The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1774, Issue 1, 2007, Pages 121-130

  Franzen, Stefan ^a   Gilvey, Lauren B ^a   Belyea, Jennifer L ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Enzyme kinetics; Fourier transform infrared spectroscopy; Peroxidase; X ray crystallography

Indexed keywords

BACTERIAL ENZYME; DEHALOPEROXIDASE; ENZYME; PEROXIDASE; UNCLASSIFIED DRUG;

AMPHITRITE ORNATA; ARTICLE; BACTERIUM; DEBROMINATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE; ESCHERICHIA COLI; FOURIER TRANSFORMATION; INFRARED SPECTROSCOPY; MARINE ENVIRONMENT; NONHUMAN; OXIDATION; PH; PRIORITY JOURNAL; TIME; ULTRAVIOLET SPECTROSCOPY; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; KINETICS; PEROXIDASES; PHENOLS; POLYCHAETA; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

AMPHITRITE ORNATA; POLYCHAETA; TEREBELLIDA;

EID: 33846029162     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2006.09.019     Document Type: Article

References (70)

1. Belyea J., Gilvey L.B., Davis M.F., Godek M., Sit T.L., Lommel S.A., and Franzen S. Enzyme function of the globin dehaloperoxidase from Amphitrite ornata is activated by substrate binding. Biochemistry 44 (2005) 15637-15644
2. Chen Y.P., Woodin S.A., Lincoln D.E., and Lovell C.R. An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata. J. Biol. Chem. 271 (1996)
3. Chen Y.P., Lincoln D.E., Woodin S.A., and Lovell C.R. Purification and properties of a unique flavin-containing chloroperoxidase from the capitellid polychaete Nontmastus lobatus. J. Biol. Chem. 266 (1991) 23909-23915
4. LaCount M.W., Zhang E.L., Chen Y.P., Han K.P., Whitton M.M., Lincoln D.E., Woodin S.A., and Lebioda L. The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins. J. Biol. Chem. 275 (2000) 18712-18716
5. Franzen S., Roach M.P., Chen Y.P., Dyer R.B., Woodruff W.H., and Dawson J.H. The unusual reactivities of Amphitrite ornata dehaloperoxidase and Notomastus lobatus chloroperoxidase do not arise from a histidine imidazolate proximal heme iron ligand. J. Am. Chem. Soc. 120 (1998) 4658-4661
6. Ferrari R.P., Laurenti E., and Trotta F. Oxidative 4-dechlorination of 2,4,6-trichlorophenol catalyzed by horseradish peroxidase. J. Biol. Inorg. Chem. 4 (1999) 232-237
7. Courteix A., and Bergel A. Horseradish peroxidase-catalyzed hydroxylation of phenol. 1. Thermodynamic analysis. Enzyme Microb. Technol. 17 (1995) 1087-1093
8. Harvey P.J., Floris R., Lundell T., Palmer J.M., Schoemaker H.E., and Wever R. Catalytic mechanisms and regulation of lignin peroxidase. Biochem. Soc. Trans. 20 (1992) 345-349
9. Monzani E., Gatti A.L., Profumo A., Casella L., and Gullotti M. Oxidation of phenolic compounds by lactoperoxidase. Evidence for the presence of a low-potential compound II during catalytic turnover. Biochemistry 36 (1997) 1918-1926
10. Bassi A., Geng Z., and Gijzen M. Enzymatic removal of phenol and chlorophenols using soybean seed hulls. Eng. Life Sci. 4 (2004) 125-130
11. Geng Z.H., Bassi A.S., and Gijzen M. Enzymatic treatment of soils contaminated with phenol and chlorophenols using soybean seed hulls. Water Air Soil Pollut. 154 (2004) 151-166
12. Ator M.A., and Montellano O.d. Protein control of prosthetic heme reactivity. Reaction of substrates with the heme edge of horseradish peroxidase. J. Biol. Chem. 262 (1987) 1542-1551
13. Howes B.D., RodriguezLopez J.N., Smith A.T., and Smulevich G. Mutation of distal residues of horseradish peroxidase: influence on substrate binding and cavity properties. Biochemistry 36 (1997) 1532-1543
14. Abelskov A.K., Smith A.T., Rasmussen C.B., Dunford H.B., and Welinder K.G. pH dependence and structural interpretation of the reactions of Coprinus cinereus peroxidase with hydrogen peroxide, ferulic acid, and 2,2′-azinobis(3-ethylbenzthiazoline-6-sulfonic acid). Biochemistry 36 (1997) 9453-9463
15. Landino L.M., Crews B.C., Gierse J.K., Hauser S.D., and Marnett L.J. Mutational analysis of the role of the distal histidine and glutamine residues of prostaglandin-endoperoxide synthase-2 in peroxidase catalysis, hydroperoxide reduction, and cyclooxygenase activation. J. Biol. Chem. 272 (1997) 21565-21574
16. Bhattacharyya D.K., Bandyopadhyay U., and Banerjee R.K. Chemical and kinetic evidence for an essential histidine residue in the electron-transfer from aromatic donor to horseradish-peroxidase compound-I. J. Biol. Chem. 268 (1993) 22292-22298
17. Foshay M.C., Vitello L.B., and Erman J.E. PH dependence of heme iron coordination, hydrogen peroxide reactivity, and cyanide binding in cytochrome c peroxidase(H52K). Biochemistry 43 (2004) 5065-5072
18. Patel P.K., Mondal M.S., Modi S., and Behere D.V. Kinetic studies on the oxidation of phenols by the horseradish peroxidase compound II. Biochim. Biophys. Acta, Prot. Struct. Mol. Enzymol. 1339 (1997) 79-87
19. Furtmuller P.G., Burner U., Regelsberger G., and Obinger C. Spectral and kinetic studies on the formation of eosinophil peroxidase compound I and its reaction with halides and thiocyanate. Biochemistry 39 (2000) 15578-15584
20. Dunford H.B. Heme Peroxidases (1999), Wiley-VCH, New York
21. Jones D.K., Dalton D.A., Rosell F.I., and Raven E.L. Class I heme peroxidases: characterization of soybean ascorbate peroxidase. Arch. Biochem. Biophys. 360 (1998) 173-178
22. Zamocky M., Janecek S., and Koller F. Common phylogeny of catalase-peroxidases and ascorbate peroxidases. Gene 256 (2000) 169-182
23. Mano J., Ohno C., Domae Y., and Asada K. Chloroplast ascorbate peroxidase is the primary target of methyl viologen-induced stress in spinach leaves: its relevance to monohydroascorbate radical detected with in vivo ESR. Biochim. Biophys. Acta 1504 (2001) 275-287
24. Hiner A.N.P., Ruiz J.H., Lopez J.N.R., Canovas F.G., Brisset N.C., Smith A.T., Arnao M.B., and Acosta M. Reactions of the class II peroxidases, lignin peroxidase and Arthromyces ramosus peroxidase, with hydrogen peroxide-catalase-like activity, compound III formation, and enzyme inactivation. J. Biol. Chem. 277 (2002) 26879-26885
25. Kvaratskhelia M., Winkel C., Naldrett M.T., and Thorneley R.N.F. A novel high activity cationic ascorbate peroxidase from tea (Camellia sinensis)-a class III peroxidase with unusual substrate specificity. J. Plant Phys. 154 (1999) 273-282
26. Wright P.J., and English A.M. Buffer-anion-dependent Ca2+ leaching from horseradish peroxidase at low pH. J. Biol. Inorg. Chem. 6 (2001) 348-358
27. Gajhede M., Schuller D.J., Henriksen A., Smith A.T., and Poulos T.L. Crystal structure of horseradish peroxidase C at 2.15 angstrom resolution. Nat. Struct. Biol. 4 (1997) 1032-1038
28. Battistuzzi G., D'Onofrio M., Loschi L., and Sola M. Isolation and characterization of two peroxidases from Cucumis sativus. Arch. Biochem. Biophys. 388 (2001) 100-112
29. Burner U., Furtmuller P.G., Kettle A.J., Koppenol W.H., and Obinger C. Mechanism of reaction of myeloperoxidase with nitrite. J. Biol. Chem. 275 (2000) 20597-20601
30. Dunford H.B., and Alberty R.A. Kinetics of fluoride binding by ferric horse radish peroxidase. Biochemistry 6 (1967) 447
31. Ricard J., Williams R.J., and Mazza G. Oxidation-reduction potentials and ionization states of 2 turnip peroxidases. Eur. J. Biochem. 28 (1972) 566
32. Poulos T.L., and Kraut J. The stereochemistry of peroxidase catalysis. J. Biol. Chem. 255 (1980) 8199-8205
33. Henriksen A., Smith A.T., and Gajhede M. The structures of the horseradish peroxidase C-ferulic acid complex and the ternary complex with cyanide suggest how peroxidases oxidize small phenolic substrates. J. Biol. Chem. 274 (1999) 35005-35011
34. Tanaka M., Ishimori K., Mukai M., Kitagawa T., and Morishima I. Catalytic activities and structural properties of horseradish peroxidase distal His42 → Glu or Gln mutant. Biochemistry 36 (1997) 9889-9898
35. Bateman L., Leger C., Goodin D.B., and Armstrong F.A. A distal histidine mutant (H52Q) of yeast cytochrome c peroxidase catalyzes the oxidation of H2O2 instead of its reduction. J. Am. Chem. Soc. 123 (2001) 9260-9263
36. Vitello L.B., Erman J.E., Miller M.A., Wang J., and Kraut J. Effect of Arginine-48 replacement on the reaction between cytochrome-c peroxidase and hydrogen-peroxide. Biochemistry 32 (1993) 9807-9818
37. RodriguezLopez J.N., Smith A.T., and Thorneley R.N.F. Role of Arginine 38 in horseradish peroxidase a critical, residue for substrate binding and catalysis. J. Biol. Chem. 271 (1996) 4023-4030
38. Hiner A.N.P., Raven E.L., Thorneley R.N.F., Garcia-Canovas F., and Rodriguez-Lopez J.N. Mechanisms of compound I formation in heme peroxidases. J. Inorg. Biochem. 91 (2002) 27-34
39. Lebioda L., LaCount M.W., Zhang E., Chen Y.P., Han K., WHitton M.M., Lincoln D.E., and Woodin S.A. An enzymatic globin from a marine worm. Nature 401 (1999) 445
40. Franzen S., Belyea J.L., Gilvey L.B.G., Davis M.F., Chaudhary C., Sit T.L., and Lommel S.A. Proximal cavity, distal histidine and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase. Biochemistry 45 (2006) 9085-9094
41. Yang F., and Phillips Jr. G.N. Crystal structures of CO-, deoxy- and met-myoglobins at various pH values. J. Mol. Biol. 256 (1996) 762-774
42. Suzuki T., Watanabe Y., Nagasawa M., Matsuoka A., and Shikama K. Dual nature of the distal histidine residue in the autoxidation reaction of myoglobin and hemoglobin-comparison of the H64 mutants. Eur. J. Biochem. 267 (2000) 6166-6174
43. Franzen S. An electrostatic model for the frequency shifts in the carbonmonoxy stretching band of myoglobin: correlation of hydrogen bonding and the Stark tuning rate. J. Am. Chem. Soc. 124 (2002) 13271-13281
44. Nienhaus K., Olson J.S., Franzen S., and Nienhaus G.U. The origin of stark splitting in the initial photoproduct state of MbCO. J. Am. Chem. Soc. 127 (2005) 40-41
45. Franzen S. Effect of a charge relay on the vibrational frequencies of carbonmonoxy iron porphine adducts: the coupling of changes in axial ligand bond strength and porphine core size. J. Am. Chem. Soc. 123 (2001) 12578-12589
46. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res. 25 (1997) 3389-3402
47. Han K.P., Woodin S.A., Lincoln D.E., Fielman K.T., and Ely B. Amphitrite ornata, a marine worm, contains two dehaloperoxidase genes. Mar. Biotechnol. 3 (2001) 287-292
48. Conti E., Moser C., Rizzi M., Mattevi A., Lionetti C., Coda A., Ascenzi P., Brunori M., and Bolognesi M. X-ray crystal-structure of ferric aplysia-limacina myoglobin in different liganded states. J. Mol. Biol. 233 (1993) 498-508
49. Suzuki T., Takagi T., and Shikama K. Amino-acid-sequence of myoglobin from Aplysia-Kurodai. Biochim. Biophys. Acta 669 (1981) 79-83
50. Chen Z.Z., Martin J., and Lee B.T.O. Hemoglobins of Kiefferulus, sister genus of Chironomus (Diptera: Insecta): evolution of the Hb VIIB cluster. J. Mol. Evol. 41 (1995) 909-919
51. Burmester T., Ebner B., Weich B., and Hankeln T. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 19 (2002) 416-421
52. de Sanctis D., Dewilde S., Pesce A., Moens L., Ascenzi P., Hankeln T., Burmester T., and Bolognesi M. Mapping protein matrix cavities in human cytoglobin through Xe atom binding. Biochem. Biophys. Res. Commun. 316 (2004) 1217-1221
53. Osborne R.L., Taylor L.O., Han K.P., Ely B., and Dawson J.H. Amphitrite ornata dehaloperoxidase: enhanced activity for the catalytically active globin using MCPBA. Biochem. Biophys. Res. Commun. 324 (2004) 1194-1198
54. Nienhaus K., Deng P.C., Belyea J., Franzen S., and Nienhaus G.U. Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata. J. Phys. Chem. B 110 (2006) 13264-13276
55. Belyea J., Belyea C.M., Lappi S., and Franzen S. Resonance Raman Study of Ferric Heme Adducts of Dehaloperoxidase from Amphitrite ornata. Biochemistry 45 (2006) 14275-14284
56. Weber R.E., Magnum C.P., Steinman H., Bonaventura C., Sullivan B., and Bonaventura J. Hemoglobins of two terebellid polychaetes: Enoplobranchus sanuigneus and Amphitire ornata. Comp. Biochem. Physiol. 56A (1977) 179-187
57. Chiancone E., Ferruzzi G., Bonaventura C., and Bonaventura J. Amphitrite-Ornata Erythrocruorin. 2. Molecular controls of function. Biochim. Biophys. Acta 670 (1981) 84-92
58. Royer Jr. W.E., Pardanani A., Gibson Q.H., Peterson E.S., and Friedman J.M. Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14526-14531
59. Heaslet H.A., and Royer W.E. Crystalline ligand transitions in Lamprey hemoglobin - structural evidence for the regulation of oxygen affinity. J. Biol. Chem. 276 (2001) 26230-26236
60. Dunford H.B. One-electron oxidations by peroxidases. Xenobiotica 25 (1995) 725-733
61. Ferreira M.L. UV/visible study of the reaction of oxidoreductases and model compounds with H2O2. Macromol. Biosci. 3 (2003) 179-188
62. Dunford H.B. How do enzymes work? Effect of electron circuits on transition state acid dissociation constants. J. Biol. Inorg. Chem. 6 (2001) 819-822
63. M.F. Davis, H. Gracz, J. Belyea, L.B. Gilvey, S.M. Decatur and S. Franzen, Binding of Both the Phenol and Phenolate Forms of the Substrate in the Hemoglobin Dehaloperoxidase from Amphitrite ornata, J. Am. Chem. Soc. (submitted for publication).
64. J. Belyea, R. MacArthur, T. Smirnova and S. Franzen, Substrate Binding Triggers a Change in the Iron Spin State in Dehaloperoxidase from Amphitrite ornata, Proc. Natl. Acad. Sci. U.S.A. (in preparation).
65. Phillips J., Teodoro M.L., Li T., Smith B., and Olson J.S. Bound CO is a molecular probe of the electrostatic potential in the distal pocket of myoglobin. J. Phys. Chem. B 103 (1999) 8817-8829
66. Franzen S. Carbonmonoxy rebinding kinetics in H93G myoglobin: separation of proximal and distal side effects. J. Phys. Chem. B 106 (2002) 4533-4542
67. Ivanov D., Sage J.T., Keim M., Powell J.R., Asher S.A., and Champion P.M. Determination of CO orientation by single-crystal infrared linear dichroism. J. Am. Chem. Soc. 116 (1994) 4139-4140
68. Vojtechovsky J., Chu K., Berendzen J., Sweet R.M., and Schlichting I. Crystal structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77 (1999) 2153-2174
69. Critchlow J.E., and Dunford H.B. Studies on horseradish-peroxidase. 9. Kinetics of oxidation of para cresol by compound II. J. Biol. Chem. 247 (1972) 3703
70. Roach M.P., Chen Y.P., Woodin S.A., Lincoln D.E., and Dawson J.H. Notomastus lobatus chloroperoxidase and Amphitrite ornata dehaloperoxidase both contain histidine as their proximal heme iron ligand. Biochemistry 36 (1997) 2197-2202