The dehaloperoxidase paradox

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 4, 2012, Pages 578-588

  Franzen, Stefan ^a   Thompson, Matthew K ^a   Ghiladi, Reza A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Competitive inhibition; Enzyme; Hemoglobin; Marine; Peroxidase; Phenol

Indexed keywords

2,4,6 TRIHALOPHENOL; 2,6 DIBROMOQUINONE; 4 BROMOPHENOL; DEHALOPEROXIDASE; DEHALOPEROXIDASE A; DEHALOPEROXIDASE B; HEME; HEMOGLOBIN; HISTIDINE; IRON; OXYFERROUS; PEROXIDASE; PHENOL DERIVATIVE; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ENZYME KINETICS; ENZYME STRUCTURE; MUTANT; OXIDATION REDUCTION POTENTIAL; OXYGEN TRANSPORT; PH; PRIORITY JOURNAL;

AMPHITRITE ORNATA;

EID: 84857252001     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.12.008     Document Type: Review

References (92)

1. S.E.V. Phillips Structure and refinement of oxymyoglobin at 1.6 Ã... resolution J. Mol. Biol. 142 1980 531 554
2. L. Lebioda, M.W. LaCount, E. Zhang, Y.P. Chen, K. Han, M.M. Whitton, D.E. Lincoln, and S.A. Woodin An enzymatic globin from a marine worm Nature (London) 401 1999 445
3. V.S. de Serrano, Z. Chen, M.F. Davis, and S. Franzen 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. D Biol. Crystallogr. D63 2007 1094 1101
4. V.S. de Serrano, J. D'Antonio, M.K. Thompson, S. Franzen, and R.A. Ghiladi Crystal structure of Dehaloperoxidase B at 1.58 A and characterization of the A/B Dimer from Amphitrite ornata Acta Crystallogr. D Biol. Crystallogr. 66 2010 529 538
5. V.S. de Serrano, M.F. Davis, J.F. Gaff, Q. Zhang, Z. Chen, E.L. D'Antonio, E.F. Bowden, R. Rose, and S. Franzen X-ray structure of the metcyano form of dehaloperoxidase from Amphitrite ornata: evidence for photoreductive dissociation of the iron-cyanide bond Acta Crystallogr. D 66 2010 770 782
6. M.W. LaCount, E. Zhang, Y.P. Chen, K. Han, M.M. Whitton, D.E. Lincoln, S.A. Woodin, and L. Lebioda The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins J. Biol. Chem. 275 2000 18712 18716
7. A. Henricksen, D.J. Schuller, K. Meno, K.G. Welinder, A.T. Smith, and M. Gajhede Structural interactions between horseradish peroxidase C and the substrate benzhydroxamic acid determined by X-ray crystallography Biochemistry 37 1998 8054 8060
8. K. Han, S.A. Woodin, D.E. Lincoln, K.T. Fielman, and B. Ely Amphitrite ornata, a marine worm, contains two dehaloperoxidase genes Mar. Biotechnol. 3 2001 287 292
9. E. Chiancone, G. Ferruzzi, C. Bonaventura, and J. Bonaventura Amphitrite-ornata erythrocruorin.2. Molecular controls of function Biochim. Biophys. Acta 670 1981 84 92
10. M.K. Thompson, M.F. Davis, V. deSerrano, F.P. Nicoletti, B.D. Howes, G. Smulevich, and S. Franzen Internal binding of halogenated phenols in dehaloperoxidase-hemoglobin inhibits peroxidase activity Biophys. J. 99 2010 1586 1599
11. M.F. Davis, B.G. Bobay, and S. Franzen Determination of separate inhibitor and substrate binding sites in the dehaloperoxidase-hemoglobin from Amphitrite ornata Biochemistry 49 2010 1199 1206
12. D.E. Lincoln, K.T. Fielman, R.L. Marinelli, and S.A. Woodin Bromophenol accumulation and sediment contamination by the marine annelids Notomastus lobatus and Thelepus crispus Biochem. Syst. Ecol. 33 2005 559 570
13. Y.P. Chen, S.A. Woodin, D.E. Lincoln, and C.R. Lovell An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata J. Biol. Chem. 271 1996 4609 4612
14. R.L. Osborne, L.O. Taylor, K.P. Han, B. Ely, and J.H. Dawson Amphitrite ornata dehaloperoxidase: enhanced activity for the catalytically active globin using MCPBA Biochem. Biophys. Res. Commun. 324 2004 1194 1198
15. R.E. Weber, C. Mangum, H. Steinman, C. Bonaventura, B. Sullivan, and J. Bonaventura Hemoglobins of two terebellid polychaetes: Enoplobranchus sanguineus and Amphitrite ornata Comp. Biochem. Physiol. A Comp. Physiol. 56 1977 179 187
16. R. Hardison Hemoglobins from bacteria to man: evolution of different patterns of gene expression J. Exp. Biol. 201 1998 1099 1117
17. X. Bailly, C. Chabasse, S. Hourdez, S. Dewilde, S. Martial, L. Moens, and F. Zal Globin gene family evolution and functional diversification in annelids FEBS J. 274 2007 2641 2652
18. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
19. J.H. Dawson, and M. Sono Cytochrome P-450 and chloroperoxidase: thiolate-ligated heme enzymes. Spectroscopic determination of their active-site structures and mechanistic implications of thiolate ligation Chem. Rev. 87 1987 1255 1276
20. P.M. Champion, B.R. Stallard, G.C. Wagner, and I.C. Gunsalus Resonance Raman detection of an Fe-S bond in cytochrome P450cam J. Am. Chem. Soc. 104 1982 5469 5472
21. T.L. Poulos, and R. Raag Cytochrome P450cam: crystallography, oxygen activation, and electron transfer FASEB J. 6 1992 674 679
22. M. Sundaramoorthy, J. Terner, and T.L. Poulos The crystal structure of chloroperoxidase: a heme peroxidase-cytochrome P450 functional hybrid Structure 3 1995 1367 1377
23. T.L. Poulos, and J. Kraut The stereochemistry of peroxidase catalysis J. Biol. Chem. 255 1980 8199 8205
24. J. D'Antonio, E.L. D'Antonio, E.F. Bowden, T. Smirnova, S. Franzen, and R.A. Ghiladi Spectroscopic and mechanistic investigations of dehaloperoxidase B from Amphitrite ornata Biochemistry 49 2011 6600 6616
25. J. Belyea, L.B. Gilvey, M.F. Davis, M. Godek, T.L. Sit, S.A. Lommel, and S. Franzen Enzyme function of the globin dehaloperoxidase from Amphitrite ornata is activated by substrate binding Biochemistry 44 2005 15637 15644
26. S. Franzen, L.B. Gilvey, and J.L. Belyea The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata Biochim. Biophys. Acta Proteins Proteomics 1774 2007 121 130
27. K.T. Fielman, S.A. Woodin, M.D. Walla, and D.E. Lincoln Widespread occurrence of natural halogenated organics among temperate marine infauna Mar. Ecol. Prog. Ser. 181 1999 1 12
28. S.A. Woodin, S.M. Lindsay, and D.E. Lincoln Biogenic bromophenols as negative recruitment cues Mar. Ecol. Prog. Ser. 157 1997 303 306
29. E. Zhang, Y.P. Chen, M.P. Roach, D.E. Lincoln, C.R. Lovell, S.A. Woodin, J.H. Dawson, and L. Lebioda Crystallization and initial spectroscopic characterization of the heme-containing dehaloperoxidase from the marine polychaete Amphitrite ornata Acta Crystallogr. D Biol. Crystallogr. D52 1996 1191 1193
30. J.P. Harrington, S. Kobayashi, S.C. Dorman, S.L. Zito, and R.E. Hirsh Acellular invertebrate hemoglobins as model therapeutic oxygen carriers: unique redox potentials Artif. Cells Blood Substit. Biotechnol. 35 2007 53 67
31. J. Du, M. Sono, and J.H. Dawson Functional switching of Amphitrite ornata dehaloperoxidase from O-2-binding globin to peroxidase enzyme facilitated by halophenol substrate and H2O2 Biochemistry 49 2010 6064 6069
32. A. Bonamore, and A. Boffi Flavohemoglobin: structure and reactivity IUBMB Life 60 2008 19 28
33. P.R.O. de Montallano Cytochrome P450: Structure, Mechanism, and Biochemistry, in 2005 Kluwer Academic/Plenum Publishers New York 689
34. P. George, and D.H. Irvine The reaction of metmyoglobin with hydrogen peroxide Biochem. J. 52 1952 511 517
35. M. Davis, H. Gracz, L. Gilvey, S. Franzen, and S. Decatur H-1 NMR analysis of substrate binding in the globin dehaloperoxidase, from Amphitrite ornata Biophysical Society Meeting 2007 538A 539A
36. K. Nienhaus, P. Deng, J. Belyea, S. Franzen, and G.U. Nienhaus Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata J. Phys. Chem. B 110 2006 13264 13276
37. V. de Serrano, S. Franzen, Structural Evidence for Stabilization of Inhibitor Binding by a Protein Cavity in the Dehaloperoxidase-Hemoglobin from Amphitrite ornata. Peptide Sci. (A.S.A.P.).
38. F.P. Nicoletti, M.K. Thompson, B.D. Howes, S. Franzen, and G. Smulevich New insights into the role of distal histidine flexibility in ligand stabilization of Dehaloperoxidase-hemoglobin from Amphitrite ornata Biochemistry 49 2010 1903 1912
39. J. Feducia, R. Dumarieh, L.B.G. Gilvey, T. Smirnova, S. Franzen, and R.A. Ghiladi Characterization of dehaloperoxidase compound ES and its reactivity with trihalophenols Biochemistry 48 2009 995 1005
40. T.I. Smirnova, R.T. Weber, M.F. Davis, and S. Franzen Substrate binding triggers a switch in the iron coordination in dehaloperoxidase from Amphitrite ornata: HYSCORE experiments J. Am. Chem. Soc. 130 2008 2128 2129
41. M.K. Thompson, S. Franzen, R.A. Ghiladi, B.J. Reeder, and D.A. Svistunenko Compound ES of dehaloperoxidase decays via two alternative pathways depending on the conformation of the distal histidine J. Am. Chem. Soc. 132 2010 17501 17510
42. Z. Chen, V. de Serrano, L. Betts, and S. Franzen Distal histidine conformational flexibility in dehaloperoxidase from Amphitrite ornata Acta Crystallogr. D Biol. Crystallogr. D65 2009 34 40
43. F. Yang, and G.N. Phillips Jr. Crystal structures of CO-, deoxy- and met-myoglobins at various pH values J. Mol. Biol. 256 1996 762 774
44. R. Davydov, R.L. Osborne, S.H. Kim, J.H. Dawson, and B.M. Hoffman EPR and ENDOR studies of cryoreduced compounds II of Peroxidases and myoglobin. Proton-coupled electron transfer and protonation status of ferryl Biochemistry 47 2008 5147 5155
45. G. Tsaprailis, and A.M. English Different pathways of radical translocation in yeast cytochrome c peroxidase and its W191F mutant on reaction with H2O2 suggest an antioxidant role J. Biol. Inorg. Chem. 8 2003 248 255
46. M.F. Davis, H. Gracz, F.A.P. Vendeix, V. de Serrano, A. Somasundaram, S.M. Decatur, and S. Franzen Different modes of binding of mono-, di-, and trihalogenated phenols to the hemoglobin dehaloperoxidase from Amphitrite ornata Biochemistry 48 2009 2164 2172
47. R. Davydov, R.L. Osborne, M. Shanmugam, J. Du, J.H. Dawson, and B.M. Hoffman Probing the oxyferrous and catalytically active ferryl states of Amphitrite ornata dehaloperoxidase by cryoreduction and EPR/ENDOR spectroscopy. Detection of compound I J. Am. Chem. Soc. 132 2010 14995 15004
48. A.P. Shreve, S. franzen, M.C. Simpson, and R.B. Dyer Dependence of NO recombination dynamics in horse heart myoglobin on solution glycerol content. J. Phys. Chem. B 103 1999 7909 7975
49. S. Franzen, A. Jasaitis, J. Belyea, S.H. Brewer, R. Casey, A.W.I.V. MacFarlane, R.J. Stanley, M.H. Vos, and J.-L. Martin Hydrophobic distal pocket affects NO-heme geminate recombination dynamics in dehaloperoxidase and H64V myoglobin J. Phys. Chem. B 110 2006 14483 14493
50. H.A. Ma, M.K. Thompson, J. Gaff, and S. Franzen Kinetic analysis of a naturally occurring bioremediation enzyme: dehaloperoxidase-hemoglobin from Amphitrite ornata J. Phys. Chem. B 114 2010 13823 13829
51. K. Nienhaus, E. Nickel, M.F. Davis, S. Franzen, and G.U. Nienhaus Deterinants of substrate internalization in the distal pocket of dehaloperoxidase-hemoglobin of Amphitrite ornata Biochemistry 47 2008 12985 12994
52. R.L. Osborne, M.K. Coggins, G.M. Raner, M. Walla, and J.H. Dawson The mechanism of oxidative halophenol dehalogenation by Amphitrite ornata dehaloperoxidase is initiated by H2O2 binding and involves two consecutive one-electron steps: role of ferryl intermediates Biochemistry 48 2009 4231 4238
53. M.P. Roach, Y.P. Chen, S.A. Woodin, D.E. Lincoln, C.R. Lovell, and J.H. Dawson Notomastus lobatus chloroperoxidase and Amphitrite ornata dehaloperoxidase both contain histidine as their proximal heme iron ligand Biochemistry 36 1997 2197 2202
54. S. Franzen, M.P. Roach, Y.P. Chen, R.B. Dyer, W.H. Woodruff, and J.H. Dawson 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 1998 4658 4661
55. B.H. Dunford Heme Peroxidases 1999 John Wiley and Sons New York
56. X.H. Qu, H. Wang, Q.Z. Zhang, X.Y. Shi, F. Xu, and W.X. Wang Mechanistic and kinetic studies on the homogeneous gas-phase formation of PCDD/Fs from 2,4,5-Trichlorophenol Environ. Sci. Technol. 43 2009 4068 4075
57. B. Dellinger, S. Loninicki, L. Khachatryan, Z. Maskos, R.W. Hall, J. Adounkpe, C. McFerrin, and H. Truong Formation and stabilization of persistent free radicals Proc. Combust. Inst. 31 2007 521 528
58. B.E. Sturgeon, B.J. Battenburg, B.J. Lyon, and S. Franzen Revisiting the peroxidase oxidation of 2,4,6-trihalophenols: ESR detection of radical intermediates Chem. Res. Toxicol. 24 2011 1862 1868
59. K. Sasan, B. Sturgeon, B.J. Lyon, B.J. Battenburg, H. Gracz, R. Dumariah, R. Ghiladi, S. Franzen, Non-photochemical base-catalyzed hydroxylation of 2,6-dichloroquinone occurs by a radical mechanism. J. Phys. Chem. B (A.S.A.P.).
60. G. Lente, and J.H. Espenson Photoaccelerated oxidation of chlorinated phenols Chem. Commun. 2003 1162 1163
61. J.E. Huyett, P.E. Doan, R. Gurbiel, A.L.P. Houseman, M. Sivaraja, D.B. Goodin, and B.M. Hoffman Compound ES of cytochrome c-peroxidase contains a Trp Pi-cation radical - characterization by CW and pulsed Q-band ENDOR spectroscopy J. Am. Chem. Soc. 117 1995 9033 9041
62. S. Hahm, L. Geren, B. Durham, and F. Millett Reaction of cytochrome-c with the radical in cytochrome-c peroxidase compound-I J. Am. Chem. Soc. 115 1993 3372 3373
63. C.W. Fenwick, and A.M. English Trapping and LC-MS identification of protein radicals formed in the horse heart metmyoglobin-H2O2 reaction J. Am. Chem. Soc. 118 1996 12236 12237
64. B.J. Reeder, D.A. Svistunenko, M.A. Sharpe, and M.T. Wilson Characteristics and mechanism of formation of peroxide-induced heme to protein cross-linking in myoglobin Biochemistry 41 2002 367 375
65. P.J. Wright, and A.M. English Scavenging with TEMPO center dot to identify peptide- and protein-based radicals by mass spectrometry: advantages of spin scavenging over spin trapping J. Am. Chem. Soc. 125 2003 8655 8665
66. D.A. Svistunenko, B.J. Reeder, M.T. Wilson, and C.E. Cooper Radical formation and migration in myoglobins Prog. React. Kinet. Mech. 28 2003 105 118
67. A. Arduini, G. Mancinelli, G.L. Radatti, W. Damonti, P. Hochstein, and E. Cadenas Reduction of sperm whale ferrylmyoglobin by endogenous reducing agents: potential reducible loci of ferrylmyoglobin Free Radic. Biol. Med. 13 1992 449 454
68. T. Matsui, S. Ozaki, and Y. Watanabe On the formation and reactivity of compound I of the His-64 myoglobin mutants J. Biol. Chem. 272 1997 32735 32738
69. M. Sivaraja, D.B. Goodin, M. Smith, and B.M. Hoffman Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES Science (Washington, DC, United States) 245 1989 738 740
70. H.M. Zhang, S.M. He, and A.G. Mauk Radical formation at Tyr39 and Tyr153 following reaction of yeast cytochrome c peroxidase with hydrogen peroxide Biochemistry 41 2002 13507 13513
71. S. Ozaki, T. Matsui, M.P. Roach, and Y. Watanabe Rational molecular design of a catalytic site: engineering of catalytic functions to the myoglobin active site framework Coord. Chem. Rev. 198 2000 39 59
72. S.-i. Ozaki, I. Hara, T. Matsui, and Y. Watanabe Molecular engineering of myoglobin: the improvement of oxidation activity by replacing Phe-43 with tryptophan Biochemistry 40 2001 1044 1052
73. L.L. Wan, M.B. Twitchett, L.D. Eltis, A.G. Mauk, and M. Smith In vitro evolution of horse heart myoglobin to increase peroxidase activity Proc. Natl. Acad. Sci. U. S. A. 95 1998 12825 12831
74. P.K. Witting, A.G. Mauk, and P.A. Lay Role of tyrosine-103 in myoglobin peroxidase activity: kinetic and steady-state studies on the reaction of wild-type and variant recombinant human myoglobins with H2O2 Biochemistry 41 2002 11495 11503
75. R.P. Mason Using anti-5,5-dimethyl-1-pyrroline N-oxide (anti-DMPO) to detect protein radicals in time and space with immuno-spin trapping Free Radic. Biol. Med. 36 2004 1214 1223
76. M.R. Gunther Probing the free radicals formed in the metmyoglobin- hydrogen peroxide reaction Free Radic. Biol. Med. 36 2004 1354
77. S. Bhattacharjee, L.J. Deterding, J. Jiang, M.G. Bonini, K.B. Tomer, D.C. Ramirez, and R.P. Mason Electron transfer between a tyrosyl radical and a cysteine residue in hemoproteins: spin trapping analysis J. Am. Chem. Soc. 129 2007 13493 13501
78. J. D'Antonio, and R.A. Ghiladi Reactivity of deoxy- and oxyferrous dehaloperoxidase B from Amphitrite ornata: identification of compound II and its ferrous-hydroperoxide precursor Biochemistry 50 2011 5999 6011
79. R.W. Noble, and Q.H. Gibson The reaction of ferrous horseradish peroxidase with hydrogen peroxide J. Biol. Chem. 245 1970 2409 2413
80. I. Aviram, B.A. Wittenberg, and J.B. Wittenberg Reaction of ferrous leghemoglobin with hydrogen peroxide to form leghemoglobin(IV) J. Biol. Chem. 253 1978 5685 5689
81. H. Kohler, A. Taurog, and H.B. Dunford Spectral studies with lactoperoxidase and thyroid peroxidase: interconversions between native enzyme, compound II, and compound III Arch. Biochem. Biophys. 264 1988 438 449
82. W. Jantschko, P.G. Furtmuller, M. Zederbauer, K. Neugschwandtner, C. Jakopitsch, and C. Obinger Reaction of ferrous lactoperoxidase with hydrogen peroxide and dioxygen: an anaerobic stopped-flow study Arch. Biochem. Biophys. 434 2005 51 59
83. W. Jantschko, P.G. Furtmuller, M. Zederbauer, M. Lanz, C. Jakopitsch, and C. Obinger Direct conversion of ferrous myeloperoxidase to compound II by hydrogen peroxide: an anaerobic stopped-flow study Biochem. Biophys. Res. Commun. 312 2003 292 298
84. C. Jakopitsch, A. Wanasinghe, W. Jantschko, P.G. Furtmuller, and C. Obinger Kinetics of interconversion of ferrous enzymes, compound II and compound III, of wild-type Synechocystis catalase-peroxidase and Y249F J. Biol. Chem. 280 2005 9037 9042
85. H. Shimahara, T. Yoshida, Y. Shibata, M. Shimizu, Y. Kyogoku, F. Sakiyama, T. Nakazawa, S. Tate, S. Ohki, T. Kato, H. Moriyama, K. Kishida, Y. Tano, T. Ohkubo, and Y. Kobayashi Tautomerism of histidine 64 associated with proton transfer in catalysis of carbonic anhydrase J. Biol. Chem. 282 2007 9646 9656
86. P. Jewsbury, and T. Kitagawa The distal residue CO interaction in carbonomonoxy myoglobins - a molecular dynamics study of two distal histidine tautomers Biophys. J. 67 1994 2236 2250
87. C. Rovira, B. Schulze, M. Eichinger, J.D. Evanseck, and M. Parrinello 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 2001 435 445
88. F.D. Angelis, A.A. Jarzecki, R. Car, and T.G. Spiro Quantum chemical evaluation of protein control over heme ligation: CO/O2 discrimination in myoglobin J. Phys. Chem. B 109 2005 3065 3070
89. J.A. Lukin, V. Simplaceanu, M. Zou, N.T. Ho, and C. Ho NMR reveals hydrogen bonds between oxygen and distal histidines in oxyhemoglobin Proc. Natl. Acad. Sci. U. S. A. 97 2000 10354 10358
90. G.N. Phillips, M.L. Teodoro, T.S. Li, B. Smith, and J.S. Olson Bound CO is a molecular probe of the electrostatic potential in the distal pocket of myoglobin J. Phys. Chem. B 103 1999 8817 8829
91. Y.P. Chen, D.E. Lincoln, S.A. Woodin, and C.R. Lovell Purification and properties of a unique flavin-containing chloroperoxidase from the capitellid polychaete Notomastus-lobatus J. Biol. Chem. 266 1991 23909 23915
92. F.P. Nicoletti, M.K. Thompson, S. Franzen, and G. Smulevich Degradation of sulfide by dehaloperoxidase-hemoglobin from Amphitrite ornata J. Biol. Inorg. Chem. 16 2011 611 619