Chemistry of the catalytic conversion of phthalate into its cis-dihydrodiol during the reaction of oxygen with the reduced form of phthalate dioxygenase

Biochemistry

Volumn 44, Issue 16, 2005, Pages 6197-6207

  Tarasev, Michael ^a   Ballou, David P ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; DATA ACQUISITION; ELECTRONS; MONOMERS; OXIDATION;

CATALYTIC CONVERSION; ELECTRON DISTRIBUTION; PHTHALATE;

OXYGEN;

FERREDOXIN; IRON; IRON SULFUR PROTEIN; OXYGEN; PHTHALIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; CATALYSIS; ELECTRON; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; HYDROXYLATION; OXIDATION; PRIORITY JOURNAL; STEADY STATE;

BURKHOLDERIA CEPACIA; CATALYTIC DOMAIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; IRON; KINETICS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; OXYGENASES; PHTHALIC ACIDS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS;

EID: 17644402801     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047724y     Document Type: Article

References (39)

1. Gassner, G. T., and Ballou, D. P. (1996) in Flavins and Flavoproteins (Stevenson, K., Massey, V., and Williams, C. H. J., Eds.) pp 909-912, University of Calgary Press, Calgary, Canada.
2. Gassner, G., Wang, L., Batie, C., and Ballou, D. P. (1994) Reaction of phthalate dioxygenase reductase with NADH and NAD: Kinetic and spectral characterization of intermediates, Biochemistry 33, 12184-12193.
3. Tarasev, M., Rhames, F., and Ballou, D. P. (2004) Rates of the phthalate dioxygenase reaction with oxygen are dramatically increased by interactions with phthalate and phthalate oxygenase reductase, Biochemistry 43, 12799-12808.
4. Gibson, D. T., and Parales, R. E. (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. (review), Curr. Opin. Biotechnol. 11, 236-243.
5. Batie, C. J., Ballou, D. P., and Correll, C. C. (1992) in Chemistry and Biochemistry of Flavoenzymes (Müller, F., Ed.) pp 543-556, CRC Press, Boca Raton, FL.
6. Batie, C. J., LaHaie, E., and Ballou, D. P. (1987) Purification and characterization of phthalate oxygenase and phthalate oxygenase reductase from Pseudomonas cepacia, J. Biol. Chem. 262, 1510-1518.
7. Coulter, E. D., Moon, N., Batie, C. J., Dunham, W. R., and Ballou, D. P. (1999) Electron paramagnetic resonance measurements of the ferrous mononuclear site of phthalate dioxygenase substituted with alternate divalent metal ions: Direct evidence for ligation of two histidines in the copper(II)-reconstituted protein, Biochemistry 38, 11062-11072.
8. 2 activation by the oxygenase component of naphthalene 1,2-dioxygenase, J. Biol. Chem. 276, 1945-1953.
9. Wolfe, M. D., Altier, D. J., Stubna, A., Popescu, C. V., Munck, E., and Lipscomb, J. D. (2002) Benzoate 1,2-dioxygenase from Pseudomonas putida: Single turnover kinetics and regulation of a two-component Rieske dioxygenase, Biochemistry 41, 9611-9626.
10. Batie, C. J., and Ballou, D. P. (1990) Phthalate dioxygenase, Methods Enzymol. 188, 61-70.
11. Davis, M. D., Kaufman, S., and Milstien, S. (1986) A modified ferrozine method for the measurement of enzyme-bound iron, J. Biochem. Biophys. Methods 13, 39-45.
12. Massey, V., and Hemmerich, P. (1977) A photochemical procedure for reduction of oxidation-reduction proteins employing deazariboflavin as catalyst, J. Biol. Chem. 252, 5612-5614.
13. Kauppi, B., Lee, K., Carredano, E., Parales, R. E., Gibson, D. T., Eklund, H., and Ramaswamy, S. (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase, Structure 6, 571-586.
14. Parales, R. E., Parales, J. V., and Gibson, D. T. (1999) Aspartate 205 in the catalytic domain of naphthalene dioxygenase is essential for activity, J. Bacteriol. 181, 1831-1837.
15. Beharry, Z. M., Eby, D. M., Coulter, E. D., Viswanathan, R., Neidle, E. L., Phillips, R. S., and Kurtz, D. M., Jr. (2003) Histidine ligand protonation and redox potential in the rieske dioxygenases: Role of a conserved aspartate in anthranilate 1,2-dioxygenase, Biochemistry 42, 13625-13636.
16. Jiang, H., Parales, R. E., Lynch, N. A., and Gibson, D. T. (1996) Site-directed mutagenesis of conserved amino acids in the α subunit of toluene dioxygenase: Potential mononuclear non-heme iron coordination sites, J. Bacteriol. 178, 3133-3139.
17. Furusawa, Y., Nagarajan, V., Tanokura, M., Masai, E., Fukuda, M., and Senda, T. (2004) Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1, J. Mol. Biol. 342, 1041-1052.
18. Tsang, H. T., Batie, C. J., Ballou, D. P., and Penner-Hahn, J. E. (1996) Structural characterization of the mononuclear iron site in Pseudomonas cepacia phthalate DB01 dioxygenase using X-ray absorption spectroscopy, J. Biol. Inorg. Chem. 1, 24-33.
19. Gassner, G. T., Ballou, D. P., Landrum, G. A., and Whittaker, J. W. (1993) Magnetic circular dichroism studies on the mononuclear ferrous active site of phthalate dioxygenase from Pseudomonas cepacia show a change of ligation state on substrate binding, Biochemistry 32, 4820-4825.
20. Pavel, E. G., Martins, L. J., Ellis, W. R. J., and Solomon, E. I. (1994) Magnetic circular dichroism studies of exogenous ligand and substrate binding to the non-heme ferrous active site in phthalate dioxygenase, Chem. Biol. 1, 173-183.
21. Solomon, E. I., Decker, A., and Lehnert, N. (2003) Non-heme iron enzymes: Contrasts to heme catalysis, Proc. Natl. Acad. Sci. U.S.A. 100, 3589-3594.
22. Bertini, I., Luchinat, C., Mincione, G., Parigi, G., Gassner, G. T., and Ballou, D. P. (1996) NMRD studies on phthalate dioxygenase: Evidence for displacement of water on binding substrate, J. Biol. Inorg. Chem. 1, 468-475.
23. Bernhardt, F. H., and Kuthan, H. (1981) Dioxygen activation by putidamonooxin. The oxygen species formed and released under uncoupling conditions, Eur. J. Biochem. 120, 547-555.
24. Wende, P., Bernhardt, F. H., and Pfleger, K. (1989) Substrate-modulated reactions of putidamonooxin. The nature of the active oxygen species formed and its reaction mechanism, Eur. J. Biochem. 181, 189-197.
25. Carredano, E., Karlsson, A., Kauppi, B., Choudhury, D., Parales, R. E., Parales, J. V., Lee, K., Gibson, D. T., Eklund, H., and Ramaswamy, S. (2000) Substrate binding site of naphthalene 1,2-dioxygenase: Functional implications of indole binding, J. Mol. Biol. 296, 701-712.
26. Ballou, D., and Batie, C. (1988) Phthalate oxygenase, a Rieske iron-sulfur protein from Pseudomonas cepacia, Prog. Clin. Biol. Res. 274, 211-226.
27. 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.
28. Price, J. C., Barr, E. W., Tirupati, B., Bollinger, J. M., Jr., and Krebs, C. (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an a-ketoglutarate-dependent dioxygenase: A high-spin FeIV complex in taurine/α-ketoglutarate dioxygenase (TauD) from Escherichia coli. [erratum appears in Biochemistry (2004) 43, 1134], Biochemistry 42, 7497-7508.
29. III-alkylperoxo complexes: Homolytic cleavage of the O-O bond, J. Am. Chem. Soc. 123, 8271-8290.
30. Ho, R. Y. N., Roelfes, G., Feringa, B. L., and Que, L. (1999) Raman evidence for a weakened O-O bond in mononuclear low-spin iron(III)- hydroperoxides, 121, 264-265.
31. Chen, K., and Que, L. J. (1999) Evidence for the participation of high-valent iron-oxo species in stereospecific alkane hydroxylation by a non-heme iron catalyst, J. Chem. Soc., Chem. Comm. 1375-1376.
32. V=O active species, J. Am. Chem. Soc. 123, 6327-6337.
33. III-OOH coin, J. Am. Chem. Soc. 124, 3026-3035.
34. Nelson, M. J., Chase, D. B., and Seitz, S. P. (1995) Photolysis of "purple" lipoxygenase: Implications for the structure of the chromophore, Biochemistry 34, 6159-6163.
35. Westre, T. E., Loeb, K. E., Zaleski, J. M., Hedman, B., Hodgson, K. O., and Solomon, E. I. (1995) Determination of the geometric and electronic structure of activated bleomycin using X-ray absorption spectroscopy, 117, 1309-1313.
36. Neese, F., Zaleski, J. M., Zaleski, K. L., and Solomon, E. I. (2000) Electronic structure of activated bleomycin: Oxygen intermediates in heme versus non-heme iron, 122, 11703-11724.
37. Groves, J. T., and Han, Y.-Z. (1995) in Cytochrome P450: Structure, Mechanism, and Biochemistry (Ortiz de Montellano, P. R., Ed.) pp 3-48, Plenum Press, New York.
38. Bassan, A., Blomberg, M. R., and Siegbahn, P. E. (2004) A theoretical study of the cis-dihydroxylation mechanism in naphthalene 1,2-dioxygenase, J. Biol. Inorg. Chem. 9, 439-452.
39. Lehnert, N., Ho, R. Y., Que, L., Jr., and Solomon, E. I. (2001) Electronic structure of high-spin iron(III)-alkylperoxo complexes and its relation to low-spin analogues: Reaction coordinate of O-O bond homolysis, J. Am. Chem. Soc. 123, 12802-12816.