Solute solvent dynamics and energetics in enzyme catalysis: The S N2 reaction of dehalogenase as a general benchmark

Journal of the American Chemical Society

Volumn 126, Issue 46, 2004, Pages 15167-15179

  Olsson, Mats H M ^a   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; MOLECULAR DYNAMICS; ORGANIC SOLVENTS; PHASE TRANSITIONS; SOLUTIONS; SULFUR COMPOUNDS;

ENZYME CATALYSIS; HALOALKAN DEHALOGENASE (DHLA); SOLUTE SOLVENT DYNAMICS; TRANSITION STATES;

ENZYMES;

ALKANE; HALOALKANE DEHALOGENASE; HALOGENATED HYDROCARBON; HYDROLASE; SOLVENT; UNCLASSIFIED DRUG; WATER;

ARTICLE; CATALYSIS; DYNAMICS; ENERGY TRANSFER; MOLECULAR MECHANICS; QUANTUM MECHANICS; SOLUTE; SOLVATION; XANTHOBACTER;

CATALYSIS; COMPUTER SIMULATION; ENZYME ACTIVATION; HYDROLASES; KINETICS; MODELS, CHEMICAL; SOLUTIONS; THERMODYNAMICS; XANTHOBACTER;

EID: 9344245168     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja047151c     Document Type: Article

References (79)

1. Borman, S. Much ado about enzyme mechanisms. Chem. Eng. News 2004, 82, 35-39.
2. Warshel, A. Computer Modeling of Chemical Reactions in Enzymes and Solutions; John Wiley & Sons: New York, 1991.
3. Villà, J.; Warshel, A. Energetics and dynamics of enzymatic reactions. J. Phys. Chem. B 2001, 105, 7887-7907.
4. Warshel, A. Energetics of Enzyme Catalysis. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 5250-5254.
5. Cannon, W. R.; Benkovic, S. J. Solvation, reorganization energy, and biological catalysis. J. Biol. Chem. 1998, 273, 26257-26260.
6. Roca, M.; Marti, S.; Andres, J., et al. Theoretical modeling of enzyme catalytic power: Analysis of "cratic" and electrostatic factors in catechol O-methyltransferase. J. Am. Chem. Soc. 2003, 125, 7726-7737.
7. Shaik, S. S.; Schlegel, H. B.; Wolfe, S. Theoretical Aspects of Physical Organic Chemistry. Application to the SN2 Transition State; Wiley-Interscience: New York, 1992.
8. N2 Reactions in Polar-Solvents. J. Chem. Phys. 1987, 86, 1377-1386.
9. N2 Reactions in Water. J. Chem. Phys. 1989, 90, 3537-3558.
10. N2 Reactions in Aqueous-Solution. J. Am. Chem. Soc. 1988, 110, 5297-5311.
11. Lau, E. Y.; Kahn, K.; Bash, P. A.; Bruice, T. C. The importance of reactant positioning in enzyme catalysis: A hybrid quantum mechanics/molecular mechanics study of a haloalkane dehalogenase. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 9937-9942.
12. Bruice, T. C. A view at the millennium: The efficiency of enzymatic catalysis. Acc. Chem. Res. 2002, 35, 139-148.
13. N2 displacement reaction. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 8417-8420.
14. Shurki, A.; Strajbl, M.; Villa, J.; Warshel, A. How much do enzymes really gain by restraining their reacting fragments? J. Am. Chem. Soc. 2002, 124, 4097-4107.
15. Dewar, M. J. S.; Storch, D. M. Alternative View of Enzyme-Reactions. Proc. Natl Acad. Sci. U.S.A. 1985, 82, 2225-2229.
16. Warshel, A.; Strajbl, M.; Villa, J.; Florian, J. Remarkable rate enhancement of orotidine 5′-monophosphate decarboxylase is due to transition-state stabilization rather than to ground-state destabilization. Biochemistry 2000, 39, 14728-14738.
17. Jencks, W. P. Catalysis in Chemistry and Enzymology; Dover: New York, 1987.
18. Aqvist, J.; Luecke, H.; Quiocho, F. A.; Warshel, A. Dipoles Localized at Helix Termini of Proteins Stabilize Charges. Proc. Natl Acad. Sci. U.S.A. 1991, 88, 2026-2030.
19. Warshel, A.; Åqvist, J.; Creighton, S. Enzymes Work by Solvation Substitution Rather Than by Desolvation. Proc. Nat. Acad. Sci. U.S.A. 1989, 86, 5820-5824.
20. Devi-Kesavan, L. S.; Gao, J. L. Combined QM/MM study of the mechanism and kinetic isotope effect of the nucleophilic substitution reaction in haloalkane dehalogenase. J. Am. Chem. Soc. 2003, 125, 1532-1540.
21. Kohen, A.; Cannio, R.; Bartolucci, S.; Klinman, J. P. Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 1999, 399, 496-499.
22. Basran, J.; Sutcliffe, M. J.; Scrutton, N. S. Enzymatic H-transfer requires vibration-driven extreme tunneling. Biochemistry 1999, 38, 3218-3222.
23. Wilson, E. K. Enzyme dynamics. Chem. Eng. News 2000, 78, 42-45.
24. Berendsen, H. J. C.; Hayward, S. Collective protein dynamics in relation to function. Curr. Opin. Struct. Biol. 2000, 10, 165-169.
25. Cameron, C. E.; Benkovic, S. J. Evidence for a functional role of the dynamics of glycine-121 of Escherichia coli dihydrofolate reductase obtained from kinetic analysis of a site-directed mutant. Biochemistry 1997, 36, 15792-15800.
26. Cannon, W. R.; Singleton, S. F.; Benkovic, S. J. A perspective on biological catalysis. Nat. Struct. Biol. 1996, 3, 821-833.
27. Careri, G.; Fasella, P.; Gratton, E. Enzyme Dynamics - Statistical Physics Approach. Ann. Rev.f Biophys. Bioeng. 1979, 8, 69-97.
28. Karplus, M.; McCammon, J. A. Dynamics of Proteins - Elements and Function. Ann. Rev. Biochem. 1983, 52, 263-300.
29. Kurzynski, M. Importance of intramolecular protein dynamics to kinetics of biochemical processes. Cell. Mol. Biol. Lett. 1999, 4, 117-130.
30. Radkiewicz, J. L.; Brooks, C. L. Protein dynamics in enzymatic catalysis: Exploration of dihydrofolate reductase. J. Am. Chem. Soc. 2000, 122, 225-231.
31. Daniel, R. M.; Dunn, R. V.; Finney, J. L.; Smith, J. C. The role of dynamics in enzyme activity. Ann. Rev. Biophys. Biomol. Struct. 2003, 32, 69-92.
32. Warshel, A.; Sussman, F.; Hwang, J. K. Evaluation of Catalytic Free-Energies in Genetically Modified Proteins. J. Mol. Biol. 1988, 201, 139-159.
33. Warshel, A. Dynamics of Enzymatic-Reactions. Proc. Nat. Acad. Sci. U.S.A.-Biol. Sci. 1984, 81, 444-448.
34. Neria, E.; Karplus, M. Molecular dynamics of an enzyme reaction: Proton transfer in TIM. Chem. Phys. Lett. 1997, 267, 23-30.
35. Billeter, S. R.; Webb, S. P.; Agarwal, P. K.; Iordanov, T.; Hammes-Schiffer, S. Hydride transfer in liver alcohol dehydrogenase: Quantum dynamics, kinetic isotope effects, and role of enzyme motion. J. Am. Chem. Soc. 2001, 123, 11262-11272.
36. Nam, K.; Prat-Resina, X.; Garcia-Viloca, M.; Devi-Kesavan, L. S.; Gao, J. L. Dynamics of an enzymatic substitution reaction in haloalkane dehalogenase. J. Am. Chem. Soc. 2004, 126, 1369-1376.
37. Warshel, A.; Levitt, M. Theoretical Studies of Enzymic Reactions - Dielectric, Electrostatic and Steric Stabilization of Carbonium-Ion in Reaction of Lysozyme. J. Mol. Biol. 1976, 103, 227-249.
38. Gao, J. L. Hybrid quantum and molecular mechanical simulations: An alternative avenue to solvent effects in organic chemistry. Acc. Chem. Res. 1996, 29, 298-305.
39. Field, M. J.; Bash, P. A.; Karplus, M. A Combined Quantum-Mechanical and Molecular Mechanical Potential for Molecular-Dynamics Simulations. J. Comput. Chem. 1990, 11, 700-733.
40. Friesner, R. A.; Beachy, M. D. Quantum mechanical calculations on biological systems. Curr. Opin. Struct. Biol. 1998, 8, 257-262.
41. Monard, G.; Merz, K. M. Combined quantum mechanical/molecular mechanical methodologies applied to biomolecular systems. Acc. Chem. Res. 1999, 32, 904-911.
42. Field, M. J. Simulating enzyme reactions: Challenges and perspectives. J. Comput. Chem. 2002, 23, 48-58.
43. Cui, Q.; Elstner, M.; Kaxiras, E.; Frauenheim, T.; Karplus, M. A QM/MM implementation of the self-consistent charge density functional tight binding (SCC-DFTB) method. J. Phys. Chem. B 2001, 105, 569-585.
44. Shurki, A.; Warshel, A. Structure/function correlations of proteins using MM, QM/MM, and related approaches: current progress. Adv. Protein Chem. 2003, 66, 249-313.
45. Aqvist, J.; Warshel, A. Simulation of Enzyme-Reactions Using Valence-Bond Force-Fields and Other Hybrid Quantum-Classical Approaches. Chem. Rev. 1993, 93, 2523-2544.
46. Hwang, J. K.; Creighton, S.; King, G.; Whitney, D.; Warshel, A. Effects of Solute Solvent Coupling and Solvent Saturation on Solvation Dynamics of Charge-Transfer Reactions. J. Chem. Phys. 1988, 89, 859-865.
47. King, G.; Warshel, A. Investigation of the Free Energy Functions for Electron Transfer Reactions. J. Chem. Phys. 1990, 93, 8682-8692.
48. Marcus, R. A. Chemical and electrochemical electron transfer theory. Ann. Rev. Phys. Chem. 1964, 15, 155-196.
49. Marcus, R. A. Electron-Transfer Reactions in Chemistry - Theory and Experiment (Nobel Lecture). Angew. Chem., Inte. Ed. Engl. 1993, 32, 1111-1121.
50. Shurki, A.; Warshel, A. Structure/Function Correlations of Protreins using MM, QM/MM and Related Approaches; Methods, Concepts, Pitfalls and Current Progress. Adv. Protein Chem. 2003, 66, 249-312.
51. Lee, F. S.; Chu, Z. T.; Bolger, M. B.; Warshel, A. Calculations of Antibody-Antigen Interactions: Microscopic and Semi-Microscopic Evaluation of the Free Energies of Binding of Phosphorylcholine Analogues to McPC603. Prot. Eng. 1992, 5, 215-228.
52. Florian, J.; Goodman, M. F.; Warshel, A. Theoretical Investigation of the Binding Free Energies and Key Substrate-Recognition Components of the Replication Fidelity of Human DNA Polymerase β. J. Phys. Chem. B 2002, 106, 5739-5753.
53. Keck, J. C. Variational theory of reaction rates. Adv. Chem. Phys. 1966, 13, 85-121.
54. Anderson, J. B. Statistical theoreticals of chemical reactions. Distributions in the transition region. J. Chem. Phys. 1973, 58, 4684-4692.
55. Bennett, C. H. Molecular dynamics and transition state theory: the simulation of infrequent events. In Algorithms for chemical computations; Christofferson, R. E., Ed.; American Chemical Society: Washington, DC, 1977; pp 63-97.
56. Chandler, D. Statistical-Mechanics of Isomerization Dynamics in Liquids and Transition-State Approximation. J. Chem. Phys. 1978, 68, 2959-2970.
57. Cline, R. E.; Wolynes, P. G. Stochastic Dynamic-Models of Curve Crossing Phenomena in Condensed Phases. J. Chem. Phys. 1987, 86, 3836-3844.
58. Straub, J. E.; Berne, B. J. A Rapid Method for Determining Rate Constants by Molecular-Dynamics. J. Chem. Phys. 1985, 83, 1138-1139.
59. Grimmelmann, E. K.; Tully, J. C.; Helfand, E. Molecular-Dynamics of Infrequent Events - Thermal-Desorption of Xenon from a Platinum Surface. J. Chem. Phys. 1981, 74, 5300-5310.
60. Warshel, A.; Parson, W. W. Dynamics of biochemical and biophysical reactions: insight from computer simulations. Quart. Rev. Biophys. 2001, 34, 563-679.
61. Bentzien, J.; Muller, R. P.; Florian, J.; Warshel, A. Hybrid ab initio quantum mechanics molecular mechanics calculations of free energy surfaces for enzymatic reactions: The nucleophilic attack in subtilisin. J. Phys. Chem. B 1998, 102, 2293-2301.
62. Kubo, R. The fluctuation-dissipation theorem. Rep. Prog. Phys. 1966, 29, 255-284.
63. Warshel, A.; Hwang, J. K. Simulation of the Dynamics of Electron-Transfer Reactions in Polar-Solvents - Semiclassical Trajectories and Dispersed Polaron Approaches. J. Chem. Phys. 1986, 84, 4938-4957.
64. Lee, F. S.; Chu, Z. T.; Warshel, A. Microscopic and Semimicroscopic Calculations of Electrostatic Energies in Proteins by the Polaris and Enzymix Programs. J. Comput. Chem. 1993, 14, 161-185.
65. King, G.; Warshel, A. A Surface Constrained All-Atom Solvent Model for Effective Simulations of Polar Solutions. Jo. Chem. Phys. 1989, 91, 3647-3661.
66. Verschueren, K. H. G.; Seljee, F.; Rozeboom, H. J.; Kalk, K. H.; Dijkstra, B. W. Crystallographic Analysis of the Catalytic Mechanism of Haloalkane Dehalogenase. Nature 1993, 363, 693-698.
67. Swain, C. G.; Scott, C. B. Qualitative correlation of relative rates. Comparison of hydroxide ion with other nucleophilic reagents toward alkyl halides, esters, epoxides and acyl halides. J. Am. Chem. Soc. 1953, 75, 141-147.
68. - group.
69. - group.
70. Crosby, J.; Stone, R.; Lienhard, G. E. Mechanisms of Thiamine-Catalyzed Reactions. Decarboxylation of 2-(1-Carboxy-1-hydroxyethyl)-3,4- dimethylthiazolium Chloride. J. Am. Chem. Soc. 1970, 92, 2891-2900.
71. Guimaraes, C. R. W.; Repasky, M. P.; Chandrasekhar, J.; Tirado-Rives, J.; Jorgensen, W. L. Contributions of conformational compression and preferential transition state stabilization to the rate enhancement by chorismate mutase. J. Am. Chem. Soc. 2003, 125, 6892-6899.
72. Marti, S.; Andres, J.; Moliner, V.; Silla, E.; Tunon, I.; Bertran, J. Transition structure selectivity in enzyme catalysis: a QM/MM study of chorismate mutase. Theor. Chem. Acc. 2001, 105, 207-212.
73. Warshel, A. Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J. Biol. Chem. 1998, 273, 27035-27038.
74. Kurz, J. L.; Kurz, L. C. Anomalous Selectivities in Methyl Transfers to Water - an Explanation Using Free-Energy Surfaces Which Model the Effects of Nonequilibrium Solvation. Isr. J. Chem. 1985, 26, 339-348.
75. Maroncelli, M.; Fleming, G. R. Computer-Simulation of the Dynamics of Aqueous Solvation. J. Chem. Phys. 1988, 89, 5044-5069.
76. Fleming, G. R.; Wolynes, P. G. Chemical-Dynamics in Solution. Phys. Today 1990, 43, 36-43.
77. Nandi, N.; Bhattacharyya, K.; Bagchi, B. Dielectric relaxation and solvation dynamics of water in complex chemical and biological systems. Chem. Rev. 2000, 100, 2013-2045.
78. Pal, S. K.; Peon, J.; Zewail, A. H. Ultrafast surface hydration dynamics and expression of protein functionality: alpha-Chymotrypsin. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15297-15302.
79. Warshel, A.; Chu, Z. T.; Parson, W. W. Dispersed Polaron Simulations of Electron-Transfer in Photosynthetic Reaction Centers. Science 1989, 246, 112-116.