Kinetic and spectroscopic studies on the quercetin 2,3-dioxygenase from Bacillus subtilis

Biochemistry

Volumn 45, Issue 3, 2006, Pages 1009-1016

  Schaab, Matthew R ^a   Barney, Brett M ^a,b   Francisco, Wilson A ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CATALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; MANGANESE; OXYGEN; SPECTROSCOPIC ANALYSIS; STOICHIOMETRY;

ASPERGILLUS QUERCETINASES; BACILLUS SUBTILIS; DIVALENT METALS; FLAVONOL QUERCETIN; OCTAHEDRAL COORDINATION; PROKARYOTIC ORGANISM; PROTOCATECHUOYLPHLOROGLUCINOLCARBOXYLIC ACID; QUERCETIN 2,3-DIOXYGENASE;

ENZYME KINETICS;

2 PROTOCATECHUOYLPHLOROGLUCINOLCARBOXYLIC ACID; CADMIUM; CARBON MONOXIDE; CARBOXYLIC ACID DERIVATIVE; CATECHOL DIOXYGENASE; COBALT; COPPER ION; DIOXYGENASE; FERROUS ION; FLAVONOL; MANGANESE; MANGANESE DIOXYGENASE; METAL; PROTOCATECHUIC ACID; QUERCETIN; QUERCETIN 2,3 DIOXYGENASE; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; ASPERGILLUS; ASPERGILLUS JAPONICUS; BACILLUS SUBTILIS; BACTERIAL GROWTH; CULTURE MEDIUM; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME MECHANISM; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF; STEADY STATE; STOICHIOMETRY;

BACILLUS SUBTILIS; DIOXYGENASES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR STRUCTURE; RECOMBINANT PROTEINS;

ASPERGILLUS; ASPERGILLUS JAPONICUS; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

EID: 31044441352     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051571c     Document Type: Article

References (47)

1. Pietta, P., Gardana, C., and Pietta, A. (2003) Flavonoids in Herbs, in Flavonoids in Health and Disease (Rice-Evans, C. A., and Packer, L., Eds.) 2nd ed., pp 43-69, Marcel Dekker, New York.
2. Medina, M. L., Kiernan, U. A., and Francisco, W. A. (2004) Proteomic analysis of rutin-induced secreted proteins from Aspergillus flavus, Fungal Genet. Biol. 41, 327-335.
3. Omori, T., Shiozawa, K., Sekiya, M., and Minoda, Y. (1986) Formation of 2,4,6-trihydroxycarboxylic acid and 2-protocatechuoylphloroglucinolcarboxylic acid from rutin by bacteria, Agric. Biol. Chem. 50, 779-780.
4. Oka, T., and Simpson, F. J. (1971) Quercetinase, a dioxygenase containing copper, Biochem. Biophys. Res. Commun. 43, 1-5.
5. Hund, H. K., Breuer, J., Lingens, F., Huttermann, J., Kappl, R., and Fetzner, S. (1999) Flavonol 2,4-dioxygenase from Aspergillus niger DSM 821, a type 2 Cu-II-containing glycoprotein, Eur. J. Biochem. 263, 871-878.
6. Fusetti, F., Schroter, K. H., Steiner, R. A., van Noort, P. I., Pijning, T., Rozeboom, H. J., Kalk, K. H., Egmond, M. R., and Dijkstra, B. W. (2002) Crystal structure of the copper-containing quercetin 2,3-dioxygenase from Aspergillus japonicus, Structure 10, 259-268.
7. Bowater, L., Fairhurst, S. A., Just, V. J., and Bornemann, S. (2004) Bacillus subtilis YxaG is a novel Fe-containing quercetin 2,3-dioxygenase, FEBS Lett. 557, 45-48.
8. Barney, B. M., Schaab, M. R., LoBrutto, R., and Francisco, W. A. (2004) Evidence for a new metal in a known active site: purification and characterization of an iron-containing quercetin 2,3-dioxygenase from Bacillus subtilis, Protein Expression Purif. 35, 131-141.
9. Gopal, B., Madan, L. L., Betz, S. F., and Kossiakoff, A. A. (2005) The crystal structure of a quercetin 2,3-dioxygenase from Bacillus subtilis suggests modulation of enzyme activity by a change in the metal ion at the active site(s), Biochemistry 44, 193-201.
10. Dunwell, J. M. (1998) Cupins: A new superfamily of functionally diverse proteins that include germins and plant storage proteins, Biotechnol. Genet. Eng. 15, 1-32.
11. Khuri, S., Bakker, F. T., and Dunwell, J. M. (2001) Phylogeny, function, and evolution of the cupins, a structurally conserved, functionally diverse superfamily of proteins, Mol. Biol. Evol. 18, 593-605.
12. Dunwell, J. M., Purvis, A., and Khuri, S. (2004) Cupins: the most functionally diverse protein superfamily?, Phytochemistry 65, 7-17.
13. Oka, T., Simpson, F. J., and Krishnam, Hg. (1972) Degradation of rutin by Aspergillus flavus-studies on specificity, inhibition, and possible reaction-mechanism of quercetinase, Can. J. Microbiol. 18, 493-508.
14. Cleland, W. W. (1979) Statistical analysis of enzyme kinetic data, Methods Enzymol. 63, 103-138.
15. Kooter, I. M., Steiner, R. A., Dijkstra, B. W., van Noort, P. I., Egmond, M. R., and Huber, M. (2002) EPR characterization of the mononuclear Cu-containing Aspergillus japonicus quercetin 2,3-dioxygenase reveals dramatic changes upon anaerobic binding of substrates, Eur. J. Biochem. 269, 2971-2979.
16. Segel, I. H. (1993) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, John Wiley & Sons, New York.
17. Tanner, A., Bowater, L., Fairhurst, S. A., and Bornemann, S. (2001) Oxalate decarboxylase requires manganese and dioxygen for activity, J. Biol. Chem. 276, 43627-43634.
18. Dai, Y., Pochapsky, T. C., and Abeles, R. H. (2001) Mechanistic studies of two dioxygenases in the methionine salvage pathway of Klebsiella pneumoniae, Biochemistry 40, 6379-6387.
19. Reddy, P. C., Prasad, K. S. S., and Rangamannar, B. (1999) Substoichiometric extraction and quantification of cobalt with potassium salts of ethyl, propyl, butyl, pentyl and benzyl xanthates, J. Radioanal. Nucl. Chem. 241, 671-674.
20. Whiting, A. K., Boldt, Y. R., Hendrich, M. P., Wackett, L. P., and Que, L. (1996) Manganese(II)-dependent extradiol-cleaving catechol dioxygenase from Archrobacter globiformis CM-2, Biochemistry 35, 160-170.
21. Bornemann, S., Bowater, L., and Tanner, A. (2001) Bacillus subtilis oxalate decarboxylase: structural conservation and functional diversity in the cupin superfamily, J. Inorg. Biochem. 86, 153-153.
22. Nordstrom, C. G. (1968) Autoxidation of quercetin in aqueous solution. Elucidation of the autoxidation reaction, Suom. Kemistil. B 41, 351-353.
23. Jovanovic, S. V., Steenken, S., Tosic, M., Marjanovic, B., and Simic, M. G. (1994) Flavonoids as antioxidants, J. Am. Chem. Soc. 116, 4846-4851.
24. Lemanska, K., Szymusiak, H., Tyrakowska, B., Zielinski, R., Soffers, A., and Rietjens, I. (2001) The influence of pH on antioxidant properties and the mechanism of antioxidant action of hydroxyflavones, Free Radical Biol. Med. 31, 869-881.
25. Reed, G. H., and Markham, G. D. (1984) EPR on Mn(II) Complexes with Enzymes and Other Proteins, in Biological Magnetic Resonance (Berliner, L. J., and Reuben, J., Eds.) Vol. 6, pp 73-142, Plenum Press, New York.
26. 12: Impact of structural distortions on Mn(II) in weak ligand fields, Inorg. Chem. 43, 506-514.
27. Valegard, K., van Scheltinga, A. C. T., Lloyd, M. D., Hara, T., Ramaswamy, S., Perrakis, A., Thompson, A., Lee, H. J., Baldwin, J. E., Schofield, C. J., Hajdu, J., and Andersson, I. (1998) Structure of a cephalosporin synthase, Nature 394, 805-809.
28. Roach, P. L., Clifton, I. J., Hensgens, C. M. H., Shibata, N., Schofield, C. J., Hajdu, J., and Baldwin, J. E. (1997) Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation, Nature 387, 827-830.
29. Titus, G. P., Mueller, H. A., Burgner, J., de Cordoba, S. R., Penalva, M. A., and Timm, D. E. (2000) Crystal structure of human homogentisate dioxygenase, Nat. Struct. Biol. 7, 542-546.
30. Clifton, I. J., Hsueh, L. C., Baldwin, J. E., Harlos, K., and Schofield, C. J. (2001) Structure of proline 3-hydroxylase-Evolution of the family of 2-oxoglutarate dependent oxygenases, Eur. J. Biochem. 268, 6625-6636.
31. Wilmouth, R. C., Turnbull, J. J., Welford, R. W. D., Clifton, I. J., Prescott, A. G., and Schofield, C. J. (2002) Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana, Structure 10, 93-103.
32. Chance, M. R., Bresnick, A. R., Burley, S. K., Jiang, J. S., Lima, C. D., Sali, A., Almo, S. C., Bonanno, J. B., Buglino, J. A., Boulton, S., Chen, H., Eswar, N., He, G. S., Huang, R., Ilyin, V., McMahan, L., Pieper, U., Ray, S., Vidal, M., and Wang, L. K. (2002) Structural genomics: A pipeline for providing structures for the biologist, Protein Sci. 11, 723-738.
33. O'Brien, J. R., Schuller, D. J., Yang, V. S., Dillard, B. D., and Lanzilotta, W. N. (2003) Substrate-induced conformational changes in Escherichia coli taurine/alpha-ketoglutarate dioxygenase and insight into the oligomeric structure, Biochemistry 42, 5547-5554.
34. Clifton, I. J., Doan, L. X., Sleeman, M. C., Topf, M., Suzuki, H., Wilmouth, R. C., and Schofield, C. J. (2003) Crystal structure of carbapenem synthase (CarC), J. Biol. Chem. 278, 20843-20850.
35. Pang, H., Bartlam, M., Zeng, Q. H., Miyatake, H., Hisano, T., Miki, K., Wong, L. L., Gao, G. F., and Rao, Z. H. (2004) Crystal structure of human pirin-An iron-binding nuclear protein and transcription cofactor, J. Biol. Chem. 279, 1491-1498.
36. Anand, R., Dorrestein, P. C., Kinsland, C., Begley, T. P., and Ealick, S. E. (2002) Structure of oxalate decarboxylase from Bacillus subtilis at 1.75 angstrom resolution, Biochemistry 41, 7659-7669.
37. Pochapsky, T. C., Pochapsky, S. S., Ju, T. T., Mo, H. P., Al-Mjeni, F., and Maroney, M. J. (2002) Modeling and experiment yields the structure of acireductone dioxygenase from Klebsiella pneumoniae, Nat. Struct. Biol. 9, 966-972.
38. Hoffman, B. J., Broadwater, J. A., Johnson, P., Harper, J., Fox, B. G., and Kenealy, W. R. (1995) Lactose fed-batch overexpression of recombinant metalloproteins in Escherichia coli BL21-(DE3)-process-control yielding high levels of metal incorporated, soluble protein, Protein Expression Purif. 6, 646-654.
39. Gabbianelli, R., Battistoni, A., Polizio, F., Carri, M. T., Demartino, A., Meier, B., Desideri, A., and Rotilio, G. (1995) Metal uptake of recombinant cambialistic superoxide dismutase from Propionibacterium shemanii affected by growth conditions of host Escherichia coli cells, Biochem. Biophys. Res. Commun. 216, 841-847.
40. Dai, Y., Wensink, P. C., and Abeles, R. H. (1999) One protein, two enzymes, J. Biol. Chem. 274, 1193-1195.
41. Steiner, R. A., Kalk, K. H., and Dijkstra, B. W. (2002) Anaerobic enzyme-substrate structures provide insight into the reaction mechanism of the copper-dependent quercetin 2,3-dioxygenase, Proc. Natl. Acad. Sci. U.S.A. 99, 16625-16630.
42. Bugg, T. D. H., and Lin, G. (2001) Solving the riddle of the intradiol and extradiol catechol dioxygenases: how do enzymes control hydroperoxide rearrangements?, Chem. Commun., 941-952.
43. Reinhardt, L. A., Svedruzic, D., Chang, C. H., Cleland, W. W., and Richards, N. G. J. (2003) Heavy atom isotope effects on the reaction catalyzed by the oxalate decarboxylase from Bacillus subtilis, J. Am. Chem. Soc. 125, 1244-1252.
44. Mendel, S., Arndt, A., and Bugg, T. D. H. (2004) Acid-base catalysis in the extradiol catechol dioxygenase reaction mechanism: site-directed mutagenesis of his-115 and his-179 in Escherichia coli 2,3-dihydroxyphenylpropionate 1,2-dioxygenase (MhpB), Biochemistry 43, 13390-13396.
45. Just, V. J., Stevenson, C. E. M., Bowater, L., Tanner, A., Lawson, D. M., and Bornemann, S. (2004) A closed conformation of Bacillus subtilis oxalate decarboxylase OxdC provides evidence for the true identity of the active site, J. Biol. Chem. 279, 19867-19874.
46. Svedruzic, D., Jonsson, S., Toyota, C. G., Reinhardt, L. A., Ricagno, S., Linqvist, Y., and Richards, N. G. J. (2005) The enzymes of oxalate metabolism: unexpected structures and mechanisms, Arch. Biochem. Biophys. 433, 176-192.
47. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L. (2004) Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates, Chem. Rev. 104, 939-986.