Proximal cavity, distal histidine, and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase

Biochemistry

Volumn 45, Issue 30, 2006, Pages 9085-9094

  Franzen, Stefan ^a   Belyea, Jennifer ^a   Gilvey, Lauren B ^a   Davis, Michael F ^a   Chaudhary, Chelsea E ^a   Sit, Tim L ^a   Lommel, Steven A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; HALOGENATION; HYDROGEN BONDS; MUTAGENESIS; PHENOXY RESINS; SUBSTRATES;

AMPHITRITE ORNATA DEHALOPEROXIDASE; ONE-ELECTRON PRODUCT; PHENOXY RADICAL; PROXIMAL HISTIDINE;

BIOCHEMISTRY;

2,4,6 TRIBROMOPHENOL; 2,4,6 TRICHLOROPHENOL; 2,6 DIBROMO 1,4 BENZOQUINONE; 2,6 DICHLORO 1,4 BENZOQUINONE; ARGININE; BENZOQUINONE DERIVATIVE; DEHALOPEROXIDASE; GLOBIN; GLYCINE; HEME PEROXIDASE; HISTIDINE; HYDROGEN PEROXIDE; HYDROXYL GROUP; MYOGLOBIN; PEROXIDASE; PHENOL DERIVATIVE; TYROSINE; UNCLASSIFIED DRUG; VALINE;

AMPHITRITE ORNATA; ARTICLE; BINDING SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; MUTATION; NONHUMAN; POLYCHAETA; PRIORITY JOURNAL;

ANIMALS; BINDING SITES; HISTIDINE; HYDROGEN BONDING; MUTAGENESIS, SITE-DIRECTED; PEROXIDASES; PHENYLALANINE; POLYCHAETA; SUBSTRATE SPECIFICITY; TYROSINE; VALINE;

AMPHITRITE ORNATA; PHYSETER CATODON;

EID: 33746584767     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060020z     Document Type: Article

References (69)

1. Belyea, J., Gilvey, L. B., Davis, M. F., Godek, M., Sit, T. L., Lommel, S. A., and Franzen, S. (2005) The enzyme function of the globin dehaloperoxidase from Amphitrite ornata is activated by substrate binding, Biochemistry 44, 15637-15644.
2. Franzen, S., Roach, M. P., Chen, Y. P., Dyer, R. B., Woodruff, W. H., and Dawson, J. H. (1998) 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, 4658-4661.
3. LaCount, M. W., Zhang, E. L., Chen, Y. P., Han, K. P., 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.
4. 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.
5. Spiro, T. G., Smulevich, G., and Su, C. (1990) Probing protein structure and dynamics with resonance Raman spectroscopy. Cytochrome c peroxidase and hemoglobin, Biochemistry 29, 4497-4508.
6. Smulevich, G., Hu, S. Z., Rodgers, K. R., Goodin, D. B., Smith, K. M., and Spiro, T. G. (1996) Heme-protein interactions in cytochrome c peroxidase revealed by site-directed mutagenesis and resonance Raman spectra of isotopically labeled hemes, Biospectroscopy 2, 365-376.
7. Yamaguchi, K., Watanabe, Y., and Morishima, I. (1992) Push effect on the heterolytic O-O bond cleavage of peroxoiron(II) porphyrin adducts, Inorg. Chem. 31, 156-157.
8. Nienhaus, K., Olson, J. S., Franzen, S., and Nienhaus, G. U. (2005) The origin of stark splitting in the initial photoproduct state of MbCO, J. Am. Chem. Soc. 127, 40-41.
9. Phillips, G. N., Jr., Teodora, M. L., Li, T., Smith, B., and Olson, J. S. (1999) Bound CO is a molecular probe of the electrostatic potential in the distal pocket of myoglobin, J. Phys. Chem. B 103, 8817-8829.
10. Bonagura, C. A., Bhaskar, B., Shimizu, H., Li, H. Y., Sundaramoorthy, M., McRee, D. E., Goodin, D. B., and Poulos, T. L. (2003) High-resolution crystal structures and spectroscopy of native and compound I cytochrome c peroxidase, Biochemistry 42, 5600-5608.
11. Blair-Johnson, M., Fiedler, T., and Fenna, R. (2001) Human myeloperoxidase: Structure of a cyanide complex and its interaction with bromide and thiocyanate substrates at 1.9 angstrom resolution, Biochemistry 40, 13990-13997.
12. Henriksen, A., Smith, A. T., and Gajhede, M. (1999) 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, 35005-35011.
13. Poulos, T. L., and Kraut, J. (1980) The stereochemistry of peroxidase catalysis, J. Biol. Chem. 255, 8199-8205.
14. Hiner, A. N. P., Raven, E. L., Thorneley, R. N. F., Garcia-Canovas, F., and Rodriguez-Lopez, J. N. (2002) Mechanisms of compound I formation in heme peroxidases, J. Inorg. Biochem. 91, 27-34.
15. Dunford, H. B. (2001) How do enzymes work? Effect of electron circuits on transition state acid dissociation constants, J. Biol. Inorg. Chem. 6, 819-822.
16. Matsui, T., Ozaki, S., Liong, E., Phillips, G. N., 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.
17. Quillin, M. L., Arduini, R. M., Olson, J. S., and Phillips, G. N. (1993) High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin, J. Mol. Biol. 234, 140-155.
18. Ling, J. H., Li, T. S., Olson, J. S., and Bocian, D. F. (1994) Identification of the iron-carbonyl stretch in distal histidine mutants of carbonmonoxymyoglobin, BBA Bioenergetics 1188, 417-421.
19. Balasubramanian, S., Lambright, D. G., and Boxer, S. G. (1993) Perturbations of the distal heme pocket in human myoglobin mutants probed by infrared spectroscopy of bound CO: Correlation with ligand binding kinetics, Proc. Natl. Acad. Sci. U.S.A. 90, 4718-4722.
20. Howes, B. D., Rodriguez-Lopez, J. N., Smith, A. T., and Smulevich, G. (1997) Mutation of distal residues of horseradish peroxidase: Influence on substrate binding and cavity properties, Biochemistry 36, 1532-1543.
21. Newmyer, S. L., and deMontellano, P. R. O. (1996) Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles, J. Biol. Chem. 271, 14891-14896.
22. Newmyer, S. L., Sun, J., Loehr, T. M., and deMontellano, P. R. O. (1996) Rescue of the horseradish peroxidase His-170 → Ala mutant activity by imidazole: Importance of proximal ligand tethering, Biochemistry 35, 12788-12795.
23. Palamakumbura, A. H., Vitello, L. B., and Erman, J. E. (1999) Oxidation of the His-52 → > Leu mutant of cytochrome c peroxidase by p-nitroperoxybenzoic acid: Role of the distal histidine in hydroperoxide activation, Biochemistry 38, 15653-15658.
24. 2 instead of its reduction, J. Am. Chem. Soc. 123, 9260-9263.
25. Meno, K., Jennings, S., Smith, A. T., Henriksen, A., and Gajhede, M. (2002) Structural analysis of the two horseradish peroxidase catalytic residue variants H42E and R38S/H42E: Implications for the catalytic cycle, Acta Crystallogr., Sect. D 58, 1803-1812.
26. Tanaka, M., Ishimori, K., Mukai, M., Kitagawa, T., and Morishima, I. (1997) Catalytic activities and structural properties of horseradish peroxidase distal His42 → Glu or Gln mutant, Biochemistry 36, 9889-9898.
27. Nienhaus, K., Deng, P., Belyea, J., Franzen, S., and Nienhaus, G. U. (2006) Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata, J. Phys. Chem. B, in press.
28. Franzen, S., Jasaitis, A., Belyea, J., Brewer, S., Casey, R., MacFarlane IV, A. W., Stanley, R., Vos, M. H., and Martin, J.-L. (2006) NO-heme geminate recombination dynamics in dehaloperoxidase, J. Phys. Chem. B, in press.
29. Franzen, S. (2002) 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, 13271-13281.
30. Yang, F., and Phillips, G. N., Jr. (1996) Crystal structures of CO-, deoxy- and met-myoglobins at various pH values, J. Mol. Biol. 256, 762-774.
31. Atkins, W. M., and Sligar, S. G. (1989) Molecular recognition in cytochrome P-450: Alteration of regioselective alkane hydroxylation via protein engineering, J. Am. Chem. Soc. 111, 2715-2717.
32. 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. Comm. 324, 1194-1198.
33. Dunford, H. B. (1995) One-electron oxidations by peroxidases, Xenobiotica 25, 725-733.
34. Matsui, T., Ozaki, S., and Watanabe, Y. (1997) On the formation and reactivity of compound I of the His-64 myoglobin mutants, J. Biol. Chem. 272, 32735-32738.
35. Ikedasaito, M., Hori, H., Andersson, L. A., Prince, R. C., Pickering, I. J., George, G. N., Sanders, C. R., Lutz, R. S., McKelvey, E. J., and Mattera, R. (1992) Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants, J. Biol. Chem. 267, 22843-22852.
36. Varadarajan, R., Lambright, D. G., and Boxer, S. G. (1989) Electrostatic interactions in wild-type and mutant recombinant human myoglobins, Biochemistry 28, 3771-3781.
37. Pin, S., Alpert, B., Cortes, R., Ascone, I., Chiu, M. L., and Sligar, S. G. (1994) The heme iron coordination complex in His64(E7)Tyr recombinant sperm whale myoglobin, Biochemistry 33, 11618-11623.
38. Hiner, A. N. P., Hernandez-Ruiz, J., Rodriguez-Lopez, J. N., Arnao, M. B., Varon, R., Garcia-Canovas, F., and Acosta, M. (2001) The inactivation of horseradish peroxidase isoenzyme A2 by hydrogen peroxide: An example of partial resistance due to the formation of a stable enzyme intermediate, J. Biol. Inorg. Chem. 6, 504-516.
39. Vitello, L. B., Erman, J. E., Miller, M. A., Wang, J., and Kraut, J. (1993) Effect of arginine-48 replacement on the reaction between cytochrome c peroxidase and hydrogen peroxide, Biochemistry 32, 9807-9818.
40. Sun, J., Fitzgerald, M. M., Goodin, D. B., and Loehr, T. M. (1997) Solution and crystal structures of the H175G mutant of cytochrome c peroxidase: A resonance Raman study, J. Am. Chem. Soc. 119, 2064-2065.
41. McRee, D. E., Jensen, G. M., Fitzgerald, M. M., Siegel, H. A., and Goodin, D. B. (1994) Construction of a bisaquo heme enzyme and binding by exogenous ligands, Proc. Nat. Acad. Sci. U.S.A. 91, 12847-12851.
42. Hirst, J., Wilcox, S. K., Williams, P. A., Blankenship, J., McRee, D. E., and Goodin, D. B. (2001) Replacement of the axial histidine ligand with imidazole in cytochrome c peroxidase. 1. Effects on structure, Biochemistry 40, 1265-1273.
43. Liu, K., Williams, J., Lee, H. R., Fitzgerald, M. M., Jensen, G. M., Goodin, D. B., and McDermott, A. E. (1998) Solid-state deuterium NMR of imidazole ligands in cytochrome c peroxidase, J. Am. Chem. Soc. 120, 10199-10202.
44. Barrick, D. (1994) Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His 93-Gly, Biochemistry 33, 6546-6554.
45. DePillis, G., Decatur, S. M., Barrick, D., and Boxer, S. G. (1994) Functional cavities in proteins: A general method for proximal ligand subsitution in myoglobin, J. Am. Chem. Soc. 116, 6981-6982.
46. Franzen, S., Boxer, S. G., Dyer, R. B., and Woodruff, W. H. (2000) Resonance Raman studies of heme axial ligation in H93G myoglobin, J. Phys. Chem. B 104, 10359-10367.
47. Franzen, S. (2002) Carbonmonoxy rebinding kinetics in H93G myoglobin: Separation of proximal and distal side effects, J. Phys. Chem. B 106, 4533-4542.
48. Dunford, H. B. (1999) Heme Peroxidases, Wiley-VCH, New York.
49. Harvey, P. J., Floris, R., Lundell, T., Palmer, J. M., Schoemaker, H. E., and Wever, R. (1992) Catalytic mechanisms and regulation of lignin peroxidase, Biochem. Soc. Trans. 20, 345-349.
50. Nicell, J. A., Bewtra, J. K., Biswas, N., and Taylor, E. (1993) Reactor development for peroxidase-catalyzed polymerization and precipitation of phenols from waste-water, Water Res. 27, 1629-1639.
51. Barr, D. P., and Aust, S. D. (1994) Conversion of lignin peroxidase compound-III to active enzyme by cation radicals, Arch. Biochem. Biophys. 312, 511-515.
52. Baynton, K. J., Bewtra, J. K., Biswas, N., and Taylor, K. E. (1994) Inactivation of horseradish peroxidase by phenol and hydrogen peroxide: a kinetic investigation, BBA Prot. Struct. Mol. Enzymol. 1206, 272-278.
53. 2, J. Biol. Chem. 267, 11149-11155.
54. Coulter, E. D., Cheek, J., Ledbetter, A. P., Chang, C. K., and Dawson, J. H. (2000) Preparation and initial characterization of the compound I, II, and III states of iron methylchlorin-reconstituted horseradish peroxidase and myoglobin: Models for key intermediates in iron chlorin enzymes, Biochem. Biophys. Res. Commun. 279, 1011-1015.
55. Hirst, J., Wilcox, S. K., Ai, J. Y., Moenne-Loccoz, P., Loehr, T. M., and Goodin, D. B. (2001) Replacement of the axial histidine ligand with imidazole in cytochrome c peroxidase. 2. Effects on heme coordination and function, Biochemistry 40, 1274-1283.
56. Poulos, T. L., Edwards, S. L., Wariishi, H., and Gold, M. H. (1993) Crystallographic refinement of lignin peroxidase at 2-angstrom, J. Biol. Chem. 268, 4429-4440.
57. Goodin, D. B., and McRee, D. E. (1993) 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, 3313-3324.
58. Franzen, S. (2001) 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, 12578-12589.
59. Belyea, J., Lappi, S., and Franzen, S. A Resonant Raman study of the core size marker modes of dehaloperoxidase from Amphitrite ornata, Biochemistry, submitted for publication.
60. Niaura, G., Reipa, V., Mayhew, M. P., Holden, M., and Vilker, V. L. (2003) Structural alterations of the heme environment of cytochrome P450cam and the Y96F mutant as deduced by resonance Raman spectroscopy, Arch. Biochem. Biophys. 409, 102-112.
61. Nickerson, D. P., Harford-Cross, C. F., Fulcher, S. R., and Wong, L.-L. (1997) The catalytic activity of cytochrome P450cam towards styrene oxidation is increased by site-specific mutagenesis, FEBS Lett. 405, 153-156.
62. Poulos, T. L., Finzel, B. C., and Howard, A. J. (1987) High-resolution crystal structure of cytochrome P450cam, J. Mol. Biol. 195, 687-700.
63. Ator, M. A., and Ortiz de Montellano, P. R. (1987) Protein control of prosthetic heme reactivity reaction of substrates with the heme edge of horseradish peroxidase, J. Biol. Chem. 262, 1542-1551.
64. La Mar, G. N., Hernandez, G. and de Ropp, J. S. (1992) Proton NMR investigation of the influence of interaction sites on the dynamics and thermodynamics of substrate and ligand binding to horseradish peroxidase, Biochemistry 31, 9158-9168.
65. Arnao, M. B., Acosta, M., Delrio, J. A., Varon, R., and Garcia-Canovas, F. (1990) A kinetic study on the suicide inactivation of peroxidase by hydrogen peroxide, Biochim. Biophys. Acta 1041, 43-47.
66. Villegas, J. A., Mauk, A. G., and Vazquez-Duhalt, R. (2000) A cytochrome c variant resistant to heme degradation by hydrogen peroxide, Chem. Biol. 7, 237-244.
67. 2, Biochemistry 41, 11495-11503.
68. Chaudhary, C. (2003) M.S. Thesis, North Carolina State University, Raleigh, NC.
69. Vojtechovsky, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution, Biophys. J. 77, 2153-2174.