Reactivity of deoxy- and oxyferrous dehaloperoxidase B from Amphitrite ornata: Identification of Compound II and Its ferrous-hydroperoxide precursor

Biochemistry

Volumn 50, Issue 27, 2011, Pages 5999-6011

  Dantonio, Jennifer ^a   Ghiladi, Reza A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC METHODS; BIFUNCTIONAL; BIFUNCTIONAL ENZYMES; BIOCHEMICAL ASSAY; CATALYTIC CYCLES; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; NEW SPECIES; OXIDATION STATE; OXYGEN BINDING; OXYGEN TRANSPORT; PEROXIDASE ACTIVITIES; PEROXIDASE CYCLE; STOPPED FLOW; UV-VISIBLE;

CATALYTIC OXIDATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; HEMOGLOBIN; HYDROGEN PEROXIDE; OXIDATION; OXYGEN; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PORPHYRINS; SPECTROSCOPY;

IRON;

DEHALOPEROXIDASE B; PEROXIDASE; UNCLASSIFIED DRUG;

AMPHITRITE ORNATA; ARTICLE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; NONHUMAN; OXIDATION REDUCTION STATE; OXYGEN TRANSPORT; POLYCHAETA; PRIORITY JOURNAL;

ANIMALS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME PRECURSORS; FERRIC COMPOUNDS; FERROUS COMPOUNDS; HYDROGEN PEROXIDE; ISOENZYMES; PEROXIDASES; POLYCHAETA; SPECTROPHOTOMETRY, ULTRAVIOLET;

AMPHITRITE ORNATA; POLYCHAETA; TEREBELLIDA;

EID: 79959950550     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200311u     Document Type: Article

References (79)

1. Woodin, S. A. (1991) Recruitment of Infauna: Positive or Negative Cues Am. Zool. 31, 797-807 (Pubitemid 23400198)
2. Woodin, S. A., Walla, M. D., and Lincoln, D. E. (1987) Occurrence of Brominated Compounds in Soft-Bottom Benthic Organisms J. Exp. Mar. Biol. Ecol. 107, 209-217
3. Chen, Y. P., Lincoln, D. E., Woodin, S. A., and Lovell, C. R. (1991) Purification and Properties of a Unique Flavin-Containing Chloroperoxidase from the Capitellid Polychaete Notomastus lobatus J. Biol. Chem. 266, 23909-23915 (Pubitemid 21908883)
4. Roach, M. P., Chen, Y. P., Woodin, S. A., Lincoln, D. E., Lovell, C. R., and Dawson, J. H. (1997) Notomastus lobatus chloroperoxidase and Amphitrite ornata dehaloperoxidase both contain histidine as their proximal heme iron ligand Biochemistry 36, 2197-2202 (Pubitemid 27104712)
5. Lincoln, D. E., Fielman, K. T., Marinelli, R. L., and Woodin, S. A. (2005) Bromophenol accumulation and sediment contamination by the marine annelids Notomastus lobatus and Thelepus crispus Biochem. Syst. Ecol. 33, 559-570 (Pubitemid 40483160)
6. King, G. M. (1986) Inhibition of Microbial Activity in Marine-Sediments by a Bromophenol from a Hemichordate Nature 323, 257-259 (Pubitemid 17249751)
7. Fielman, K. T. and Targett, N. M. (1995) Variation of 2,3,4-Tribromopyrrole and Its Sodium Sulfamate Salt in the Hemichordate Saccoglossus kowalevskii Mar. Ecol.: Prog. Ser. 116, 125-136
8. Chen, Y. P., Woodin, S. A., Lincoln, D. E., and Lovell, C. R. (1996) An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata J. Biol. Chem. 271, 4609-4612 (Pubitemid 26074937)
9. Osborne, R. L., Taylor, L. O., Han, K. P., Ely, B., and Dawson, J. H. (2004) Amphitrite ornata dehaloperoxidase: Enhanced activity for the catalytically active globin using MCPBA Biochem. Biophys. Res. Commun. 324, 1194-1198 (Pubitemid 40292148)
10. Feducia, J., Dumarieh, R., Gilvey, L. B., Smirnova, T., Franzen, S., and Ghiladi, R. A. (2009) Characterization of dehaloperoxidase compound ES and its reactivity with trihalophenols Biochemistry 48, 995-1005
11. Chen, Z., de Serrano, V., Betts, L., and Franzen, S. (2009) Distal histidine conformational flexibility in dehaloperoxidase from Amphitrite ornata Acta Crystallogr. D65, 34-40
12. Davis, M. F., Gracz, H., Vendeix, F. A., de Serrano, V., Somasundaram, A., Decatur, S. M., and Franzen, S. (2009) Different modes of binding of mono-, di-, and trihalogenated phenols to the hemoglobin dehaloperoxidase from Amphitrite ornata Biochemistry 48, 2164-2172
13. Smirnova, T. I., Weber, R. T., Davis, M. F., and Franzen, S. (2008) Substrate binding triggers a switch in the iron coordination in dehaloperoxidase from Amphitrite ornata: HYSCORE experiments J. Am. Chem. Soc. 130, 2128-2129 (Pubitemid 351287968)
14. Miksovska, J., Horsa, S., Davis, M. F., and Franzen, S. (2008) Conformational dynamics associated with photodissociation of CO from dehaloperoxidase studied using photoacoustic calorimetry Biochemistry 47, 11510-11517
15. Nienhaus, K., Nickel, E., Davis, M. F., Franzen, S., and Nienhaus, G. U. (2008) Determinants of substrate internalization in the distal pocket of dehaloperoxidase hemoglobin of Amphitrite ornata Biochemistry 47, 12985-12994
16. Franzen, S., Gilvey, L. B., and Belyea, J. L. (2007) The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata Biochim. Biophys. Acta 1774, 121-130 (Pubitemid 46049138)
17. de Serrano, V., Chen, Z., Davis, M. F., and Franzen, S. (2007) X-ray crystal structural analysis of the binding site in the ferric and oxyferrous forms of the recombinant heme dehaloperoxidase cloned from Amphitrite ornata Acta Crystallogr. D63, 1094-1101 (Pubitemid 47480522)
18. Franzen, S., Jasaitis, A., Belyea, J., Brewer, S. H., Casey, R., MacFarlane, A. W. t., Stanley, R. J., Vos, M. H., and Martin, J. L. (2006) Hydrophobic distal pocket affects NO-heme geminate recombination dynamics in dehaloperoxidase and H64V myoglobin J. Phys. Chem. B 110, 14483-14493 (Pubitemid 44188016)
19. Franzen, S., Belyea, J., Gilvey, L. B., Davis, M. F., Chaudhary, C. E., Sit, T. L., and Lommel, S. A. (2006) Proximal cavity, distal histidine, and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase Biochemistry 45, 9085-9094 (Pubitemid 44156371)
20. Belyea, J., Belyea, C. M., Lappi, S., and Franzen, S. (2006) Resonance Raman study of ferric heme adducts of dehaloperoxidase from Amphitrite ornata Biochemistry 45, 14275-14284 (Pubitemid 44868121)
21. 2 binding and involves two consecutive one-electron steps: Role of ferryl intermediates Biochemistry 48, 4231-4238
22. 2-dependent oxidative dehalogenation of chlorophenols to DNA-binding radicals and quinones Biochemistry 46, 9823-9829 (Pubitemid 47328588)
23. Osborne, R. L., Raner, G. M., Hager, L. P., and Dawson, J. H. (2006) C. fumago chloroperoxidase is also a dehaloperoxidase: Oxidative dehalogenation of halophenols J. Am. Chem. Soc. 128, 1036-1037 (Pubitemid 43190593)
24. Osborne, R. L., Sumithran, S., Coggins, M. K., Chen, Y. P., Lincoln, D. E., and Dawson, J. H. (2006) Spectroscopic characterization of the ferric states of Amphitrite ornata dehaloperoxidase and Notomastus lobatus chloroperoxidase: His-ligated peroxidases with globin-like proximal and distal properties J. Inorg. Biochem. 100, 1100-1108
25. Han, K., Woodin, S. A., Lincoln, D. E., Fielman, K. T., and Ely, B. (2001) Amphitrite ornata, a marine worm, contains two dehaloperoxidase genes Mar. Biotechnol. 3, 287-292 (Pubitemid 32943855)
26. DAntonio, J., DAntonio, E. L., Thompson, M. K., Bowden, E. F., Franzen, S., Smirnova, T., and Ghiladi, R. A. (2010) Spectroscopic and mechanistic investigations of dehaloperoxidase B from Amphitrite ornata Biochemistry 49, 6600-6616
27. Dunford, H. B. and Stillman, J. S. (1976) Function and Mechanism of Action of Peroxidases Coord. Chem. Rev. 19, 187-251
28. 2 Biochemistry 49, 6064-6069
29. Matsui, T., Ozaki, S., Liong, E., Phillips, G. N., Jr., and Watanabe, Y. (1999) Effects of the location of distal histidine in the reaction of myoglobin with hydrogen peroxide J. Biol. Chem. 274, 2838-2844 (Pubitemid 29075367)
30. Finzel, B. C., Poulos, T. L., and Kraut, J. (1984) Crystal structure of yeast cytochrome c peroxidase refined at 1.7-Å resolution J. Biol. Chem. 259, 13027-13036 (Pubitemid 15223817)
31. Phillips, G. N., Jr., Arduini, R. M., Springer, B. A., and Sligar, S. G. (1990) Crystal structure of myoglobin from a synthetic gene Proteins 7, 358-365 (Pubitemid 20218372)
32. Gajhede, M., Schuller, D. J., Henriksen, A., Smith, A. T., and Poulos, T. L. (1997) Crystal structure of horseradish peroxidase C at 2.15 Å resolution Nat. Struct. Biol. 4, 1032-1038 (Pubitemid 27525808)
33. de Serrano, V., DAntonio, J., Franzen, S., and Ghiladi, R. A. (2010) Structure of dehaloperoxidase B at 1.58 Å resolution and structural characterization of the AB dimer from Amphitrite ornata Acta Crystallogr. D66, 529-538
34. LaCount, M. W., Zhang, E., Chen, Y. P., Han, K., Whitton, M. M., Lincoln, D. E., Woodin, S. A., and Lebioda, L. (2000) The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins J. Biol. Chem. 275, 18712-18716 (Pubitemid 30422829)
35. Lebioda, L., LaCount, M. W., Zhang, E., Chen, Y. P., Han, K., Whitton, M. M., Lincoln, D. E., and Woodin, S. A. (1999) An enzymatic globin from a marine worm Nature 401, 445 (Pubitemid 129515774)
36. Beers, R. F., Jr. and Sizer, I. W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase J. Biol. Chem. 195, 133-140
37. Zoia, L. and Argyropoulos, D. S. (2009) Phenoxy radical detection using P-31 NMR spin trapping J. Phys. Org. Chem. 22, 1070-1077
38. Mayhew, S. G. (1978) The redox potential of dithionite and SO-2 from equilibrium reactions with flavodoxins, methyl viologen and hydrogen plus hydrogenase Eur. J. Biochem. 85, 535-547 (Pubitemid 8335277)
39. Kizek, R., Vacek, J., Trnkova, L., and Jelen, F. (2004) Cyclic voltammetric study of the redox system of glutathione using the disulfide bond reductant tris(2-carboxyethyl)phosphine Bioelectrochemistry 63, 19-24 (Pubitemid 38534189)
40. Heineman, W. R., Meckstroth, M. L., Norris, B. J., and Su, C.-H. (1979) Optically transparent thin layer electrode techniquesfor the study of biological redox systems J. Electroanal. Chem. 104, 577-585 (Pubitemid 10102342)
41. Ball, E. G. (1937) Studies on Oxidation-Reduction XXIII: Ascorbic Acid J. Biol. Chem. 118, 219-239
42. Belyea, J., Gilvey, L. B., Davis, M. F., Godek, M., Sit, T. L., Lommel, S. A., and Franzen, S. (2005) Enzyme function of the globin dehaloperoxidase from Amphitrite ornata is activated by substrate binding Biochemistry 44, 15637-15644 (Pubitemid 41746894)
43. Lardinois, O. M. and Ortiz de Montellano, P. R. (2004) Autoreduction of ferryl myoglobin: Discrimination among the three tyrosine and two tryptophan residues as electron donors Biochemistry 43, 4601-4610 (Pubitemid 38500589)
44. Giulivi, C. and Cadenas, E. (1994) Ferrylmyoglobin: Formation and chemical reactivity toward electron-donating compounds Methods Enzymol. 233, 189-202
45. Herold, S. and Rehmann, F. J. (2003) Kinetics of the reactions of nitrogen monoxide and nitrite with ferryl hemoglobin Free Radical Biol. Med. 34, 531-545 (Pubitemid 36254827)
46. Giulivi, C. and Davies, K. J. (1994) Hydrogen peroxide-mediated ferrylhemoglobin generation in vitro and in red blood cells Methods Enzymol. 231, 490-496
47. Yadav, R. K., Dolai, S., Pal, S., and Adak, S. (2008) Role of tryptophan-208 residue in cytochrome c oxidation by ascorbate peroxidase from Leishmania major: Kinetic studies on Trp208Phe mutant and wild type enzyme Biochim. Biophys. Acta 1784, 863-871
48. Marquez, L. A., Quitoriano, M., Zilinskas, B. A., and Dunford, H. B. (1996) Kinetic and spectral properties of pea cytosolic ascorbate peroxidase FEBS Lett. 389, 153-156 (Pubitemid 26226490)
49. Hewson, W. D. and Hager, L. P. (1979) Oxidation of horseradish peroxidase compound II to compound I J. Biol. Chem. 254, 3182-3186
50. Belevich, I., Borisov, V. B., and Verkhovsky, M. I. (2007) Discovery of the true peroxy intermediate in the catalytic cycle of terminal oxidases by real-time measurement J. Biol. Chem. 282, 28514-28519 (Pubitemid 47606033)
51. Shintaku, M., Matsuura, K., Yoshioka, S., Takahashi, S., Ishimori, K., and Morishima, I. (2005) Absence of a detectable intermediate in the compound I formation of horseradish peroxidase at ambient temperature J. Biol. Chem. 280, 40934-40938 (Pubitemid 41780587)
52. Baek, H. K. and Van Wart, H. E. (1989) Elementary steps in the formation of horseradish peroxidase compound I: Direct observation of compound 0, a new intermediate with a hyperporphyrin spectrum Biochemistry 28, 5714-5719
53. Egawa, T., Yoshioka, S., Takahashi, S., Hori, H., Nagano, S., Shimada, H., Ishimori, K., Morishima, I., Suematsu, M., and Ishimura, Y. (2003) Kinetic and spectroscopic characterization of a hydroperoxy compound in the reaction of native myoglobin with hydrogen peroxide J. Biol. Chem. 278, 41597-41606 (Pubitemid 37310415)
54. Thompson, M. K., Franzen, S., Ghiladi, R. A., Reeder, B. J., and Svistunenko, D. A. (2010) Compound ES of Dehaloperoxidase Decays via Two Alternative Pathways Depending on the Conformation of the Distal Histidine J. Am. Chem. Soc. 132, 17501-17510
55. Lente, G. and Espenson, J. H. (2004) Photoreduction of 2,6-dichloroquinone in aqueous solution: Use of a diode array spectrophotometer concurrently to drive and detect a photochemical reaction J. Photochem. Photobiol., A 163, 249-258
56. Lente, G. and Espenson, J. H. (2004) A kinetic study of the early steps in the oxidation of chlorophenols by hydrogen peroxide catalyzed by a water-soluble iron(III) porphyrin New J. Chem. 28, 847-852 (Pubitemid 39108024)
57. Dunford, H. B. (1999) Heme Peroxidases, Wiley-VCH, New York.
58. Noble, R. W. and Gibson, Q. H. (1970) The reaction of ferrous horseradish peroxidase with hydrogen peroxide J. Biol. Chem. 245, 2409-2413
59. Aviram, I., Wittenberg, A., and Wittenberg, J. B. (1978) The reaction of ferrous leghemoglobin with hydrogen peroxide to form leghemoglobin(IV) J. Biol. Chem. 253, 5685-5689 (Pubitemid 8403700)
60. Kohler, H., Taurog, A., and Dunford, H. B. (1988) Spectral studies with lactoperoxidase and thyroid peroxidase: Interconversions between native enzyme, compound II, and compound III Arch. Biochem. Biophys. 264, 438-449
61. Jantschko, W., Furtmuller, P. G., Zederbauer, M., Neugschwandtner, K., Jakopitsch, C., and Obinger, C. (2005) Reaction of ferrous lactoperoxidase with hydrogen peroxide and dioxygen: An anaerobic stopped-flow study Arch. Biochem. Biophys. 434, 51-59 (Pubitemid 40040470)
62. Jantschko, W., Georg Furtmuller, P., Zederbauer, M., Lanz, M., Jakopitsch, C., and Obinger, C. (2003) Direct conversion of ferrous myeloperoxidase to compound II by hydrogen peroxide: An anaerobic stopped-flow study Biochem. Biophys. Res. Commun. 312, 292-298 (Pubitemid 37445171)
63. Jakopitsch, C., Wanasinghe, A., Jantschko, W., Furtmueller, P. G., and Obinger, C. (2005) Kinetics of interconversion of ferrous enzyme, compound II and compound III of wild-type Synechocystis catalase-peroxidase and Y249F. Proposal for the catalatic mechanism J. Biol. Chem. 280, 9037-9042 (Pubitemid 40409596)
64. Tanaka, M., Matsuura, K., Yoshioka, S., Takahashi, S., Ishimori, K., Hori, H., and Morishima, I. (2003) Activation of hydrogen peroxide in horseradish peroxidase occurs within approximately 200 micro s observed by a new freeze-quench device Biophys. J. 84, 1998-2004 (Pubitemid 36322962)
65. Ichikawa, Y., Nakajima, H., and Watanabe, Y. (2006) Characterization of peroxide-bound heme species generated in the reaction of thermally tolerant cytochrome c552 with hydrogen peroxide ChemBioChem 7, 1582-1589 (Pubitemid 44556005)
66. Denisov, I. G., Dawson, J. H., Hager, L. P., and Sligar, S. G. (2007) The ferric-hydroperoxo complex of chloroperoxidase Biochem. Biophys. Res. Commun. 363, 954-958 (Pubitemid 47554699)
67. Denisov, I. G., Makris, T. M., and Sligar, S. G. (2002) Formation and decay of hydroperoxo-ferric heme complex in horseradish peroxidase studied by cryoradiolysis J. Biol. Chem. 277, 42706-42710 (Pubitemid 35285641)
68. Brittain, T., Baker, A. R., Butler, C. S., Little, R. H., Lowe, D. J., Greenwood, C., and Watmough, N. J. (1997) Reaction of variant sperm-whale myoglobins with hydrogen peroxide: The effects of mutating a histidine residue in the haem distal pocket Biochem. J. 326 (Part 1) 109-115 (Pubitemid 27386924)
69. Ozaki, S., Inada, Y., and Watanabe, Y. (1998) Characterization of polyethylene glycolated horseradish peroxidase in organic solvents: Generation and stabilization of transient catalytic intermediates at low temperature J. Am. Chem. Soc. 120, 8020-8025 (Pubitemid 28417611)
70. Franzen, S., Roach, M. P., Chen, Y. P., Dyer, R. B., Woodruff, W. H., and Dawson, J. H. (1998) The unusual reactivities of Amphirite ornata dehaloperoxidase and Notomastus lobatus chloroperoxidase do not arise from a histidine imidazolate proximal heme iron ligand J. Am. Chem. Soc. 120, 4658-4661 (Pubitemid 28282717)
71. Alayash, A. I., Ryan, B. A., Eich, R. F., Olson, J. S., and Cashon, R. E. (1999) Reactions of sperm whale myoglobin with hydrogen peroxide. Effects of distal pocket mutations on the formation and stability of the ferryl intermediate J. Biol. Chem. 274, 2029-2037
72. Shimahara, H., Yoshida, T., Shibata, Y., Shimizu, M., Kyogoku, Y., Sakiyama, F., Nakazawa, T., Tate, S., Ohki, S. Y., Kato, T., Moriyama, H., Kishida, K., Tano, Y., Ohkubo, T., and Kobayashi, Y. (2007) Tautomerism of histidine 64 associated with proton transfer in catalysis of carbonic anhydrase J. Biol. Chem. 282, 9646-9656 (Pubitemid 47104596)
73. Jewsbury, P. and Kitagawa, T. (1994) The distal residue-CO interaction in carbonmonoxy myoglobins: A molecular dynamics study of two distal histidine tautomers Biophys. J. 67, 2236-2250 (Pubitemid 24369646)
74. Rovira, C., Schulze, B., Eichinger, M., Evanseck, J. D., and Parrinello, M. (2001) Influence of the heme pocket conformation on the structure and vibrations of the Fe-CO bond in myoglobin: A QM/MM density functional study Biophys. J. 81, 435-445 (Pubitemid 32605982)
75. 2 discrimination in myoglobin J. Phys. Chem. B 109, 3065-3070 (Pubitemid 40307808)
76. Lukin, J. A., Simplaceanu, V., Zou, M., Ho, N. T., and Ho, C. (2000) NMR reveals hydrogen bonds between oxygen and distal histidines in oxyhemoglobin Proc. Natl. Acad. Sci. U.S.A. 97, 10354-10358
77. Phillips, G. N., Teodoro, M. L., Li, T. S., Smith, B., and Olson, J. S. (1999) Bound CO is a molecular probe of electrostatic potential in the distal pocket of myoglobin J. Phys. Chem. B 103, 8817-8829 (Pubitemid 129613930)
78. Rovira, C. (2003) Role of the His64 residue on the properties of the Fe-CO and Fe-O-2 bonds in myoglobin. A CHARMM/DFT study THEOCHEM 632, 309-321
79. Rovira, C. (2003) The structure and dynamics of the Fe-CO bond in myoglobin J. Phys.: Condens. Matter 15, S1809-S1822