Oxy intermediates of homoprotocatechuate 2,3-dioxygenase: Facile electron transfer between substrates

Biochemistry

Volumn 50, Issue 47, 2011, Pages 10262-10274

  Mbughuni, Michael M ^a   Chakrabarti, Mrinmoy ^c   Hayden, Joshua A ^c   Meier, Katlyn K ^c   Dalluge, Joseph J ^b   Hendrich, Michael P ^c   Münck, Eckard ^c   Lipscomb, John D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFERRO-MAGNETICALLY COUPLED; AROMATIC RINGS; COORDINATION SITES; ELECTRON TRANSFER; INTERMEDIATE SUPPORT; MOSSBAUER; PARALLEL MODE; PEROXO LIGANDS; SEMIQUINONES; SSBAUER SPECTROSCOPIES;

AROMATIC COMPOUNDS; CHROMOPHORES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRONS; ENZYMES; FREE RADICAL REACTIONS; PARAMAGNETIC RESONANCE; PARAMAGNETISM; SUBSTRATES;

REACTION INTERMEDIATES;

HOMOPROTOCATECHUATE 2, 3 DIOXYGENASE; IRON; OXYGEN; SEMIQUINONE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL REACTION; CHROMATOPHORE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; MOSSBAUER SPECTROSCOPY; PRIORITY JOURNAL; SPECTROSCOPY;

BACTERIAL PROTEINS; BINDING SITES; BREVIBACTERIUM FLAVUM; DIOXYGENASES; ELECTRON TRANSPORT; FERROUS COMPOUNDS; KINETICS; MODELS, MOLECULAR; OXYGEN; PROTEIN BINDING;

EID: 81855199906     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201436n     Document Type: Article

References (41)

1. Lipscomb, J. D. and Orville, A. M. (1992) Mechanistic aspects of dihydroxybenzoate dioxygenases Metal Ions Biol. Syst. 28, 243-298
2. 2+ environment J. Biol. Chem. 258, 14981-14991
3. Boldt, Y. R., Sadowsky, M. J., Ellis, L. B. M., Que, L., and Wackett, L. P. (1995) A manganese-dependent dioxygenase From Arthrobacter globiformis CM-2 belongs to the major extradiol dioxygenase family J. Bacteriol. 177, 1225-1232
4. Vaillancourt, F. H., Bolin, J. T., and Eltis, L. D. (2006) The ins and outs of ring-cleaving dioxygenases Crit. Rev. Biochem. Mol. Biol. 41, 241-267
5. 2 activation pathways of non-heme iron oxygenases Acc. Chem. Res. 40, 475-483
6. Dagley, S. (1978) Microbial catabolism, the carbon cycle and environmental pollution Naturwissenschaften 65, 85-95 (Pubitemid 8270376)
7. Bugg, T. D. H. and Winfield, C. J. (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 (Pubitemid 28514544)
8. Hegg, E. L. and Que, L. (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)
9. 2+ of extradiol dioxygenases J. Biol. Chem. 260, 14035-14044 (Pubitemid 16194608)
10. 2+ of extradiol dioxygenases J. Biol. Chem. 261, 2170-2178 (Pubitemid 17205144)
11. Kovaleva, E. G. and Lipscomb, J. D. (2008) Versatility of biological non-heme Fe(II) centers in oxygen activation reactions Nat. Chem. Biol. 4, 186-193 (Pubitemid 351265327)
12. 2+ dioxygenase superoxo, alkylperoxo, and bound product intermediates Science 316, 453-457 (Pubitemid 46651494)
13. Shu, L., Chiou, Y. M., Orville, A. M., Miller, M. A., Lipscomb, J. D., and Que, L., Jr. (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
14. Spence, E. L., Langley, G. J., and Bugg, T. D. H. (1996) Cis-trans isomerization of a cyclopropyl radical trap catalyzed by extradiol catechol dioxygenases: Evidence for a semiquinone intermediate J. Am. Chem. Soc. 118, 8336-8343 (Pubitemid 26305255)
15. Emerson, J. P., Kovaleva, E. G., Farquhar, E. R., Lipscomb, J. D., and Que, L., Jr. (2008) Swapping metals in Fe- and Mn-dependent dioxygenases: Evidence for oxygen activation without a change in metal redox state Proc. Natl. Acad. Sci. U.S.A. 105, 7347-7352 (Pubitemid 351830021)
16. Fielding, A. J., Kovaleva, E. G., Farquhar, E. R., Lipscomb, J. D., and Que, L., Jr. (2011) A hyperactive cobalt-substituted extradiol-cleaving catechol dioxygenase J. Biol. Inorg. Chem. 16, 341-355
17. Gunderson, W. A., Zatsman, A. I., Emerson, J. P., Farquhar, E. R., Que, L., Lipscomb, J. D., and Hendrich, M. P. (2008) Electron paramagnetic resonance detection of intermediates in the enzymatic cycle of an extradiol dioxygenase J. Am. Chem. Soc. 130, 14465-14467
18. Groce, S. L. and Lipscomb, J. D. (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 (Pubitemid 40656662)
19. III-superoxo intermediate from a nonheme mononuclear iron-containing enzyme Proc. Natl. Acad. Sci. U.S.A. 107, 16788-16793
20. Groce, S. L., Miller-Rodeberg, M. A., and Lipscomb, J. D. (2004) Single-turnover kinetics of homoprotocatechuate 2,3-dioxygenase Biochemistry 43, 15141-15153 (Pubitemid 39602175)
21. Jollie, D. R. and Lipscomb, J. D. (1990) Formate dehydrogenase from Methylosinus trichosporium OB3b Methods Enzymol. 188, 331-334 (Pubitemid 20384917)
22. Miller, M. A. and Lipscomb, J. D. (1996) Homoprotocatechuate 2,3-dioxygenase from Brevibacterium fuscum: A dioxygenase with catalase activity J. Biol. Chem. 271, 5524-5535
23. 57Fe Mössbauer spectroscopy. In Physical Methods in Bioinorganic Chemistry (Que, L., Jr., Ed.) pp 287-319, University Science Books, Sausalito, CA.
24. Sucharitakul, J., Chaiyen, P., Entsch, B., and Ballou, D. P. (2005) The reductase of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii requires p-hydroxyphenylacetate for effective catalysis Biochemistry 44, 10434-10442 (Pubitemid 41076839)
25. Whittaker, J. W., Lipscomb, J. D., Kent, T. A., and Münck, E. (1984) Brevibacterium fuscum protocatechuate 3,4-dioxygenase. Purification, crystallization, and characterization J. Biol. Chem. 259, 4466-4475 (Pubitemid 14126899)
26. Wolgel, S. A., Dege, J. E., Perkins-Olson, P. E., Jaurez-Garcia, C. H., Crawford, R. L., Münck, E., and Lipscomb, J. D. (1993) Purification and characterization of protocatechuate 2,3-dioxygenase from Bacillus macerans: A new extradiol catecholic dioxygenase J. Bacteriol. 175, 4414-4426 (Pubitemid 23206943)
27. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L., Jr. (2004) Dioxygen activation at mononuclear nonheme iron active sites: Enzymes, models, and intermediates Chem. Rev. 104, 939-986
28. Cox, D. D., Benkovic, S. J., Bloom, L. M., Bradley, F. C., Nelson, M. J., Que, L., Jr., and Wallick, D. E. (1988) Catecholate LMCT bands as probes for the active sites of nonheme iron oxygenases J. Am. Chem. Soc. 110, 2026-2032 (Pubitemid 18095725)
29. Anitha, N. and Palaniandavar, M. (2011) Mononuclear iron(III) complexes of 3N ligands in organized assemblies: Spectral and redox properties and attainment of regioselective extradiol dioxygenase activity J. Chem. Soc., Dalton Trans. 40, 1888-1901
30. Stallings, M. D., Morrison, M. M., and Sawyer, D. T. (1981) Redox chemistry of metal-catechol complexes in aprotic media. 1. Electrochemistry of substituted catechols and their oxidation products Inorg. Chem. 20, 2655-2660
31. Chedekel, M. R., Land, E. J., Thompson, A., and Truscott, T. G. (1984) Early steps in the free radical polymerization of 3,4-dihydroxyphenylalanine (dopa) into melanin J. Chem. Soc., Chem. Commun., 1170-1172
32. z (m = 1, 2; z = -1, 0, +1) complexes Inorg. Chem. 31, 1687-1695
33. Mialane, P., Anxolabeheremallart, E., Blondin, G., Nivorojkine, A., Guilhem, J., Tchertanova, L., Cesario, M., Ravi, N., Bominaar, E., Girerd, J. J., and Münck, E. (1997) Structure and electronic properties of (N,N′-Bis(4-Methyl-6-Tert-Butyl-2-Methyl-Phenolate)-N,N′-bismethyl- 1,2-di aminoethane)Fe-III (DBSQ): Spectroelectrochemical study of the red-ox properties. Relevance to intradiol catechol dioxygenases Inorg. Chim. Acta 263, 367-378 (Pubitemid 127346140)
34. Kessel, S. L., Emberson, R. M., Debrunner, P. G., and Hendrickson, D. N. (1980) Iron(III), manganese(III), and cobalt(III) complexes with single chelating o-semiquinone ligands Inorg. Chem. 19, 1170-1178
35. Lynch, M. W., Valentine, M., and Hendrickson, D. N. (1982) Mixed-valence semi-quinone catecholate iron complexes J. Am. Chem. Soc. 104, 6982-6989
36. Siegbahn, P. E. M. and Haeffner, F. (2004) Mechanism for catechol ring-cleavage by non-heme iron extradiol dioxygenases J. Am. Chem. Soc. 126, 8919-8932 (Pubitemid 38971065)
37. Deeth, R. J. and Bugg, T. D. H. (2003) A density functional investigation of the extradiol cleavage mechanism in non-heme iron catechol dioxygenases J. Biol. Inorg. Chem. 8, 409-418 (Pubitemid 36578192)
38. Girerd, J.-J., Banse, F., and Simaan, A. J. (2000) Characterization and properties of non-heme iron peroxo complexes Struct. Bonding (Berlin, Ger.) 97, 145-177
39. Roelfes, G., Vrajmasu, V., Chen, K., Ho, R. Y., Rohde, J.-U., Zondervan, C., La Crois, R. M., Schudde, E. P., Lutz, M., Spek, A. L., Hage, R., Feringa, B. L., Münck, E., and Que, L., Jr. (2003) End-on and side-on peroxo derivatives of non-heme iron complexes with pentadentate ligands: models for putative intermediates in biological iron/dioxygen chemistry Inorg. Chem. 42, 2639-2653
40. Karlsson, A., Parales, J. V., Parales, R. E., Gibson, D. T., Eklund, H., and Ramaswamy, S. (2003) Crystal structure of naphthalene dioxygenase: Side-on binding of dioxygen to iron Science 299, 1039-1042 (Pubitemid 36222924)
41. Neibergall, M. B., Stubna, A., Mekmouche, Y., Münck, E., and Lipscomb, J. D. (2007) Hydrogen peroxide dependent cis-dihydroxylation of benzoate by fully oxidized benzoate 1,2-dioxygenase Biochemistry 46, 8004-8016 (Pubitemid 47051636)