External electric field can control the catalytic cycle of cytochrome P450cam: A QM/MM study

Journal of Physical Chemistry Letters

Volumn 1, Issue 14, 2010, Pages 2082-2087

  Lai, Wenzhen ^a   Chen, Hui ^a   Cho, Kyung Bin ^a,b   Shaik, Sason ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b Ewha Womans University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SPECIES; BOND ACTIVATION REACTIONS; CATALYTIC CYCLES; CYTOCHROME P450; EXTERNAL ELECTRIC FIELD; RATE DETERMINING STEP; RESTING STATE; SPIN-STATE; SYSTEMATIC STUDY;

CHEMICAL ACTIVATION; ELECTRIC FIELDS; ELECTRONIC STRUCTURE; PORPHYRINS;

CAMS;

EID: 77954756366     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz100695n     Document Type: Article

References (50)

1. Ortiz de Montellano, P. R., Ed. Cytochrome P450: Structure, Mechanism, and Biochemistry, 3 rd ed.; Kluwer Academic/Plenum Publisher: New York, 2005.
2. Sono, M.; Roach, M. P.; Coulter, E. D.; Dawson, J. H. Heme-Containing Oxygenases Chem. Rev. 1996, 96, 2841-2887
3. Denisov, I. G.; Makris, T. M.; Sligar, S. G.; Schlichting, I. Structure and Chemistry of Cytochrome P450 Chem. Rev. 2005, 105, 2253-2277
4. 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
5. Sligar, S. G. Coupling of Spin, Substrate, and Redox Equilibria in Cytochrome P450 Biochemistry 1976, 15, 5399-5406
6. Ogliaro, F.; Cohen, S.; de Visser, S. P.; Shaik, S. Medium Polarization and Hydrogen Bonding Effects on Compound I of Cytochrome P450: What Kind of a Radical Is It Really? J. Am. Chem. Soc. 2000, 122, 12892-12893
7. Shaik, S.; Hirao, H.; Kumar, D. Reactivity of High-Valent Iron-Oxo Species in Enzymes and Synthetic Reagents: A Tale of Many States Acc. Chem. Res. 2007, 40, 532-542
8. Shaik, S.; Filatov, M.; Schröder, D.; Schwarz, H. Electronic Structure Makes a Difference: Cytochrome P450 Mediated Hydroxylations of Hydrocarbons as a Two-State Reactivity Paradigm Chem.-Eur. J. 1998, 4, 193-199
9. +. Selection Rules and Reactivity Effects J. Am. Chem. Soc. 1997, 119, 1773-1786. The state energy gap affects the spin flip probability since it affects the relative slopes of the states at their intersection points
10. 6 2.
11. 2 couple to a singlet.
12. Harada, A.; Kataoka, K. Switching by Pulse Electric Field of the Elevated Enzymatic Reaction in the Core of Polyion Complex Micelles J. Am. Chem. Soc. 2003, 125, 15306-15307
13. Giuseppone, N.; Lehn, J.-M. Electric-Field Modulation of Component Exchange in Constitutional Dynamic Liquid Crystals Angew. Chem., Int. Ed. 2006, 45, 4619-4624
14. de Biase, P. M.; Paggi, D. A.; Doctorovich, F.; Hildebrandt, P.; Estrin, D. A.; Murgida, D. H.; Marti, M. A. Molecular Basis for the Electric Field Modulation of Cytochrome c Structure and Function J. Am. Chem. Soc. 2009, 131, 16248-16256
15. Murgida, D. H.; Hildebrandt, P. Electron-Transfer Processes of Cytochrome c at Interfaces. New Insights by Surface-Enhanced Resonance Raman Spectroscopy Acc. Chem. Res. 2004, 37, 854-861
16. Kranich, A.; Ly, H. K.; Hildebrandt, P.; Murgida, D. H. Direct Observation of the Gating Step in Protein Electron Transfer: Electric-Field-Controlled Protein Dynamics J. Am. Chem. Soc. 2008, 130, 9844-9848
17. Alemany, M.; Peters, M. V.; Hecht, S.; Rieder, K.-H.; Moresco, F.; Grill, L. Electric Field-Induced Isomerization of Azobenzene by STM J. Am. Chem. Soc. 2006, 128, 14446-14447
18. Shaik, S.; de Visser, S. P.; Kumar, D. External Electric Field Will Control the Selectivity of Enzymatic-Like Bond Activations J. Am. Chem. Soc. 2004, 126, 11746-11749
19. de Visser, S. P. What External Perturbations Influence the Electronic Properties of Catalase Compound I? Inorg. Chem. 2006, 45, 9551-9557
20. Hirao, H.; Chen, H.; Carvajal, M. A.; Wang, Y.; Shaik, S. Effect of External Electric Fields on the C-H Bond Activation Reactivity of Nonheme Iron-Oxo Reagents J. Am. Chem. Soc. 2008, 130, 3319-3327
21. cam: A QM/MM Study J. Phys. Chem. B 2004, 108, 7468-7478
22. cam Complexes J. Phys. Chem. B 2005, 109, 1268-1280
23. cam in Quantum Mechanical/Molecular Mechanical Studies J. Comput. Chem. 2007, 28, 2147-2158
24. Wang, D. Q.; Thiel, W. The Oxyheme Complexes of P450cam: A QM/MM Study J. Mol. Struct.: THEOCHEM 2009, 898, 90-96
25. 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
26. Schöneboom, 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
27. 2 Bonding in Oxy-Myoglobin: The Effect of the Protein J. Am. Chem. Soc. 2008, 130, 14778-14790
28. Schöneboom, J. C.; Neese, F.; Thiel, W. Toward Identification of the Compound I Reactive Intermediate in Cytochrome P450 Chemistry: A QM/MM Study of Its EPR and Mössbauer Parameters J. Am. Chem. Soc. 2005, 127, 5840-5853
29. Cho, K.-B.; Hirao, H.; Chen, H.; Carvajal, M. A.; Cohen, S.; Derat, E.; Thiel, W.; Shaik, S. Compound I in Heme Thiolate Enzymes: A Comparative QM/MM Study J. Phys. Chem. A 2008, 112, 13128-13138
30. Clarke, R. J. The Dipole Potential of Phospholipid Membranes and Methods for Its Detection Adv. Colloid Interface Sci. 2001, 89, 263-281
31. Rovira, C.; Kunc, K.; Hutter, J.; Ballone, P.; Parrinello, M. Equilibrium Geometries and Electronic Structure of Iron-Porphyrin Complexes: A Density Functional Study J. Phys. Chem. A 1997, 101, 8914-8925
32. 2 Binds to Heme J. Biol. Chem. 2004, 279, 14561-14569
33. Strickland, N.; Harvey, J. N. Spin-Forbidden Ligand Binding to the Ferrous-Heme Group: Ab Initio and DFT Studies J. Phys. Chem. B 2007, 111, 841-852
34. Weiss, J. J. Nature of the Iron-Oxygen Bond in Oxyhamoglobin Nature 1964, 202, 83-84
35. McClure, D. S. Electronic Structure of Transition-Metal Complex Ions Radiation. Res. Suppl. 1960, 2, 218-242
36. cam Biochemistry 1997, 36, 5104-5107
37. Wallrapp, F.; Masone, D.; Guallar, V. Electron Transfer in the P450cam/PDX Complex. The QM/MM e-Pathway J. Phys. Chem. A 2008, 112, 12989-12994
38. Ullrich, V. Cytochrome P450 and Biological Hydroxylation Reactions Top. Curr. Chem. 1979, 83, 67-104
39. Ogliaro, F.; de Visser, S. P.; Groves, J. T.; Shaik, S. Chameleon States: High-Valent Metal-Oxo Species of Cytochrome P450 and Its Ruthenium Analogue Angew. Chem., Int. Ed. 2001, 40, 2874-2878
40. See assembly of metalloporphyrins in a controllable orientation to an electrified surface: Ashkenasy, G.; Kalyuzhny, G.; Libman, J.; Rubinstein, I.; Shanzer, A. Functional Monolayers with Coordinatively Embedded Metalloporphyrins Angew. Chem., Int. Ed. 1999, 38, 1257-1261
41. Kijac, A. Z.; Li, Y.; Sligar, S. G.; Rienstra, C. M. Magic-Angle Spinning Solid-State NMR Spectroscopy of Nanodisc-Embedded Human CYP3A4 Biochemistry 2007, 46, 13696-13703. Note (as proposed by Sligar) that charged lipids can be embedded into the nanodiscs and generate large local fields.
42. Choi, Y.; Yau, S.-T. Field-Effect Enzymatic Amplifying Detector with Picomolar Detection Limit Anal. Chem. 2009, 81, 7123-7126
43. Murase, T.; Horiuchi, S.; Fujita, M. Naphthalene Diels-Alder in a Self-Assembled Molecular Flask J. Am. Chem. Soc. 2010, 132, 2866-2867
44. 2-SAM), which can link to the surface lysines. At the same time, the reductase will be coordinate to the side of Cys357. For such strategies, see ref 15 herein.
45. Sherwood, P.; de Vries, A. H.; Guest, M. F.; Schreckenbach, G.; Catlow, C. R. A.; French, S. A.; Sokol, A. A.; Bromley, S. T.; Thiel, W.; Turner, A. J. QUASI: A General Purpose Implementation of the QM/MM Approach and Its Application to Problems in Catalysis J. Mol. Struct.: THEOCHEM 2003, 632, 1-28
46. Ahlrichs, R.; Bär, M.; Häser, M.; Horn, H.; Kölmel, C. Electronic Structure Calculations on Workstation Computers: The Program System Turbomole Chem. Phys. Lett. 1989, 162, 165-169
47. Smith, W.; Forester, T. R. DL-POLY-2.0: A General-Purpose Parallel Molecular Dynamics Simulation Package J. Mol. Graph. 1996, 14, 136-141
48. Becke, A. D. Density-Functional Thermochemistry. III. The Role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
49. Mackerell, A. D., Jr.; Bashford, D.; Bellott, M.; Dunbrack, R. L., Jr.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
50. Wachters, A. J. H. Gaussian Basis Set for Molecular Wavefuncitons Containing Third-Row Atoms J. Chem. Phys. 1970, 52, 1033-1036