The role of T56 in controlling the flexibility of the distal histidine in dehaloperoxidase-hemoglobin from Amphitrite ornata

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 10, 2013, Pages 2020-2029

  Jiang, Shu ^a   Wright, Iain ^a   Swartz, Paul ^a   Franzen, Stefan ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Catalytic efficiency; Enzyme kinetics; Hemichrome; Molecular dynamics; Raman; Resonance

Indexed keywords

AMINO ACID; DEHALOPEROXIDASE; ENZYME; HEME; HEMOGLOBIN; HISTIDINE; LEAD; PEROXIDASE; UNCLASSIFIED DRUG;

ANNELID; ARTICLE; CATALYSIS; CATALYST; CONFORMATION; EISENIA (ANNELID); ENZYME ACTIVITY; ENZYME KINETICS; LIGATION; MUTAGENESIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; STEREOSPECIFICITY; WILD TYPE;

2,4,6-TBP; 2,4,6-TCP; 2,4,6-TRIBROMOPHENOL; 2,4,6-TRICHLOROPHENOL; 2,6-DCQ; 2,6-DICHLOROQUINONE; 5CHS; 6CHS; 6CLS; CATALYTIC EFFICIENCY; ENZYME KINETICS; FIVE-COORDINATE HIGH SPIN; FOURIER TRANSFORM INFRARED; FTIR; HEMICHROME; MD; MOLECULAR DYNAMICS; RESONANCE RAMAN; RR; SIX-COORDINATE HIGH SPIN; SIX-COORDINATE LOW SPIN; SPERM WHALE MYOGLOBIN; SWMB; WILD-TYPE DEHALOPEROXIDASE-HEMOGLOBIN A; WT-DHP;

ANIMALS; BIOCATALYSIS; HEME; HEMOGLOBINS; HISTIDINE; IRON; KINETICS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PEROXIDASES; POLYCHAETA; RECOMBINANT PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPECTRUM ANALYSIS, RAMAN; THERMODYNAMICS; THREONINE;

EID: 84884497354     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.06.005     Document Type: Article

References (69)

1. 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 Physiol. 56 1977 179 187
2. 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 (Pubitemid 41746894)
3. 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 (Pubitemid 26074937)
4. S. Franzen, M.P. Roach, Y.P. Chen, R.B. Dyer, W.H. Woodruff, and J.H. Dawson 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 (Pubitemid 28282717)
5. L. Lebioda, M.W. LaCount, E. Zhang, Y.P. Chen, K. Han, M.M. Whitton, D.E. Lincoln, and S.A. Woodin Protein structure: an enzymatic globin from a marine worm Nature 401 1999 445 (Pubitemid 129515774)
6. V. 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. 63 2007 1094 1101 (Pubitemid 47480522)
7. Z. Chen, V. de Serrano, L. Betts, and S. Franzen Distal histidine conformational flexibility in dehaloperoxidase from Amphitrite ornata Acta Crystallogr. D: Biol. Crystallogr. 65 2009 34 40
8. 2 binding and involves two consecutive one-electron steps: role of ferryl intermediates Biochemistry 48 2009 4231 4238
9. 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
10. H. 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
11. R.P. Ferrari, E. Laurenti, and F. Trotta Oxidative 4-dechlorination of 2,4,6-trichlorophenol catalyzed by horseradish peroxidase J. Biol. Inorg. Chem. 4 1999 232 237 (Pubitemid 29227799)
12. A. Gumiero, E.J. Murphy, C.L. Metcalfe, P.C.E. Moody, and E.L. Raven An analysis of substrate binding interactions in the heme peroxidase enzymes: a structural perspective Arch. Biochem. Biophys. 500 2010 13 20
13. 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 (Pubitemid 351620752)
14. 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
15. 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
16. S. Franzen, M.K. Thompson, and R.A. Ghiladi The dehaloperoxidase paradox Biochim. Biophys. Acta 1824 2012 578 588
17. J. Zhao, J. Rowe, J. Franzen, C. He, and S. Franzen Study of the electrostatic effects of mutations on the surface of dehaloperoxidase hemoglobin A Biochem. Biophys. Res. Commun. 420 2012 733 737
18. G. Schkolnik, T. Utesch, J. Zhao, S. Jiang, M. Thompson, M.-A. Mroginski, P. Hildebrandt, and S. Franzen Catalytic efficiency of dehaloperoxidase A is controlled by electrostatics - application of the vibrational Stark effect to understand enzyme kinetics Biochem. Biophys. Res. Commun. 430 2013 1101 1105
19. E.L. D'Antonio, J. D'Antonio, V.S. de Serrano, H.S. Gracz, M.K. Thompson, R.A. Ghiladi, E.F. Bowden, and S. Franzen The functional consequences of the creation of an Asp-His-Fe triad in a 3/3 globin Biochemistry 50 2011
20. 2 activation and heme protection in both peroxidase and globin functions J. Phys. Chem. B 116 2012 12065 12077
21. 2 Biochemistry 49 2010 6064 6069
22. 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 (Pubitemid 32943855)
23. J. D'Antonio, E.L. D'Antonio, M.K. Thompson, E.F. Bowden, S. Franzen, T. Smirnova, and R.A. Ghiladi Spectroscopic and mechanistic investigations of dehaloperoxidase B from Amphitrite ornata Biochemistry 49 2010 6600 6616
24. V. de Serrano, J. D'Antonio, S. Franzen, and R.A. Ghiladi Structure of dehaloperoxidase B at 1.58 angstrom resolution and structural characterization of the AB dimer from Amphitrite ornata, Acta Crystallogr Section D Biol. Crystallogr. 66 2010 529 538
25. D.B. Goodin, and D.E. McRee The Asp-His-Fe triad of cytochrome c peroxidase controls the reduction potential, electronic structure, and coupling of the tryptophan free radical to the heme Biochemistry 32 1993 3313 3324 (Pubitemid 23126897)
26. M.M. Fitzgerald, M.L. Trester, G.M. Jensen, D.E. McRee, and D.B. Goodin The role of aspartate-235 in the binding of cations to an artificial cavity at the radical site of cytochrome-C peroxidase Protein Sci. 4 1995 1844 1850
27. A.T. Smith, and N.C. Veitch Substrate binding and catalysis in heme peroxidases Curr. Opin. Chem. Biol. 2 1998 269 278 (Pubitemid 128428135)
28. A.J. Sitter, C. Reczek, and J. Terner Heme-linked ionization of horseradish peroxidase compound II monitored by the resonance Raman Fe (IV)=O stretching vibration J. Biol. Chem. 260 1985 7515 7522 (Pubitemid 15063030)
29. L.B. Vitello, J.E. Erman, M.A. Miller, J. Wang, and J. Kraut Effect of arginine-48 replacement on the reaction between cytochrome c peroxidase and hydrogen peroxide Biochemistry 32 1993 9807 9818 (Pubitemid 23296828)
30. S. Franzen, and S.G. Boxer On the origin of heme absorption band shifts and associated protein structural relaxation in myoglobin following flash photolysis J. Biol. Chem. 272 1997 9655 9660 (Pubitemid 27171625)
31. S. Franzen Carbonmonoxy rebinding kinetics in H93G myoglobin: separation of proximal and distal side effects J. Phys. Chem. B 106 2002 4533 4542 (Pubitemid 35282024)
32. T.L. Poulos, and J. Kraut The stereochemistry of peroxidase catalysis J. Biol. Chem. 255 1980 8199 8205
33. G. Smulevich, A. Feis, and B.D. Howes Fifteen years of Raman spectroscopy of engineered heme containing peroxidases: what have we learned? Acc. Chem. Res. 38 2005 433 440 (Pubitemid 40816655)
34. J.H. Dawson Probing structure-function relations in heme-containing oxygenases and peroxidases Science 240 1988 433 439
35. J.E. Erman, L.B. Vitello, M.A. Miller, A. Shaw, K.A. Brown, and J. Kraut Histidine 52 is a critical residue for rapid formation of cytochrome c peroxidase compound I Biochemistry 32 1993 9798 9806 (Pubitemid 23296827)
36. T.L. Poulos Heme enzyme crystal structures Adv. Inorg. Biochem. 7 1988 1 36
37. 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 (Pubitemid 30422829)
38. T. Matsui, S. Ozaki, E. Liong, G.N. Phillips Jr., and Y. Watanabe Effects of the location of distal histidine in the reaction of myoglobin with hydrogen peroxide J. Biol. Chem. 274 1999 2838 2844 (Pubitemid 29075367)
39. M.C. Foshay, L.B. Vitello, and J.E. Erman Relocation of the distal histidine in cytochrome c peroxidase: properties of CcP(W51H), CcP(W51H/H52W), and CcP(W51H/H52L) Biochemistry 48 2009 5417 5425
40. S. Franzen, J. Belyea, L.B. Gilvey, M.F. Davis, C.E. Chaudhary, T.L. Sit, and S.A. Lommel Proximal cavity, distal histidine, and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase Biochemistry 45 2006 9085 9094 (Pubitemid 44156371)
41. 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
42. M.K. Thompson, M.F. Davis, V. De Serrano, F.P. Nicoletti, B.D. Howes, G. Smulevich, and S. Franzen Internal binding of halogenated phenols in dehaloperoxidase-hemoglobin inhibits peroxidase function Biophys. J. 99 2010 1586 1595
43. 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 (Pubitemid 44115665)
44. K. Nienhaus, E. Nickel, M.F. Davis, S. Franzen, and G.U. Nienhaus Determinants of substrate internalization in the distal pocket of dehaloperoxidase hemoglobin of Amphitrite ornata Biochemistry 47 2008 12985 12994
45. 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
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. J. Du, X. Huang, S.F. Sun, C.X. Wang, L. Lebioda, and J.H. Dawson Amphitrite ornata dehaloperoxidase (DHP): investigations of structural factors that influence the mechanism of halophenol dehalogenation using "peroxidase-like" myoglobin mutants and "myoglobin-like" DHP mutants Biochemistry 50 2011 8172 8180
48. H.H. Lai, T. Li, D.S. Lyons, G.N. Phillips Jr., J.S. Olson, and Q.H. Gibson Phe 46 (CD4) orients the distal histidine for hydrogen bonding to bound ligands in sperm whale myoglobin Proteins Struct. Funct. Bioinform. 22 1995 322 339
49. 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 (Pubitemid 26108816)
50. M.T. Nelson, W. Humphrey, A. Gursoy, A. Dalke, L.V. Kalé, R.D. Skeel, and K. Schulten NAMD: a parallel, object-oriented molecular dynamics program Intl. J. High Perf. Comp. Appl. 10 1996 251 268
51. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 (Pubitemid 26152973)
52. S. Chanchevalap, Z. Yang, N. Cui, Z. Qu, G. Zhu, C. Liu, L.R. Giwa, L. Abdulkadir, and C. Jiang Involvement of histidine residues in proton sensing of ROMK1 channel J. Biol. Chem. 275 2000 7811
53. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326 (Pubitemid 27085611)
54. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of coot Acta Crystallogr. D: Biol. Crystallogr. 66 2010 486 501
55. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G.W. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D: Biol. Crystallogr. 67 2011 235 242
56. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D: Biol. Crystallogr. 66 2010 213 221
57. A. Plummer, M.K. Thompson, and S. Franzen The role of polarity of the distal pocket in the control of inhibitor binding in dehaloperoxidase-hemoglobin Biochemistry 52 2013 2218 2227
58. E.V. Arnold, D.S. Bohle, and P.A. Jordan Reversible and irreversible hemichrome generation by the oxygenation of nitrosylmyoglobin Biochemistry 38 1999 4750 4756
59. A. Boffi, L. Guarrera, L. Giangiacomo, C. Spagnuolo, and E. Chiancone Proximal and distal effects on the coordination chemistry of ferric Scapharca homodimeric hemoglobin as revealed by heme pocket mutants Biochemistry 39 2000 3500 3504 (Pubitemid 30170023)
60. J.W. Smalley, M.F. Thomas, A.J. Birss, R. Withnall, and J. Silver A combination of both arginine- and lysine-specific gingipain activity of Porphyromonas gingivalis is necessary for the generation of the micro-oxo bishaem-containing pigment from haemoglobin Biochem. J. 379 2004 833
61. X.Y. Li, and T.G. Spiro Is bound carbonyl linear or bent in heme proteins? Evidence from resonance Raman and infrared spectroscopic data J. Am. Chem. Soc. 110 1988 6024 6033
62. J. Zhao, V. de Serrano, J. Zhao, P. Le, and S. Franzen Structural and kinetic study of an internal substrate binding site in dehaloperoxidase- hemoglobin A from Amphitrite ornata Biochemistry 52 2013 2427 2439
63. 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
64. 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
65. H. Pelletier, and J. Kraut Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c Science 258 1992 1748 1755 (Pubitemid 23087339)
66. S. Franzen, L.B. Gilvey, and J.L. Belyea The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata Biochim. Biophys. Acta-Prot. Proteom. 1774 2007 121 130 (Pubitemid 46049138)
67. R. Hardison Hemoglobins from bacteria to man: evolution of different patterns of gene expression J. Expmtl. Biol. 201 1998 1099 1117 (Pubitemid 28278316)
68. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
69. 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: Biol. Crystallogr. 66 2010 770 782