Trapping and spectroscopic characterization of an FeIII-superoxo intermediate from a nonheme mononuclear iron-containing enzyme

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 39, 2010, Pages 16788-16793

  Mbughuni, Michael M ^a   Chakrabarti, Mrinmoy ^b   Hayden, Joshua A ^b   Bominaar, Emile L ^b   Hendrich, Michael P ^b   Münck, Eckard ^b   Lipscomb, John D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Oxygen activation; Oxygenase; Spectroscopy; Superoxide

Indexed keywords

4 NITROCATECHOL; HEME; HISTIDINE; IRON; NONHEME IRON PROTEIN; OXYGEN; OXYGEN 17; OXYGEN RADICAL; OXYGENASE; 3,4-DIHYDROXYPHENYLACETATE 2,3-DIOXYGENASE; CATECHOL DERIVATIVE; DIOXYGENASE; NITRO DERIVATIVE; NITROCATECHOL; SUPEROXIDE;

ABSORPTION SPECTROSCOPY; ARTICLE; CHEMICAL BINDING; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME SUBSTRATE; MOSSBAUER SPECTROSCOPY; PRIORITY JOURNAL; CHEMISTRY; CRYSTALLOGRAPHY; ENZYME SPECIFICITY; GENETICS; MUTATION; OXIDATION REDUCTION REACTION;

CATECHOLS; CRYSTALLOGRAPHY; DIOXYGENASES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; IRON; MUTATION; NITRO COMPOUNDS; OXIDATION-REDUCTION; SPECTROSCOPY, MOSSBAUER; SUBSTRATE SPECIFICITY; SUPEROXIDES;

EID: 78049259568     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1010015107     Document Type: Article

References (44)

1. 2+ of extradiol dioxygenases. J Biol Chem 261:2170-2178.
2. Baldwin JE, Bradley M (1990) Isopenicillin N synthase: Mechanistic studies. Chem Rev 90:1079-1088.
3. 2+ oxidase with metal coordination sites for small molecules and substrate. J Biol Chem 264:21677-21681.
4. Rocklin AM, et al. (2004) Mechanistic studies of 1-aminocyclopropane-1- carboxylic acid oxidase: Single turnover reaction. J Biol Inorg Chem 9:171-182.
5. Price JC, et al. (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 alpha-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42:7497-7508.
6. Proshlyakov DA, et al. (2004) Direct detection of oxygen intermediates in the nonheme Fe enzyme taurine/alpha-ketoglutarate dioxygenase. J Am Chem Soc 126:1022-1023.
7. Mukherjee A, et al. (2010) Oxygen activation at mononuclear nonheme iron centers: A superoxo perspective. Inorg Chem 49:3618-3628.
8. Kovaleva EG, Lipscomb JD (2008) Versatility of biological nonheme Fe(II) centers in oxygen activation reactions. Nat Chem Biol 4:186-193.
9. Weiss JJ (1964) Nature of the iron-oxygen bond in oxyhaemoglobin. Nature 202:83-84.
10. cam and its complexes. Mössbauer parameters of the heme iron. Biochim Biophys Acta 420:8-26.
11. cam at atomic resolution. Science 287:1615-1622.
12. Davydov R, et al. (2001) Hydroxylation of camphor by reduced oxy-cytochrome P450cam: Mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes. J Am Chem Soc 123:1403-1415. (Pubitemid 32167333)
13. Xing G, et al. (2006) Evidence for C-H cleavage by an iron-superoxide complex in the glycol cleavage reaction catalyzed by myo-inositol oxygenase. Proc Natl Acad Sci USA 103:6130-6135.
14. 2+ dioxygenase superoxo, alkylperoxo, and bound product intermediates. Science 316:453-457.
15. Shu L, et al. (1995) X-ray absorption spectroscopic studies of the Fe(II) active site of catechol 2,3-dioxygenase. Implications for the extradiol cleavage mechanism. Biochemistry 34:6649-6659.
16. Bugg TDH, Winfield CJ (1998) Enzymic cleavage of aromatic rings: Mechanistic aspects of the catechol dioxygenases and later enzymes of bacterial oxidative cleavage pathways. Nat Prod Rep 15:513-530.
17. Groce SL, Miller-Rodeberg MA, Lipscomb JD (2004) Single-turnover kinetics of homoprotocatechuate 2,3-dioxygenase. Biochemistry 43:15141-15153.
18. Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41:241-267.
19. Groce SL, Lipscomb JD (2005) Aromatic ring cleavage by homoprotocatechuate 2,3-dioxygenase: Role of His200 in the kinetics of interconversion of reaction cycle intermediates. Biochemistry 44:7175-7188.
20. Lipscomb JD (2008) Mechanism of extradiol aromatic ring-cleaving dioxygenases. Curr Opin Struct Biol 18:644-649.
21. Siegbahn PEM, Haeffner F (2004) Mechanism for catechol ring-cleavage by nonheme iron extradiol dioxygenases. J Am Chem Soc 126:8919-8932.
22. Emerson JP, et al. (2008) Swapping metals in Fe- and Mn-dependent dioxygenases: Evidence for oxygen activation without a change in metal redox state. Proc Natl Acad Sci USA 105:7347-7352.
23. Gunderson WA, et al. (2008) Electron paramagnetic resonance detection of intermediates in the enzymatic cycle of an extradiol dioxygenase. J Am Chem Soc 130:14465-14467.
24. 2+ environment. J Biol Chem 258:14981-14991.
25. Münck E (2000) Physical Methods in Bioinorganic Chemistry, ed L Que, Jr (University Science Books, Sausalito, CA), pp 287-319.
26. VettingMW, et al. (2004) Crystallographic comparison of manganese- and iron-dependent homoprotocatechuate 2,3-dioxygenases. J Bacteriol 186:1945-1958.
27. Whittaker JW, Lipscomb JD, Kent TA, Münck E (1984) Brevibacterium fuscum protocatechuate 3,4-dioxygenase. Purification, crystallization, and characterization. J Biol Chem 259:4466-4475.
28. Zhou J, et al. (1998) Substrate binding to the alpha-ketoglutarate- dependent nonheme iron enzyme clavaminate synthase 2: Coupling mechanism of oxidative decarboxylation and hydroxylation. J Am Chem Soc 120:13539-13540. (Pubitemid 29025230)
29. 2 activation by the oxygenase component of naphthalene 1,2-dioxygenase. J Biol Chem 276:1945-1953.
30. Price JC, et al. (2005) Kinetic dissection of the catalytic mechanism of taurine:alphaketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 44:8138-8147.
31. 2 activation pathways of nonheme iron oxygenases. Acc Chem Res 40:475-483.
32. Bollinger JM, Krebs C (2006) Stalking intermediates in oxygen activation by iron enzymes: Motivation and method. J Inorg Biochem 100:586-605.
33. Che M, Tench AJ, Naccache C (1974) Electron spin resonance studies of isotopically labeled oxygen species adsorbed on supported molybdenum. J Chem Soc Farad T 1 70:263-272.
34. 2- adsorbed on the MgO surface. J Chem Phys 116:4266-4274.
35. Dickinson LC, Chien JCW (1980) Electron paramagnetic resonance crystallography of oxygen-17-enriched oxycobaltomyoglobin: Stereoelectronic structure of the cobalt dioxygen system. Proc Natl Acad Sci USA 77:1235-1239.
36. Shaik S, et al. (2010) P450 enzymes: Their structure, reactivity, and selectivities modeled by QM/MM calculations. Chem Rev 110:949-1017.
37. Jousserandot A, et al. (1998) Microsomal cytochrome P450 dependent oxidation of N-hydroxyguanidines, amidoximes, and ketoximes: Mechanism of the oxidative cleavage of their C:N(OH) bond with formation of nitrogen oxides. Biochemistry 37:17179-17191. (Pubitemid 29013775)
38. 8 complexes of isopenicillin N synthase: Substrate determination of oxidase versus oxygenase activity in nonheme Fe enzymes. J Am Chem Soc 129:7427-7438.
39. Pierpont CG, Lange CW (1994) The chemistry of transition metal complexes containing catechol and semiquinone ligands. Progress in Inorganic Chemistry, ed KD Karlin (Wiley, New York), 41, pp 331-442.
40. Pierpont CG, Buchanan RM (1981) Transition metal complexes of o-benzoquinone, o-semiquinone, and catecholate ligands. Coord Chem Rev 38:45-87.
41. Kessel SL, Emberson RM, Debrunner PG, Hendrickson DN (1980) Iron(III), manganese (III), and cobalt(III) complexes with single chelating o-semiquinone ligands. Inorg Chem 19:1170-1178.
42. Hegg EL, Que L (1997) The 2-His-1-carboxylate facial triad: An emerging structural motif in mononuclear nonheme iron(II) enzymes. Eur J Biochem 250:625-629.
43. Wang YZ, Lipscomb JD (1997) Cloning, overexpression, and mutagenesis of the gene for homoprotocatechuate 2,3-dioxygenase from Brevibacterium fuscum. Protein Expres Purif 10:1-9.
44. Miller MA, Lipscomb JD (1996) Homoprotocatechuate 2,3-dioxygenase from Brevibacterium fuscum - A dioxygenase with catalase activity. J Biol Chem 271:5524-5535.