Car-parrinello molecular dynamics/molecular mechanics (CPMD/MM) simulation study of coupling and uncoupling mechanisms of cytochrome P450cam

Journal of Physical Chemistry B

Volumn 117, Issue 26, 2013, Pages 7849-7856

  Lian, Peng ^a   Li, Jue ^a   Wang, Dong Qi ^b   Wei, Dong Qing ^a  

^a Shanghai Jiao Tong University   (China)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

C (PROGRAMMING LANGUAGE); CHEMICAL BONDS; CHEMICAL REACTIONS; ENZYMES; PEROXIDES; PROTON TRANSFER;

CAR-PARRINELLO MOLECULAR DYNAMICS; COUPLING REACTION; DELIVERY PATHWAYS; DYNAMICS SIMULATION; SIMULATION STUDIES; TRANSFER PATHWAY; UNCOUPLING MECHANISM; WILD-TYPE ENZYMES;

COMPUTER SIMULATION;

EID: 84879771824     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp312107r     Document Type: Article

References (65)

1. Ortiz de Montellano, P. R., Ed. Cytochrome P450: Structure, Mechanism, and Biochemistry; Klewer Academic/Plenum Publishers: New York, 2005.
2. Dawson, J. H.; Sono, M. Cytochrome P-450 and Chloroperoxidase: Thiolate-Ligated Heme Enzymes. Spectroscopic Determination of Their Active-Site Structures and Mechanistic Implications of Thiolate Ligation Chem. Rev. 1987, 87, 1255-1276
3. Sono, M.; Roach, M. P.; Coulter, E. D.; Dawson, J. H. Heme-Containing Oxygenases Chem. Rev. 1996, 96, 2841-2887
4. Hawkes, D. B.; Adams, G. W.; Burlingame, A. L.; Ortiz de Montellano, P. R.; De Voss, J. J. Cytochrome P450cin (CYP176A), Isolation, Expression, and Characterization J. Biol. Chem. 2002, 277, 27725-27732
5. Denisov, I. G.; Makris, T. M.; Sligar, S. G.; Schlichting, I. Structure and Chemistry of Cytochrome P450 Chem. Rev. 2005, 105, 2253-2277
6. de Visser, S. P.; Valentine, J. S.; Nam, W. A Biomimetic Ferric Hydroperoxo Porphyrin Intermediate Angew. Chem., Int. Ed. 2010, 49, 2099-2101
7. Coon, M. J. Cytochrome P450: Nature's Most Versatile Biological Catalyst Annu. Rev. Pharmacol. Toxicol. 2005, 45, 1-25
8. Guallar, V.; Friesner, R. A. Cytochrome P450CAM Enzymatic Catalysis Cycle: A Quantum Mechanics/Molecular Mechanics Study J. Am. Chem. Soc. 2004, 126, 8501-8508
9. Gunsalus, I. C.; Pederson, T. C.; Sligar, S. G. Oxygenase-Catalyzed Biological Hydroxylations Annu. Rev. Biochem. 1975, 44, 377-407
10. Schlichting, I.; Berendzen, J.; Chu, K.; Stock, A. M.; Maves, S. A.; Benson, D. E.; Sweet, R. M.; Ringe, D.; Petsko, G. A.; Sligar, S. G. The Catalytic Pathway of Cytochrome P450cam at Atomic Resolution Science 2000, 287, 1615-1622
11. Egawa, T.; Shimada, H.; Ishimura, Y. Evidence for Compound I Formation in the Reaction of Cytochrome-P450cam with M-Chloroperbenzoic Acid Biochem. Biophys. Res. Commun. 1994, 201, 1464-1469
12. Kellner, D. G.; Hung, S. C.; Weiss, K. E.; Sligar, S. G. Kinetic Characterization of Compound I Formation in the Thermostable Cytochrome P450 CYP119 J. Biol. Chem. 2002, 277, 9641-9644
13. Rittle, J.; Green, M. T. Cytochrome P450 Compound I: Capture, Characterization, and CH Bond Activation Kinetics Science 2010, 330, 933-937
14. Meunier, B.; de Visser, S. P.; Shaik, S. Mechanism of Oxidation Reactions Catalyzed by Cytochrome P450 Enzymes Chem. Rev. 2004, 104, 3947-3980
15. Shaik, S.; Cohen, S.; Wang, Y.; Chen, H.; Kumar, D.; Thiel, W. P450 Enzymes: Their Structure, Reactivity, and Selectivity-Modeled by QM/MM Calculations Chem. Rev. 2010, 110, 949-1017
16. Liu, J. G.; Ohta, T.; Yamaguchi, S.; Ogura, T.; Sakamoto, S.; Maeda, Y.; Naruta, Y. Spectroscopic Characterization of a Hydroperoxo-Heme Intermediate: Conversion of a Side-On Peroxo to an End-On Hydroperoxo Complex Angew. Chem., Int. Ed. 2009, 48, 9262-9267
17. Newcomb, M.; Shen, R.; Choi, S. Y.; Toy, P. H.; Hollenberg, P. F.; Vaz, A. D. N.; Coon, M. J. Cytochrome P450-Catalyzed Hydroxylation of Mechanistic Probes that Distinguish between Radicals and Cations. Evidence for Cationic but Not for Radical Intermediates J. Am. Chem. Soc. 2000, 122, 2677-2686
18. Vaz, A. D. N.; McGinnity, D. F.; Coon, M. J. Epoxidation of Olefins by Cytochrome P450: Evidence from Site-Specific Mutagenesis for Hydroperoxo-Iron as an Electrophilic Oxidant Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 3555-3560
19. Ogliaro, F.; de Visser, S. P.; Cohen, S.; Sharma, P. K.; Shaik, S. Searching for the Second Oxidant in the Catalytic Cycle of Cytochrome P450: A Theoretical Investigation of the Iron (III)-Hydroperoxo Species and Its Epoxidation Pathways J. Am. Chem. Soc. 2002, 124, 2806-2817
20. Shaik, S.; de Visser, S. P.; Ogliaro, F.; Schwarz, H.; Schroder, D. Two-State Reactivity Mechanisms of Hydroxylation and Epoxidation by Cytochrome P-450 Revealed by Theory Curr. Opin. Chem. Biol. 2002, 6, 556-567
21. Kamachi, T.; Shiota, Y.; Ohta, T.; Yoshizawa, K. Does the Hydroperoxo Species of Cytochrome P450 Participate in Olefin Epoxidation with the Main Oxidant, Compound I? Criticism from Density Functional Theory Calculations Bull. Chem. Soc. Jpn. 2003, 76, 721-732
22. Park, M. J.; Lee, J.; Suh, Y.; Kim, J.; Nam, W. Reactivities of Mononuclear Non-Heme Iron Intermediates including Evidence that Iron(III)-Hydroperoxo Species is a Sluggish Oxidant J. Am. Chem. Soc. 2006, 128, 2630-2634
23. Kumar, D.; Hirao, H.; de Visser, S. P.; Zheng, J. J.; Wang, D. Q.; Thiel, W.; Shaik, S. New Features in the Catalytic Cycle of Cytochrome P450 during the Formation of Compound I from Compound 0 J. Phys. Chem. B 2005, 109, 19946-19951
24. Zheng, J. J.; Wang, D. Q.; Thiel, W.; Shaik, S. QM/MM Study of Mechanisms for Compound I Formation in the Catalytic Cycle of Cytochrome P450cam J. Am. Chem. Soc. 2006, 128, 13204-13215
25. Altarsha, M.; Benighaus, T.; Kumar, D.; Thiel, W. How is the Reactivity of Cytochrome P450cam Affected by Thr252X Mutation? A QM/MM Study for X = Serine, Valine, Alanine, Glycine J. Am. Chem. Soc. 2009, 131, 4755-4763
26. Altarsha, M.; Wang, D.; Benighaus, T.; Kumar, D.; Thiel, W. QM/MM Study of the Second Proton Transfer in the Catalytic Cycle of the D251N Mutant of Cytochrome P450cam J. Phys. Chem. B 2009, 113, 9577-9588
27. Harris, D. L.; Loew, G. H. Theoretical Investigation of the Proton Assisted Pathway to Formation of Cytochrome P450 Compound I J. Am. Chem. Soc. 1998, 120, 8941-8948
28. Hata, M.; Hirano, Y.; Hoshino, T.; Nishida, R.; Tsuda, M. Theoretical Study on Compound I Formation in Monooxygenation Mechanism by Cytochrome P450 J. Phys. Chem. B 2004, 108, 11189-11195
29. Shaik, S.; Kumar, D.; de Visser, S. P.; Altun, A.; Thiel, W. Theoretical Perspective on the Structure and Mechanism of Cytochrome P450 Enzymes Chem. Rev. 2005, 105, 2279-2328
30. Sen, K.; Hackett, J. C. Molecular Oxygen Activation and Proton Transfer Mechanisms in Lanosterol 14a-Demethylase Catalysis J. Phys. Chem. B 2009, 113, 8170-8182
31. Altarsha, M.; Benighaus, T.; Kumar, D.; Thiel, W. Coupling and Uncoupling Mechanisms in the Methoxythreonine Mutant of Cytochrome P450cam: A Quantum Mechanical/Molecular Mechanical Study J. Biol. Inorg. Chem. 2010, 15, 361-372
32. Taraphder, S.; Hummer, G. Protein Side-Chain Motion and Hydration in Proton-Transfer Pathways. Results for Cytochrome P450cam J. Am. Chem. Soc. 2003, 125, 3931-3940
33. Vidakovic, M.; Sligar, S.; Li, H.; Poulos, T. Understanding the Role of the Essential Asp251 in Cytochrome P450cam Using Site-Directed Mutagenesis, Crystallography, and Kinetic Solvent Isotope Effect Biochemistry 1998, 37, 9211-9219
34. Agmon, N. The Grotthuss Mechanism Chem. Phys. Lett. 1995, 244, 456-462
35. Schoneboom, J. C.; Lin, H.; Reuter, N.; Thiel, W.; Cohen, S.; Ogliaro, F.; Shaik, S. The Elusive Oxidant Species of Cytochrome P450 Enzymes: Characterization by Combined Quantum Mechanical/Molecular Mechanical (QM/MM) Calculations J. Am. Chem. Soc. 2002, 124, 8142-8151
36. Schoneboom, J. C.; Thiel, W. The Resting State of P450cam: A QM/MM Study J. Phys. Chem. B 2004, 108, 7468-7478
37. Altun, A.; Thiel, W. Combined Quantum Mechanical/Molecular Mechanical Study on the Pentacoordinated Ferric and Ferrous Cytochrome P450cam Complexes J. Phys. Chem. B 2005, 109, 1268-1280
38. Wang, D.; Zheng, J.; Shaik, S.; Thiel, W. Quantum and Molecular Mechanical Study of the First Proton Transfer in the Catalytic Cycle of Cytochrome P450cam and Its Mutant D251N J. Phys. Chem. B 2008, 112, 5126-5138
39. Koster, A. M.; Flores-Moreno, R.; Geudtner, G.; Goursot, A.; Heine, T.; Reveles, J. U.; Vela, A.; Salahub, D. R. deMon 2003 Code; NRC: Ottawa, Canada, 2003.
40. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; Hermans, J. Interaction Models for Water in Relation to Protein Hydration. In Intermolecular Forces; Pullman, B., Ed.; D. Reidel Publishing Company: Dordrecht, The Netherlands, 1981; pp 331-342.
41. Oprea, T. I.; Hummer, G.; García, A. E. Identification of a Functional Water Channel in Cytochrome P450 Enzymes Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 2133-2138
42. Becke, A. D. Density-Functional Exchange-Energy Approximation with Correct Asymptotic Behavior Phys. Rev. A 1988, 38, 3098-3100
43. Vanderbilt, D. Soft Self-Consistent Pseudopotentials in a Generalized Eigenvalue Formalism Phys. Rev. B 1990, 41, 7892-7895
44. Laasonen, K.; Car, R.; Lee, C.; Vanderbilt, D. Implementation of Ultrasoft Pseudopotentials in Ab Initio Molecular Dynamics Phys. Rev. B 1991, 43, 6796-6799
45. Laasonen, K.; Pasquarello, A.; Car, R.; Lee, C.; Vanderbilt, D. Car-Parrinello Molecular Dynamics with Vanderbilt Ultrasoft Pseudopotentials Phys. Rev. B 1993, 47, 10142-10153
46. Jorgensen, W. L.; Tirado-Rives, J. The OPLS Force Field for Proteins. Energy Minimizations for Crystals of Cyclic Peptides and Crambin J. Am. Chem. Soc. 1988, 110, 1657-1666
47. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and Testing of the OPLS All-Atom Force Field on Conformational Energetics and Properties of Organic Liquids J. Am. Chem. Soc. 1996, 118, 11225-11236
48. Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. GROMACS: A Message-Passing Parallel Molecular Dynamics Implementation Comput. Phys. Commun. 1995, 91, 43-56
49. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A Package for Molecular Simulation and Trajectory Analysis J. Mol. Model. 2001, 7, 306-317
50. van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718
51. Biswas, P. K.; Gogonea, V. A Regularized and Renormalized Electrostatic Coupling Hamiltonian for Hybrid Quantum-Mechanical-Molecular-Mechanical Calculations J. Chem. Phys. 2005, 123, 164114-164122
52. Das, D.; Eurenius, K. P.; Billings, E. M.; Sherwood, P.; Chatfield, D. C.; Hodoscek, M.; Brooks, B. R. Optimization of Quantum Mechanical Molecular Mechanical Partitioning Schemes: Gaussian Delocalization of Molecular Mechanical Charges and the Double Link Atom Method J. Chem. Phys. 2002, 117, 10534-10547
53. Hestenes, M. R.; Stiefel, E. Methods of Conjugate Gradients for Solving Linear Systems J. Res. Natl. Bur. Stand. 1952, 49, 409-436
54. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684-3690
55. Car, R.; Parrinello, M. Unified Approach for Molecular-Dynamics and Density-Functional Theory Phys. Rev. Lett. 1985, 55, 2471-2474
56. Kamachi, T.; Yoshizawa, K. A Theoretical Study on the Mechanism of Camphor Hydroxylation by Compound I of Cytochrome P450 J. Am. Chem. Soc. 2003, 125, 4652-4661
57. Glendening, E. D.; Reed, A. E.; Carpenter, J. E.; Weinhold, F. NBO Version 3.1.
58. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Gaussian 09, revision A.1; Gaussian, Inc.: Wallingford CT, 2009.
59. Sharma, P. K.; Kevorkiants, R.; de Visser, S. P.; Kumar, D.; Shaik, S. Porphyrin Traps Its Terminator! Concerted and Stepwise Porphyrin Degradation Mechanisms Induced by Heme-Oxygenase and Cytochrome P450 Angew. Chem. 2004, 116, 1149-1152
60. Derat, E.; Kumar, D.; Hirao, H.; Shaik, S. Gauging the Relative Oxidative Powers of Compound I, Ferric-Hydroperoxide, and the Ferric-Hydrogen Peroxide Species of Cytochrome P450 toward CH Hydroxylation of a Radical Clock Substrate J. Am. Chem. Soc. 2006, 128, 473-484
61. Shimada, H.; Makino, R.; Imai, M.; Horiuchi, T.; Ishimura, Y. Mechanism of Oxygen Activation by Cytochrome P-450cam. International Symposium on Oxygenases and Oxygen Activation: Yamada Conference XXVII, 1990, Osaka, Japan.
62. Gerber, N. C.; Sligar, S. G. Catalytic Mechanism of Cytochrome P-450: Evidence for a Distal Charge Relay J. Am. Chem. Soc. 1992, 114, 8742-8743
63. Hishik, T.; Shimada, H.; Nagano, S.; Egawa, T.; Kanamori, Y.; Makino, R.; Park, S. Y.; Adachi, S.; Shiro, Y.; Ishimura, Y. X-ray Crystal Structure and Catalytic Properties of Thr252Ile Mutant of Cytochrome P450cam: Roles of Thr252 and Water in the Active Center J. Biochem. 2000, 128, 965-974
64. Imai, M.; Shimada, H.; Watanabe, Y.; Matsushima-Hibiya, Y.; Makino, R.; Koga, H.; Horiuchi, T.; Ishimura, Y. Uncoupling of the Cytochrome P-450cam Monooxygenase Reaction by a Single Mutation, Threonine-252 to Alanine or Valine: Possible Role of the Hydroxy Amino Acid in Oxygen Activation Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 7823-7827
65. Kimata, Y.; Shimada, H.; Hirose, T.; Ishimura, Y. Role of Thr-252 in Cytochrome P450(Cam): A Study with Unnatural Amino-Acid Mutagenesis Biochem. Biophys. Res. Commun. 1995, 208, 96-102