Substrate specificity of Sphingobium chlorophenolicum 2,6- dichlorohydroquinone 1,2-dioxygenase

Biochemistry

Volumn 50, Issue 41, 2011, Pages 8899-8913

  MacHonkin, Timothy E ^a   Doerner, Amy E ^a  

^a WHITMAN COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIOXYGENASES; ENZYME INACTIVATION; EXTRADIOL; HYDROXYL GROUPS; OXIDATIVE CLEAVAGES; POTENT INHIBITOR; REGIOSPECIFICITY; RING CLEAVAGE; SPHINGOBIUM CHLOROPHENOLICUM; SPHINGOBIUM CHLOROPHENOLICUM ATCC 39723; STEADY-STATE KINETICS; SUBSTRATE BINDS; SUBSTRATE SPECIFICITY;

ENZYMES; KETONES; PHENOLS;

SUBSTRATES;

2,6 DICHLOROHYDROQUINONE 1,2 DIOXYGENASE; BACTERIAL ENZYME; FENCLONINE; HYDROQUINONE DERIVATIVE; IRON; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; BINDING AFFINITY; CATABOLISM; ENZYME BINDING; ENZYME INACTIVATION; ENZYME KINETICS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SPHINGOBIUM CHLOROPHENOLICUM;

ALPHAPROTEOBACTERIA; CATALYSIS; CHEMISTRY; DIOXYGENASES; HALOGENS; HYDROQUINONES; KINETICS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; OXYGEN; PHENOLS; SUBSTRATE SPECIFICITY;

SPHINGOBIUM CHLOROPHENOLICUM;

EID: 80054757502     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200855m     Document Type: Article

References (76)

1. Furukawa, K. (2000) Engineering dioxygenases for efficient degradation of environmental pollutants Curr. Opin. Biotechnol. 11, 244-249 (Pubitemid 30326470)
2. Pieper, D. H. and Reineke, W. (2000) Engineering bacteria for bioremediation Curr. Opin. Biotechnol. 11, 262-270 (Pubitemid 30326473)
3. Pieper, D. H. (2005) Aerobic degradation of polychlorinated biphenyls Appl. Microbiol. Biotechnol. 67, 170-191 (Pubitemid 40591268)
4. Phillips, T. M., Seech, A. G., Lee, H., and Trevors, J. T. (2005) Biodegradation of hexachlorocyclohexane (HCH) by microorganisms Biodegradation 16, 363-392 (Pubitemid 40601910)
5. Stolz, A. (2009) Molecular characteristics of xenobiotic-degrading sphingomonads Appl. Microbiol. Biotechnol. 81, 793-811
6. 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 (Pubitemid 32521812)
7. Bugg, T. D. H. (2003) Dioxygenase enzymes: Catalytic mechanisms and chemical models Tetrahedron 59, 7075-7101 (Pubitemid 36993589)
8. Vaillancourt, F. H., Bolin, J. T., and Eltis, L. (2004) Ring-Cleavage Dioxygenase. In Pseudomonas (Ramos, J.-L., Ed.) pp 359-396, Kluwer Academic/Plenum, New York.
9. 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
10. Bugg, T. D. H. and Ramaswamy, S. (2008) Non-heme iron-dependent dioxygenases: Unravelling catalytic mechanisms for complex enzymatic oxidations Curr. Opin. Chem. Biol. 12, 134-140
11. 2+ dioxygenase superoxo, alkylperoxo, and bound product intermediates Science 316, 453-457 (Pubitemid 46651494)
12. Kovaleva, E. G. and Lipscomb, J. D. (2008) Intermediate in the O-O Bond Cleavage Reaction of an Extradiol Dioxygenase Biochemistry 47, 11168-11170
13. Deeth, R. J. and Bugg, T. D. H. (2003) A density functional investigation of the extradiol cleavage mechanism in non-heme iron catechol dioxygenase J. Biol. Inorg. Chem. 8, 409-418 (Pubitemid 36578192)
14. Siegbahn, P. E. M. and Haeffner, F. (2004) Mechanism for Catechol Ring-Cleavage by Non-Heme Iron Extradiol Dioxygenase J. Am. Chem. Soc. 126, 8919-8932 (Pubitemid 38971065)
15. Harpel, M. R. and Lipscomb, J. D. (1990) Gentisate 1,2-Dioxygenase from Pseudomonas. Purification, Characterization, and Comparison of the Enzymes from Pseudomonas testosteroni and Pseudomonas acidovorans J. Biol. Chem. 265, 6301-6311
16. 2+ and Mechanism of Turnover J. Biol. Chem. 265, 22187-22196
17. Hintner, J.-P., Lechner, C., Rigert, U., Kuhm, A. E., Storm, T., Reemtsma, T., and Stolz, A. (2001) Direct Ring Fission of Salicylate by a Salicylate 1,2-Dioxygenase Activity from Pseudaminobacter salicylatoxidans J. Bacteriol. 183, 6936-6942 (Pubitemid 33064208)
18. Hintner, J.-P., Remtsma, T., and Stolz, A. (2004) Biochemical and molecular characterization of a ring fission dioxygenase with the ability to oxidize (substituted) salicylate(s) from Pseudaminobacter salicylatoxidans J. Biol. Chem. 279, 37250-37260 (Pubitemid 39195431)
19. Adams, M. A., Singh, V. K., Keller, B. O., and Jia, Z. C. (2006) Structural and biochemical characterization of gentisate 1,2-dioxygenase from Escherichia coli O157: H7 Mol. Microbiol. 61, 1469-1484 (Pubitemid 44359376)
20. Chen, J., Li, W., Wang, M. Z., Zhu, G. Y., Liu, D. Q., Sun, F., Hao, N., Li, X. M., Rao, Z. H., and Zhang, X. C. (2008) Crystal structure and mutagenic analysis of GDOsp, a gentisate 1,2-dioxygenase from Silicibacter pomeroyi Protein Sci. 17, 1362-1373
21. Matera, I., Ferraroni, M., Burger, S., Scozzafava, A., Stolz, A., and Briganti, F. (2008) Salicylate 1,2-dioxygenase from Pseudaminobacter salicylatoxidans: Crystal structure of a peculiar ring-cleaving dioxygenase J. Mol. Biol. 380, 856-868
22. Titus, G. P., Mueller, H. A., Burgner, J., Rodríguez-de- Córba, S., Peñalva, M. A., and Timm, D. E. (2000) Crystal structure of human homogentisate dioxygenase Nat. Struct. Biol. 7, 542-546 (Pubitemid 30445908)
23. Veldhuizen, E. J. A., Vaillancourt, F. H., Whiting, C. J., Hsiao, M. M. Y., Gingras, G., Xiao, Y. F., Tanguay, R. M., Boukouvalas, J., and Eltis, L. D. (2005) Steady-state kinetics and inhibition of anaerobically purified human homogentisate 1,2-dioxygenase Biochem. J. 386, 305-314 (Pubitemid 40343788)
24. Malherbe, P., Kohler, C., Daprada, M., Lang, G., Kiefer, V., Schwarcz, R., Lahm, H. W., and Cesura, A. M. (1994) Molecular-Cloning and Functional Expression of Human 3-Hydroxyanthranilic-Acid Dioxygenase J. Biol. Chem. 269, 13792-13797
25. Lendenmann, U. and Spain, J. C. (1996) 2-Aminophenol 1,6-Dioxygenase: A Novel Aromatic Ring Cleavage Enzyme Purified from Pseudomonas pseudoalcaligenes JS45 J. Bacteriol. 178, 6227-6232 (Pubitemid 26365703)
26. Davis, J. K., He, Z., Somerville, C. C., and Spain, J. C. (1999) Genetic and biochemical comparison of 2-aminophenol 1,6-dixygenase of Pseudomonas pseudoalcaligenes JS45 to meta-cleavage dioxygenases: Divergent evolution of 2-aminophenol meta-cleavage pathway Arch. Microbiol. 172, 330-339 (Pubitemid 29496281)
27. Zhang, Y., Colabroy, K. L., Begley, T. P., and Ealick, S. E. (2005) Structural studies on 3-hydroxyanthranilate-3,4-dioxygenase: The catalytic mechanism of a complex oxidation involved in NAD biosynthesis Biochemistry 44, 7632-7643 (Pubitemid 40740747)
28. Ohtsubo, Y., Miyauchi, K., Kanda, K., Hatta, T., Kiyohara, H., Senda, T., Nagata, Y., Mitsui, Y., and Takagi, M. (1999) PcpA, which is involved in the degradation of pentachlorophenol in Sphingomonas chlorophenolica ATCC39723, is a novel type of ring-cleavage dioxygenase FEBS Lett. 459, 395-398 (Pubitemid 29467375)
29. Xu, L., Resing, K., Lawson, S. L., Babbitt, P. C., and Copley, S. D. (1999) Evidence That pcpA Encodes 2,6-Dichlorohydroquinone Dioxygenase, the Ring Cleavage Enzyme Required for Pentachlorophenol Degradation in Sphingomonas chlorophenolica Strain ATCC 39723 Biochemistry 38, 7659-7669
30. Xun, L., Bohuslavek, J., and Cai, M. (1999) Characterization of 2,6-Dichloro- p -hydroquinone 1,2-Dioxygenase (PcpA) of Sphingomonas chlorophenolica ATCC 39723 Biochem. Biophys. Res. Commun. 266, 322-325 (Pubitemid 30028666)
31. Miyauchi, K., Adachi, Y., Nagata, Y., and Takagi, M. (1999) Cloning and Sequencing of a Novel meta -Clevage Dioxygenase Gene Whose Product Is Involved in Degradation of γ-Hexachlorocyclohexane in Sphingomonas paucimobilis J. Bacteriol. 181, 6712-6719 (Pubitemid 29517986)
32. Moonen, M. J. H., Synowsky, S. A., van den Berg, W. A. M., Westphal, A. H., Heck, A. J. R., van den Heuvel, R. H. H., Fraaije, M. W., and van Berkel, W. J. H. (2008) Hydroquinone dioxygenase from Pseudomonas fluorescens ACB: A novel member of the family of nonheme-iron(II)-dependent dioxygenases J. Bacteriol. 190, 5199-5209
33. Shen, W. J., Liu, W. D., Zhang, J., Tao, J. A., Deng, H. H., Cao, H., and Cui, Z. L. (2010) Cloning and characterization of a gene cluster involved in the catabolism of p -nitrophenol from Pseudomonas putida DLL-E4 Bioresour. Technol. 101, 7516-7522
34. Yin, Y. and Zhou, N. Y. (2010) Characterization of MnpC, a Hydroquinone Dioxygenase Likely Involved in the meta -Nitrophenol Degradation by Cupriavidus necator JMP134 Curr. Microbiol. 61, 471-476
35. Machonkin, T. E., Holland, P. L., Smith, K. N., Liberman, J. S., Dinescu, A., Cundari, T. R., and Rocks, S. S. (2010) Determination of the Active Site of Sphingobium chlorophenolicum 2,6-dichlorohydroquinone dioxygenase (PcpA) J. Biol. Inorg. Chem. 10, 291-301
36. Bartels, I., Knackmuss, H.-J., and Reineke, W. (1984) Suicide Inactivation of Catechol 2,3-Dioxygenase from Pseudomonas putida mt-2 by 3-Halocatechols Appl. Environ. Microbiol. 47, 500-505 (Pubitemid 14155116)
37. Cerdan, P., Wasserfallen, A., Rekik, M., Timmis, K. N., and Harayama, S. (1994) Substrate Specificity of Catechol 2,3-Dioxygenase Encoded by TOL Plasmid pWW0 of Pseudomonas putida and Its Relationship to Cell Growth J. Bacteriol. 176, 6074-6081 (Pubitemid 24309947)
38. Vaillancourt, F. H., Labbé, G., Drouin, N. M., Fortin, P. D., and Eltis, L. D. (2002) The Mechanism-based Inactivation of 2,3-Dihydroxybiphenyl 1,2-Dioxygenase by Catecholic Substrates J. Biol. Chem. 277, 2019-2027 (Pubitemid 34968783)
39. Dai, S., Vaillancourt, F. H., Maaroufi, H., Drouin, N. M., Neau, D. B., Snieckus, V., Bolin, J. T., and Eltis, L. D. (2002) Identification and analysis of a bottleneck in PCB biodegradation Nat. Struct. Biol. 9, 934-939 (Pubitemid 35417063)
40. Mars, A. E., Kasberg, T., Kaschabek, S. R., vanAgteren, M. H., Janssen, D. B., and Reineke, W. (1997) Microbial Degradation of Chloroaromatics: Use of the meta -Cleavage Pathway for Mineralization of Chlorobenzene J. Bacteriol. 179, 4530-4537 (Pubitemid 27299069)
41. Kaschabek, S. R., Kasberg, T., Müller, D., Mars, A. E., Janssen, D. B., and Reineke, W. (1998) Degradation of Chloroaromatics: Purification and Characterization of a Novel Type of Chlorocatechol 2,3-Dioxygenase of Pseudomonas putida GJ31 J. Bacteriol. 180, 296-302 (Pubitemid 28100295)
42. Riegert, U., Heiss, G., Fischer, P., and Stolz, A. (1998) Distal Cleavage of 3-Chlorocatechol by an Extradiol Dioxygenase to 3-Chloro-2-Hydroxymuconic Semialdehyde J. Bacteriol. 180, 2849-2853 (Pubitemid 29122109)
43. Mars, A. E., Kingma, J., Kaschabek, S. R., Reineke, W., and Janssen, D. (1999) Conversion of 3-Chlorocatechol by Various Catechol 2,3-Dioxygenases and Sequence Analysis of the Chlorocatechol Dioxygenase Region of Pseudomonas putida GJ31 J. Bacteriol. 181, 1309-1318 (Pubitemid 29119571)
44. Riegert, U., Heiss, G., Kuhn, A. E., Müller, C., Contzen, M., Knackmuss, H.-J., and Stolz, A. (1999) Catalytic Properties of the 3-Chlorocatechol-Oxidizing 2,3-Dihydroxybiphenyl 1,2-Dioxygenase from Sphingomonas sp. Strain BN6 J. Bacteriol. 181, 4812-4817 (Pubitemid 29383508)
45. Vaillancourt, F. H., Haro, M. A., Drouin, N. M., Karim, Z., Maaroufi, H., and Eltis, L. D. (2003) Characterization of extradiol dioxygenases from a polychlorinated biphenyl-degrading strain that possess higher specificities for chlorinated metabolites J. Bacteriol. 185, 1253-1260 (Pubitemid 36176857)
46. Fortin, P. D., Lo, A. T.-F., Haro, M.-A., Kaschabek, S. R., Reineke, W., and Eltis, L. D. (2005) Evolutionarily Divergent Extradiol Dioxygenases Possess Higher Specificities for Polychlorinated Biphenyl Metabolites J. Bacteriol. 187, 415-421 (Pubitemid 40096229)
47. Riegert, U., Bürger, S., and Stolz, A. (2001) Altering Catalytic Properties of 3-Chlorocatechol-Oxidizing Extradiol Dioxygenase from Sphingomonas xenophaga BN6 by Random Mutagenesis J. Bacteriol. 183, 2322-2330 (Pubitemid 32240403)
48. Ohnishi, K., Okuta, A., Ju, J. S., Hamada, T., Misono, H., and Harayama, S. (2004) Molecular breeding of 2,3-dihydroxybiphenyl 1,2-dioxygenase for enhanced resistance to 3-chlorocatechol J. Biochem. 135, 305-317 (Pubitemid 38506756)
49. Okuta, A., Ohnishi, K., and Harayama, S. (2004) Construction of chimeric catechol 2,3-dioxygenase exhibiting improved activity against the suicide inhibitor 4-methylcatechol Appl. Environ. Microbiol. 70, 1804-1810 (Pubitemid 38365166)
50. Fortin, P. D., MacPherson, I., Neau, D. B., Bolin, J. T., and Eltis, L. D. (2005) Directed evolution of a ring-cleaving dioxygenase for polychlorinated biphenyl degradation J. Biol. Chem. 280, 42307-42314 (Pubitemid 43023202)
51. Ungnade, H. E. and Zilch, K. T. (1951) Phenoxyquinones. II. The Diphenoxyquinones J. Org. Chem. 16, 64-69
52. Burton, H. and Prail, P. F. G. (1952) Acylation Reactions Catalyzed by Strong Acids. Part VI. A Comparison of Zinc Chloride and Perchloric Acid as Catalysts for the Thiele Acetylation of Quinones J. Chem. Soc., 755-759
53. Harris, D. C. (1998) Nonlinear least-squares curve fitting with Microsoft excel solver J. Chem. Educ. 75, 119-121 (Pubitemid 128590127)
54. Kaschabek, S. R. and Reineke, W. (1992) Maleylacetate Reductase of Pseudomonas Sp Strain B13: Dechlorination of Chloromaleylacetates, Metabolites in the Degradation of Chloroaromatic Compounds Arch. Microbiol. 158, 412-417
55. Fowler, J. and Seltzer, S. (1970) Synthesis of Model Compounds for Maleylacetoacetic Acid. Maleylacetone J. Org. Chem. 35, 3529-3532
56. Prucha, M., Wray, V., and Pieper, D. H. (1996) Metabolism of 5-chlorosubstituted muconolactones Eur. J. Biochem. 237, 357-366 (Pubitemid 26126079)
57. Pieper, D. H., Pollmann, K., Nikodem, P., Gonzalez, B., and Wray, V. (2002) Monitoring key reactions in degradation of chloroaromatics by in situ H-1 nuclear magnetic resonance: Solution structures of metabolites formed from cis -dienelactone J. Bacteriol. 184, 1466-1470 (Pubitemid 34157574)
58. Seltzer, S. (1981) Nuclear Magnetic Resonance, Paramagnetic Ion Induced Relaxation Method to Differentiate between 1,3-Diketo and 1,3-Keto-Enol Isomers J. Org. Chem. 46, 2643-2650
59. Cain, R. B., Fortnagel, P., Hebenbrock, S., Kirby, G. W., McLenaghan, H. J. S., Rao, G. V., and Schmidt, S. (1997) Biosynthesis of a cyclic tautomer of (3-methylmaleyl)acetone from 4-hydroxy-3,5-dimethylbenzoate by Pseudomonas sp. HH35 but not by Rhodococcus rhodochrous N75 Biochem. Biophys. Res. Commun. 238, 197-201 (Pubitemid 27453300)
60. Schmidt, S. and Kirby, G. W. (2001) Dioxygenative cleavage of C-methylated hydroquinones and 2,6-dichlorohydroquinone by Pseudomonas sp HH35 Biochim. Biophys. Acta 1568, 83-89 (Pubitemid 33145388)
61. Silverstein, R. M., Bassler, G. C., and Morrill, T. C. (1991) Spectrometric Identification of Organic Compounds, 5th ed., Wiley, New York.
62. Fujiwara, M., Golovleva, L. A., Saeki, Y., Nozaki, M., and Hayaishi, O. (1975) Extradiol Cleavage of 3-Substituted Catechols by an Intradiol Dioxygenase, Pyrocatechase, from a Pseudomonad J. Biol. Chem. 250, 4848-4855
63. Cornish-Bowden, A. (2004) Fundamentals of Enzyme Kinetics, 3rd ed., Portland Press, London.
64. Borowski, T., Georgiev, V., and Siegbahn, P. E. M. (2005) Catalytic reaction mechanism of homogentisate dioxygenase: A hybrid DFT study J. Am. Chem. Soc. 127, 17303-17314 (Pubitemid 41791049)
65. Auffinger, P., Hays, F. A., Westhof, E., and Ho, P. S. (2004) Halogen bonds in biological molecules Proc. Natl. Acad. Sci. U.S.A. 101, 16789-16794 (Pubitemid 39601317)
66. Imai, Y. N., Inoue, Y., Nakanishi, I., and Kitaura, K. (2008) Cl-π interactions in protein-ligand complexes Protein Sci. 17, 1129-1137
67. Lommerse, J. P. M., Stone, A. J., Taylor, R., and Allen, F. H. (1996) The nature and geometry of intermolecular interactions between halogens and oxygen or nitrogen J. Am. Chem. Soc. 118, 3108-3116 (Pubitemid 26135501)
68. Matter, H., Nazare, M., Gussregen, S., Will, D. W., Schreuder, H., Bauer, A., Urmann, M., Ritter, K., Wagner, M., and Wehner, V. (2009) Evidence for C-Cl/C-Br•••π Interactions as an Important Contribution to Protein-Ligand Binding Affinity Angew. Chem., Int. Ed. 48, 2911-2916
69. Metrangolo, P., Meyer, F., Pilati, T., Resnati, G., and Terraneo, G. (2008) Mutual induced coordination in halogen-bonded anionic assemblies with (6,3) cation-templated topologies Chem. Commun. 1635-1637 (Pubitemid 351441895)
70. Kulawiec, R. J. and Crabtree, R. H. (1990) Coordination Chemistry of Halocarbons Coord. Chem. Rev. 99, 89-115
71. Wulfsberg, G., Yanisch, J., Meyer, R., Bowers, J., and Essig, M. (1984) Lewis-Base Properties of Ortho Chlorines in Copper(II) 2,4,6- Trichlorophenolates, 4-Bromo-2,6-Dichlorophenolates, and 2,6-Dichlorophenolates as Studied by Cl-35 Nuclear-Quadrupole Resonance Spectroscopy Inorg. Chem. 23, 715-719
72. Richardson, M. F., Wulfsberg, G., Marlow, R., Zaghonni, S., McCorkle, D., Shadid, K., Gagliardi, J., Jr., and Farris, B. (1993) Coordination of ortho chlorines in nickel and zinc 4-substituted 2,6-dichlorophenolates. Crystal and molecular structures of (N,N,N′,N′-tetramethyl-1,2-ethanediamine) bis(2,4,6-trichlorophenolato-O,Cl)nickel(II) and tris(pyridine)bis(2,4,6- trichlorophenolato-O)nickel(II) Inorg. Chem. 32, 1913-1919
73. Rocks, S. S., Brennessel, W. W., Machonkin, T. E., and Holland, P. L. (2010) Solution and Structural Characterization of Iron(II) Complexes with Ortho -Halogenated Phenolates: Insights Into Potential Substrate Binding Modes in Hydroquinone Dioxygenases Inorg. Chem. 49, 10914-10929
74. 17O]Water and Nitric Oxide Binding by Protocatechuate 4,5-Dioxygenase and Catechol 2,3-Dioxygenase J. Biol. Chem. 260, 14035-14044
75. Bertini, I., Briganti, F., and Scozzafava, A. (1994) Aliphatic and Aromatic Inhibitors Binding to the Active-Site of Catechol 2,3-Dioxygenase from Pseudomonas putida mt-2 FEBS Lett. 343, 56-60 (Pubitemid 24123946)
76. Kobayashi, T., Ishida, T., Horiike, K., Takahara, Y., Numao, N., Nakazawa, A., Nakazawa, T., and Nozaki, M. (1995) Overexpression of Pseudomonas putida Catechol 2,3-Dioxygenase with High Specific Activity by Genetically-Engineered Escherichia coli J. Biochem. 117, 614-622