Paramagnetic nuclear magnetic resonance relaxation and molecular mechanics studies of the chloroperoxidase-indole complex: Insights into the mechanism of chloroperoxidase-catalyzed regioselective oxidation of indole

Biochemistry

Volumn 52, Issue 21, 2013, Pages 3688-3701

  Zhang, Rui ^a   He, Qinghao ^a   Chatfield, David ^a   Wang, Xiaotang ^a  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGICAL APPLICATIONS; COMPUTATIONAL TECHNIQUE; DISSOCIATION CONSTANT; MAGNETIC RESONANCE RELAXATION; NUCLEAR MAGNETIC RESONANCE(NMR); REGIOSELECTIVE OXIDATION; RELAXATION MEASUREMENTS; VAN DER WAALS INTERACTIONS;

ASSOCIATION REACTIONS; CATALYSIS; CHLORINE COMPOUNDS; DISSOCIATION; HYDROGEN BONDS; IRON COMPOUNDS; MOLECULAR MODELING; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PARAMAGNETISM; PORPHYRINS; REGIOSELECTIVITY; SIMULATED ANNEALING; VAN DER WAALS FORCES;

POLYCYCLIC AROMATIC HYDROCARBONS;

CHLORIDE; CHLORIDE PEROXIDASE; INDOLE DERIVATIVE; IODIDE ION; PYRROLE;

ARTICLE; BINDING SITE; CATALYSIS; CHEMICAL INTERACTION; CHEMICAL MODIFICATION; CONCENTRATION (PARAMETERS); DISSOCIATION CONSTANT; ENZYME ACTIVE SITE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DOCKING; MOLECULAR MECHANICS; NUCLEAR MAGNETIC RESONANCE; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEREOCHEMISTRY; STRUCTURE ACTIVITY RELATION;

CATALYSIS; CHLORIDE PEROXIDASE; HYDROGEN-ION CONCENTRATION; INDOLES; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DOCKING SIMULATION; OXIDATION-REDUCTION;

EID: 84878298319     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4002437     Document Type: Article

References (94)

1. Morris, D. R. and Hager, L. P. (1966) Chloroperoxidase I. Isolation and properties of the crystalline glycoprotein J. Biol. Chem. 241, 1763-1768
2. Sundaramoorthy, M., Terner, J., and Poulos, T. L. (1995) The crystal structure of chloroperoxidase: A heme peroxidase-cytochrome P450 functional hybrid Structure (Oxford, U.K.) 3, 1367-1378
3. Hager, L. P., Morris, D. R., Brown, F. S., and Eberwein, H. (1966) Chloroperoxidase II. Utilization of halogen anions J. Biol. Chem. 241, 1769-1777
4. 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
5. Kedderis, G. L., Koop, D. R., and Hollenberg, P. F. (1980) N -Demethylation reactions catalyzed by chloroperoxidase J. Biol. Chem. 255, 10174-10182
6. Allain, E. J., Hager, L. P., Deng, L., and Jacobsen, E. N. (1993) Highly enantioselective epoxidation of disubstituted alkenes with hydrogen peroxide catalyzed by chloroperoxidase J. Am. Chem. Soc. 115, 4415-4416
7. Carmichael, R., Fedorak, P. M., and Pickard, M. A. (1985) Oxidation of phenols by chloroperoxidase Biotechnol. Lett. 7, 289-294
8. Colonna, S., Gaggero, N., Manfredi, A., Casella, L., Gullotti, M., Carrea, G., and Pasta, P. (1990) Enantioselective oxidations of sulfides catalyzed by chloroperoxidase Biochemistry 29, 10465-10468
9. Corbett, M. D., Baden, D. G., and Chipko, B. R. (1979) Arylamine oxidations by chloroperoxidase Bioorg. Chem. 8, 91-95
10. Geigert, J., Dalietos, D. J., Neidleman, S. L., Lee, T. D., and Wadsworth, J. (1983) Peroxide oxidation of primary alcohols to aldehydes by chloroperoxidase catalysis Biochem. Biophys. Res. Commun. 114, 1104-1108
11. Kiljunen, E. and Kanerva, L. T. (2000) Chloroperoxidase-catalysed oxidation of alcohols to aldehydes J. Mol. Catal. B: Enzym. 9, 163-172
12. Hager, L. P. (2010) A lifetime of playing with enzymes J. Biol. Chem. 285, 14852-14860
13. Hager, L. P., Lakner, F. J., and Basavapathruni, A. (1998) Chiral synthons via chloroperoxidase catalysis J. Mol. Catal. B: Enzym. 5, 95-101
14. Lakner, F. J., Cain, K. P., and Hager, L. P. (1997) Enantioselective epoxidation of ω-bromo-2-methyl-1-alkenes catalyzed by chloroperoxidase. Effect of chain length on selectivity and efficiency J. Am. Chem. Soc. 119, 443-444
15. Lakner, F. J. and Hager, L. P. (1996) Chloroperoxidase as enantioselective epoxidation catalyst: An efficient synthesis of (R)-(-)-mevalonolactone J. Org. Chem. 61, 3923-3925
16. Zaks, A. and Dodds, D. R. (1995) Chloroperoxidase-catalyzed asymmetric oxidations: Substrate specificity and mechanistic study J. Am. Chem. Soc. 117, 10419-10424
17. Dawson, J. H. (1988) Probing structure-function relations in heme-containing oxygenases and peroxidases Science 240, 433-439
18. Dawson, J. H. and Sono, M. (1987) 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, 1255-1276
19. Woggon, W. D., Wagenknecht, H. A., and Claude, C. (2001) Synthetic active site analogues of heme-thiolate proteins: Characterization and identification of intermediates of the catalytic cycles of cytochrome P450cam and chloroperoxidase J. Inorg. Biochem. 83, 289-300
20. Torres, E. and Ayala, M. (2010) Challenges in the application of peroxidases. In Biocatalysis based on heme peroxidases: Peroxidases as potential industrial biocatalysts, pp 209-352, Springer, New York.
21. Sundaramoorthy, M., Terner, J., and Poulos, T. L. (1998) Stereochemistry of the chloroperoxidase active site: Crystallographic and molecular-modeling studies Chem. Biol. 5, 461-473
22. Kühnel, K., Blankenfeldt, W., Terner, J., and Schlichting, I. (2006) Crystal structures of chloroperoxidase with its bound substrates and complexed with formate, acetate, and nitrate J. Biol. Chem. 281, 23990-23998
23. Wang, X. and Goff, H. M. (1997) A nuclear paramagnetic relaxation study of the interaction of the cyclopentanedione substrate with chloroperoxidase Biochim. Biophys. Acta 1339, 88-96
24. Bakhmutov, V. I. (2005) Paramagnetic NMR Relaxation. In Practical nuclear magnetic resonance relaxation for chemists, pp 179-193, Wiley, New York.
25. Otting, G. (2010) Protein NMR using paramagnetic ions Annu. Rev. Biophys. 39, 387-405
26. Modi, S., Primrose, W. U., Boyle, J. M. B., Gibson, C. F., Lian, L. Y., and Roberts, G. C. K. (1995) NMR studies of substrate binding to cytochrome P450 BM3: Comparisons to cytochrome P450cam Biochemistry 34, 8982-8988
27. Solomon, I. (1955) Relaxation processes in a system of two spins Phys. Rev. 99, 559
28. Casella, L., Gullotti, M., Selvaggini, C., Poli, S., Beringhelli, T., and Marchesini, A. (1994) The chloroperoxidase-catalyzed oxidation of phenols. Mechanism, selectivity, and characterization of enzyme-substrate complexes Biochemistry 33, 6377-6386
29. Casella, L., Gullotti, M., Ghezzi, R., Poli, S., Beringhelli, T., Colonna, S., and Carrea, G. (1992) Mechanism of enantioselective oxygenation of sulfides catalyzed by chloroperoxidase and horseradish peroxidase. Spectral studies and characterization of enzyme-substrate complexes Biochemistry 31, 9451-9459
30. Bikiel, D. E., Boechi, L., Capece, L., Crespo, A., De Biase, P. M., Di Lella, S., Lebrero, M. C. G., Martí, M. A., Nadra, A. D., and Perissinotti, L. L. (2006) Modeling heme proteins using atomistic simulations Phys. Chem. Chem. Phys. 8, 5611-5628
31. van Gunsteren, W. F., Dolenc, J., and Mark, A. E. (2008) Molecular simulation as an aid to experimentalists Curr. Opin. Struct. Biol. 18, 149-153
32. Brünger, A. T., Adams, P. D., and Rice, L. M. (1997) New applications of simulated annealing in X-ray crystallography and solution NMR Structure (Oxford, U.K.) 5, 325-336
33. Clore, G. M. and Schwieters, C. D. (2002) Theoretical and computational advances in biomolecular NMR spectroscopy Curr. Opin. Struct. Biol. 12, 146-153
34. Roberts, A. G., Sjögren, S. E. A., Fomina, N., Vu, K. T., Almutairi, A., and Halpert, J. R. (2011) NMR-derived models of amidopyrine and its metabolites complexed to rabbit cytochrome P450 2B4 reveal a structural mechanism of sequential N -dealkylation Biochemistry 50, 2123-2134
35. Roberts, A. G., Yang, J., Halpert, J. R., Nelson, S. D., Thummel, K. T., and Atkins, W. M. (2011) The structural basis for homotropic and heterotropic cooperativity of midazolam metabolism by human cytochrome P450 3A4 Biochemistry 50, 10804-10818
36. Corbett, M. D. and Chipko, B. R. (1979) Peroxide oxidation of indole to oxindole by chloroperoxidase catalysis Biochem. J. 183, 269-276
37. van Deurzen, M. P. J., van Rantwijk, F., and Sheldon, R. A. (1996) Synthesis of substituted oxindoles by chloroperoxidase catalyzed oxidation of indoles J. Mol. Catal. B: Enzym. 2, 33-42
38. Hallenberg, P. F. and Hager, L. P. (1978) Purification of chloroperoxidase from Caldariomyces fumago Methods Enzymol. 52, 521-529
39. Hashimoto, A. and Pickard, M. A. (1984) Chloroperoxidases from caldariomyces (= leptoxyphium) cultures: Glycoproteins with variable carbohydrate content and isoenzymic forms J. Gen. Microbiol. 130, 2051-2058
40. Vold, R. L., Waugh, J. S., Klein, M. P., and Phelps, D. E. (1968) Measurement of spin relaxation in complex systems J. Chem. Phys. 48, 3831-3832
41. Rea, V., Kolkman, A. J., Vottero, E., Stronks, E. J., Ampt, K. A. M., Honing, M., Vermeulen, N. P. E., Wijmenga, S. S., and Commandeur, J. N. M. (2012) Active site substitution A82W improves the regioselectivity of steroid hydroxylation by cytochrome P450 BM3 mutants as rationalized by spin relaxation nuclear magnetic resonance studies Biochemistry 51, 750-760
42. Sakurada, J., Takahashi, S., and Hosoya, T. (1986) Nuclear magnetic resonance studies on the spatial relationship of aromatic donor molecules to the heme iron of horseradish peroxidase J. Biol. Chem. 261, 9657-9662
43. 1 paramagnetic relaxation study Biochemistry 44, 14143-14151
44. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 19, 1639-1662
45. Oostenbrink, C., Villa, A., Mark, A. E., and Van Gunsteren, W. F. (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25, 1656-1676
46. Zong, Q., Osmulski, P. A., and Hager, L. P. (1995) High-pressure-assisted reconstitution of recombinant chloroperoxidase Biochemistry 34, 12420-12425
47. Pickard, M. A. (1981) A defined growth medium for the production of chloroperoxidase by Caldariomyces fumago Can. J. Microbiol. 27, 1298-1305
48. Neese, F. (2012) The ORCA program system Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2, 73-78
49. Head-Gordon, M., Pople, J. A., and Frisch, M. J. (1988) MP2 energy evaluation by direct methods Chem. Phys. Lett. 153, 503-506
50. Weigend, F. and Ahlrichs, R. (2005) Balanced basis sets of split valence, triple ζ valence and quadruple ζ valence quality for H to Rn: Design and assessment of accuracy Phys. Chem. Chem. Phys. 7, 3297-3305
51. Sanner, M. F. (1999) Python: A programming language for software integration and development J. Mol. Graphics Modell. 17, 57-61
52. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4, 435-447
53. Schuttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D60, 1355-1363
54. Lemkul, J. A., Allen, W. J., and Bevan, D. R. (2010) Practical considerations for building GROMOS-compatible small-molecule topologies J. Chem. Inf. Model. 50, 2221-2235
55. Seminario, J. M. (1996) Calculation of intramolecular force fields from second-derivative tensors Int. J. Quantum Chem. 60, 1271-1277
56. Breneman, C. M. and Wiberg, K. B. (1990) Determining atom-centered monopoles from molecular electrostatic potentials. The need for high sampling density in formamide conformational analysis J. Comput. Chem. 361-373
57. Berendsen, H. J. C., Postma, J. P. M., van Gunstetren, W. F., and Hermans, J. (1981) Interaction models for water in relation to protein hydration. In Intermolecular forces, pp 331-342, D. Reidel Publishing Co., Dordrecht, The Netherlands.
58. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
59. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18, 1463-1472
60. van Deurzen, M. P. J., Remkes, I. J., Van Rantwijk, F., and Sheldon, R. A. (1997) Chloroperoxidase catalyzed oxidations in t -butyl alcohol/water mixtures J. Mol. Catal. A: Chem. 117, 329-337
61. Huang, W. C., Westlake, A. C., Maréchal, J. D., Joyce, M. G., Moody, P. C., and Roberts, G. C. (2007) Filling a hole in cytochrome P450 BM3 improves substrate binding and catalytic efficiency J. Mol. Biol. 373, 633-651
62. Constantine, K. L. (2001) Evaluation of site-directed spin labeling for characterizing protein-ligand complexes using simulated restraints Biophys. J. 81, 1275-1284
63. Yue, S. Y. (1990) Distance-constrained molecular docking by simulated annealing Protein Eng. 4, 177-184
64. Pickard, M. A., Kadima, T. A., and Carmichael, R. D. (1991) Chloroperoxidase, a peroxidase with potential J. Ind. Microbiol. Biotechnol. 7, 235-241
65. Manoj, K. M. and Hager, L. P. (2001) Utilization of peroxide and its relevance in oxygen insertion reactions catalyzed by chloroperoxidase Biochim. Biophys. Acta 1547, 408-417
66. Hinman, R. L. and Whipple, E. B. (1962) The protonation of indoles: Position of protonation J. Am. Chem. Soc. 84, 2534-2539
67. Butler, A. and Sandy, M. (2009) Mechanistic considerations of halogenating enzymes Nature 460, 848-854
68. Vaillancourt, F. H., Yeh, E., Vosburg, D. A., Garneau-Tsodikova, S., and Walsh, C. T. (2006) Nature's inventory of halogenation catalysts: Oxidative strategies predominate Chem. Rev. 106, 3364-3378
69. Filizola, M. and Loew, G. H. (2000) Probing the role of protein environment in compound I formation of chloroperoxidase (CPO) J. Am. Chem. Soc. 122, 3599-3605
70. Yi, X., Conesa, A., Punt, P. J., and Hager, L. P. (2003) Examining the role of glutamic acid 183 in chloroperoxidase catalysis J. Biol. Chem. 278, 13855-13859
71. Morozov, A. N. and Chatfield, D. C. (2012) Chloroperoxidase-catalyzed epoxidation of cis -β-methylstyrene: Distal pocket flexibility tunes catalytic reactivity J. Phys. Chem. B 116, 12905-12914
72. 2-promoted oxidation of arylalkanols catalysed by chloroperoxidase Eur. J. Biochem. 268, 665-672
73. Huey, R., Morris, G. M., Olson, A. J., and Goodsell, D. S. (2007) A semiempirical free energy force field with charge-based desolvation J. Comput. Chem. 28, 1145-1152
74. Li, W., Tang, Y., Hoshino, T., and Neya, S. (2009) Molecular modeling of human cytochrome P450 2W1 and its interactions with substrates J. Mol. Graphics Modell. 28, 170-176
75. Gay, S. C., Roberts, A. G., Maekawa, K., Talakad, J. C., Hong, W. X., Zhang, Q., Stout, C. D., and Halpert, J. R. (2010) Structures of cytochrome P450 2B4 complexed with the antiplatelet drugs ticlopidine and clopidogrel Biochemistry 49, 8709-8720
76. Huang, Q., Deshmukh, R. S., Ericksen, S. S., Tu, Y., and Szklarz, G. D. (2012) Preferred binding orientations of phenacetin in CYP 1A1 and 1A2 are associated with isoform-selective metabolism Drug Metab. Dispos. 40, 2324-2331
77. Chen, H., Hirao, H., Derat, E., Schlichting, I., and Shaik, S. (2008) Quantum mechanical/molecular mechanical study on the mechanisms of compound I formation in the catalytic cycle of chloroperoxidase: An overview on heme enzymes J. Phys. Chem. B 112, 9490-9500
78. Wang, X., Tachikawa, H., Yi, X., Manoj, K. M., and Hager, L. P. (2003) Two-dimensional NMR study of the heme active site structure of chloroperoxidase J. Biol. Chem. 278, 7765-7774
79. Manoj, K. M. and Hager, L. P. (2008) Chloroperoxidase, a Janus Enzyme? Biochemistry 47, 2997-3003
80. Morozov, A. N., D'Cunha, C., Alvarez, C. A., and Chatfield, D. C. (2011) Enantiospecificity of chloroperoxidase-catalyzed epoxidation: Biased molecular dynamics study of a cis -β-methylstyrene/chloroperoxidase-compound I complex Biophys. J. 100, 1066-1075
81. Aburto, J., Correa-Basurto, J., and Torres, E. (2008) Atypical kinetic behavior of chloroperoxidase-mediated oxidative halogenation of polycyclic aromatic hydrocarbons Arch. Biochem. Biophys. 480, 33-40
82. Stone, K. L., Behan, R. K., and Green, M. T. (2005) X-ray absorption spectroscopy of chloroperoxidase compound I: Insight into the reactive intermediate of P450 chemistry Proc. Natl. Acad. Sci. U.S.A. 102, 16563-16565
83. Kuhnel, K., Derat, E., Terner, J., Shaik, S., and Schlichting, I. (2007) Structure and quantum chemical characterization of chloroperoxidase compound 0, a common reaction intermediate of diverse heme enzymes Proc. Natl. Acad. Sci. U.S.A. 104, 99-104
84. Porro, C. S., Sutcliffe, M. J., and de Visser, S. P. (2009) Quantum mechanics/molecular mechanics studies on the sulfoxidation of dimethyl sulfide by compound I and compound 0 of cytochrome P450: Which is the better oxidant? J. Phys. Chem. A 113, 11635-11642
85. Rutter, R., Hager, L. P., Dhonau, H., Hendrich, M., Valentine, M., and Debrunner, P. (1984) Chloroperoxidase compound I: Electron paramagnetic resonance and Mössbauer studies Biochemistry 23, 6809-6816
86. Kim, S. H., Perera, R., Hager, L. P., Dawson, J. H., and Hoffman, B. M. (2006) Rapid freeze-quench ENDOR study of chloroperoxidase compound I: The site of the radical J. Am. Chem. Soc. 128, 5598-5599
87. Green, M. T., Dawson, J. H., and Gray, H. B. (2004) Oxoiron(IV) in chloroperoxidase compound II is basic: Implications for P450 chemistry Science 304, 1653-1656
88. Cooper, H. L. R. and Groves, J. T. (2011) Molecular probes of the mechanism of cytochrome P450. Oxygen traps a substrate radical intermediate Arch. Biochem. Biophys. 507, 111-118
89. Tuynman, A., Vink, M. K. S., Dekker, H. L., Schoemaker, H. E., and Wever, R. (2001) The sulphoxidation of thioanisole catalysed by lactoperoxidase and Coprinus cinereus peroxidase: Evidence for an oxygen-rebound mechanism Eur. J. Biochem. 258, 906-913
90. Gross, Z. and Nimri, S. (1995) Seeing the long-sought intermediate in the reaction of oxoiron(IV) porphyrin cation radicals with olefins J. Am. Chem. Soc. 117, 8021-8022
91. Takahashi, A., Kurahashi, T., and Fujii, H. (2011) Redox potentials of oxoiron(IV) porphyrin π-cation radical complexes: Participation of electron transfer process in oxygenation reactions Inorg. Chem. 50, 6922-6928
92. Bukowski, M. R., Koehntop, K. D., Stubna, A., Bominaar, E. L., Halfen, J. A., Münck, E., Nam, W., and Que, L., Jr. (2005) A thiolate-ligated nonheme oxoiron(IV) complex relevant to cytochrome P450 Science 310, 1000-1002
93. Green, M. T. (2009) CH bond activation in heme proteins: The role of thiolate ligation in cytochrome P450 Curr. Opin. Chem. Biol. 13, 84-88
94. Osborne, R. L., Coggins, M. K., Terner, J., and Dawson, J. H. (2007) Caldariomyces fumago chloroperoxidase catalyzes the oxidative dehalogenation of chlorophenols by a mechanism involving two one-electron steps J. Am. Chem. Soc. 129, 14838-14839