IJ, Doan LX, Sleeman MC, Topf M, Suzuki H, Wilmouth RC and Schofield CJ (2003) Crystal structure of carbapenem synthase (CarC). J Biol Chem 278, 20843–20850.
43. Salowe SP, Krol WJ, Iwata-Reuyl D and Townsend CA (1991) Elucidation of the order of oxidations and identification of an intermediate in the multistep clavaminate synthase reaction. Biochemistry 30, 2281–2292.
44. Nam W, Lee YM and Fukuzumi S (2014) Tuning reactivity and mechanism in oxidation reactions by mononuclear nonheme iron (IV)-oxo complexes. Acc Chem Res 47, 1146–1154.
45. Khaleeli N, Busby RW and Townsend CA (2000) Site-directed mutagenesis and biochemical analysis of the endogenous ligands in the ferrous active site of clavaminate synthase. The His-3 variant of the 2-His-1-carboxylate model. Biochemistry 39, 8666–8673.
46. Elkins JM, Ryle MJ, Clifton IJ, Dunning Hotopp JC, Lloyd JS, Burzlaff NI, Baldwin JE, Hausinger RP and Roach PL (2002) X-ray crystal structure of Escherichia coli taurine/α-ketoglutarate dioxygenase complexed to ferrous iron and substrates. Biochemistry 41, 5185–5192.
47. Jaroszewski L (2009) Protein structure prediction based on sequence similarity. Methods Mol Biol 569, 129–156.