Reaction-Path Energetics and Kinetics of the Hydride Transfer Reaction Catalyzed by Dihydrofolate Reductase

Biochemistry

Volumn 42, Issue 46, 2003, Pages 13558-13575

  Garcia Viloca, Mireia ^a   Truhlar, Donald G ^a   Gao, Jiali ^a  

^a University of Minnesota ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSMISSION COEFFICIENTS; VALENCE BOND POTENTIAL;

AMINES; BIOCHEMISTRY; BOUNDARY CONDITIONS; CHEMICAL BONDS; COMPUTER SIMULATION; ELECTROSTATICS; ENZYME KINETICS; FREE ENERGY; ISOTOPES; PH EFFECTS; RATE CONSTANTS; SUBSTRATES;

ENZYMES;

DIHYDROFOLATE REDUCTASE; ION; ISOTOPE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TETRAHYDROFOLIC ACID;

ARTICLE; CALCULATION; CATALYSIS; CHEMICAL BOND; CHEMICAL REACTION; CHEMICAL REACTION KINETICS; ELECTRICITY; ENERGY TRANSFER; ENZYME SUBSTRATE; FORCE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOLECULAR STABILITY; PH; PRIORITY JOURNAL; QUANTUM MECHANICS; SIMULATION; SURFACE PROPERTY; THERMODYNAMICS; VIBRATION;

AMINO ACIDS; BINDING SITES; CATALYSIS; COMPUTER SIMULATION; DEUTERIUM; FOLIC ACID; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; NADP; QUANTUM THEORY; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS;

EID: 0344391945     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034824f     Document Type: Article

References (118)

1. Blakley, R. L. (1995) Adv. Enzymol. 70, 23.
2. Fierke, C. A., Johnson, K. A., and Benkovic, S. J. (1987) Biochemistry 26, 4085.
3. Morrison, J. F., and Stone, S. R. (1988) Biochemistry 27, 5499.
4. McTigue, M. A., Davies, J. F., II, Kaufman, B. T., and Kraut, J. (1992) Biochemistry 31, 7264.
5. Chen, Y.-Q., Kraut, J., Blakley, R. L., and Callender, R. (1994) Biochemistry 33, 7021.
6. Lee, H., Reyes, V. M., and Kraut, J. (1996) Biochemistry 35, 7012.
7. Deng, H., and Callender, R. (1998) J. Am. Chem. Soc. 120, 7730.
8. Cannon, W. R., Garrison, B. J., and Benkovic, S. J. (1997) J. Am. Chem. Soc. 119, 2386.
9. Cummins, P. L., and Gready, J. E. (2001) J. Am. Chem. Soc. 123, 3418.
10. Shrimpton, P., and Allemann, R. K. (2002) Protein Sci. 11, 1442.
11. Falzone, C. J., Wright, P. E., and Benkovic, S. J. (1994) Biochemistry 33, 439.
12. Epstein, D. M., Benkovic, S. J., and Wright, P. E. (1995) Biochemistry 34, 11037.
13. Cameron, C. E., and Benkovic, S. J. (1997) Biochemistry 36, 15792.
14. Sawaya, M. R., and Kraut, J. (1997) Biochemistry 36, 586.
15. Miller, G. P., and Benkovic, S. J. (1998) Biochemistry 37, 6327.
16. Miller, G. P., and Benkovic, S. J. (1998) Biochemistry 37, 6336.
17. Osborne, M. J., Schnell, J., Benkovic, S. J., Dyson, H. J., and Wright, P. E. (2001) Biochemistry 40, 9846.
18. Miller, G. P., Wahnon, D. C., and Benkovic, S. J. (2001) Biochemistry 40, 867.
19. Appleman, J. R., Beard, W. A., Delcamp, T. J., Prendergast, N. J., Freisheim, J. H., and Blakeley, R. A. (1990) J. Biol. Chem. 265, 2740.
20. Rajagopalan, P. T. R., and Benkovic, S. J. (2002) Chem. Rec. 2, 24.
21. Huang, Z., Wagner, C. R., and Benkovic, S. J. (1994) Biochemistry 33, 11576. Wagner, C. R., Huang, Z., Singleton, S. F., and Benkovic, S. J. (1995) Biochemistry 34, 15671.
22. Huang, Z., Wagner, C. R., and Benkovic, S. J. (1994) Biochemistry 33, 11576. Wagner, C. R., Huang, Z., Singleton, S. F., and Benkovic, S. J. (1995) Biochemistry 34, 15671.
23. Rajagopalan, P. T. R., Lutz, S., and Benkovic, S. J. (2002) Biochemistry 41, 12618.
24. Radkiewicz, J. L., and Brooks, C. L., III. (2000) J. Am. Chem. Soc. 122, 225.
25. Agarwal, P. K., Billeter, S. R., Rajagopalan, P. T. R., Benkovic, S. J., and Hammes-Schiffer, S. (2002) Proc. Natl. Acad. Sci. U.S.A. 99, 2794.
26. Agarwal, P. K., Billeter, S. R., and Hammes-Schiffer, S. (2002) J. Phys. Chem. B 106, 3283.
27. Hammes-Schiffer, S. (2002) Biochemistry 41, 13335.
28. Watney, J. B., Agarwal, P. K., and Hammes-Schiffer, S. (2003) J. Am. Chem. Soc. 125, 3745.
29. Thorpe, I. F., and Brooks, C. L., III, personal communication.
30. Bajorath, J., Kraut, J., Li, Z., Kitson, D. H., and Hagler, A. T. (1991) Proc. Natl. Acad. Sci. U.S.A. 88, 6423.
31. Greatbanks, S. P., Gready, J. E., Limaye, A. C., and Rendell, A. P. (2000) J. Comput. Chem. 21, 788.
32. Garcia-Viloca, M., Truhlar, D. G., and Gao, J. (2003) J. Mol. Biol. 327, 549.
33. Cummins, P. L., and Gready, J. E. (1998) J. Comput. Chem. 19, 977.
34. Castillo, R., Andres, J., and Moliner, V. (1999) J. Am. Chem. Soc. 121, 12140.
35. Field, M. J., Bash, P. A., and Karplus, M. (1990) J. Comput. Chem. 11, 700.
36. Gao, J. (1995) in Rev. Comput. Chem. (Lipkowitz, K. B., Boyd, D. B., Eds.) Vol. 7, p 119, VCH, New York.
37. Gao, J., Amara, P., Alhambra, C., and Field, M. J. (1998) J. Phys. Chem. A 102, 4714.
38. Alhambra, C., Corchado, J. C., Sanchez, M. L., Garcia-Viloca, M., Gao, J., and Truhlar, D. G. (2001) J. Phys. Chem. B 105, 11326.
39. Truhlar, D. G., Gao, J., Alhambra, C., Garcia-Viloca, M., Corchado, J. C., Sánchez, M. L., and Villà, J. (2002) Acc. Chem. Res. 35, 341.
40. Cook, P. F., Ed. (1991) Enzyme Mechanism from Isotope Effects, CRC Press, Boca Raton, FL.
41. Devi-Kesavan, L. S., Garcia-Viloca, M., and Gao, J. (2003) Theor. Chem. Acc. 109, 133.
42. Garcia-Viloca, M., Alhambra, C., Truhlar, D. G., and Gao, J. (2003) J. Comput. Chem. 24, 177.
43. Garcia-Viloca, M., Alhambra, C., Truhlar, D. G., and Gao, J. (2001) J. Chem. Phys. 114, 9953.
44. Truhlar, D. G., Isaacson, A. D., and Garrett, B. C. (1985) in Theory of Chemical Reaction Dynamics (Baer, M., Ed.) Vol. 4, p 65, CRC Press: Boca Raton.
45. Anderson, J. B. (1995) Adv. Chem. Phys. 91, 381.
46. Liu, Y.-P., Lynch, G. C., Truong, T. N., Lu, D. H., Truhlar, D. G., and Garrett, B. (1993) C. J. Am. Chem. Soc. 115, 2408.
47. (a) Liu, Y.-P., Lu, D.-h., Gonzalez-Lafont, A., Truhlar, D. G., and Garrett, B. C. (1993) J. Am. Chem. Soc. 115, 7806.
48. (b) Fernandez-Ramos, A., and Truhlar, D. G. (2001) J. Chem. Phys. 114, 1491.
49. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., and Swaminathan, S. (1983) J. Comput. Chem. 4, 187.
50. (a) MacKerell, A., Bashford, D., Bellot, M., Dunbrack, R., Evanseck, J. D., Field, M., Gao, J., Guo, H., Ha, S., Joseph, D., Kuchnir, L., Kuczera, K., Lau, F., Mattos, C., Minchnick, S., Ngo, T., Nguyen, D., Prodhom, B., Reiher, W. E., Roux, B., Schlenkrich, M., Smith, J., Stote, R., Strub, J., Watanabe, M., Wiokiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) J. Phys. Chem. B 102, 3586.
51. (b) Pavelites, J. J. P., Gao, J., Bash, P. A., and MacKerell, A. D., Jr. (1997) J. Comput. Chem. 18, 221.
52. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) J. Chem. Phys. 79, 926.
53. Mulliken, R. S. (1955) J. Chem. Phys. 23, 1833.
54. Dewar, M. J. S., Zoebisch, E. G., Healy, E. F., and Stewart, J. J. P. (1985) J. Am. Chem. Soc. 107, 3902.
55. Stewart, J. J. P. (1989) J. Comput. Chem. 10, 221.
56. Adamo, C., and Barone, V. (1997) Chem. Phys. Lett. 274, 242.
57. Lynch, B. J., Zhao, Y., and Truhlar, D. G. (2003) J. Phys. Chem. A 107, 1384.
58. Hockney, R. W. (1970) Methods Comput. Phys. 9, 136-211.
59. Nosé, S. (1984) J. Chem. Phys. 81, 511.
60. Hoover, W. G. (1985) Phys. Rev. A 31, 1695.
61. Andersen, H. C. (1980) J. Chem. Phys. 72, 2384.
62. Rychaert, J. P., Cicotti, G., and Berensden, H. J. C. (1977) J. Comput. Phys. 23, 327.
63. Shirley, W. A., and Brooks, C. L., III. (1997) Proteins: Struct. Funct. Genet. 28, 59.
64. Verlet, L. (1967) Phys. Rev. 159, 98.
65. Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A., and Rosenberg, J. M. (1992) J. Comput. Chem. 13, 1011.
66. Boczko, E. M., and Brooks, C. L., III. (1993) J. Phys. Chem. 97, 4509.
67. Rajamani, R., Naidoo, K., and Gao, J. (2003) J. Comput. Chem., in press.
68. Alhambra, C., Gao, J., Corchado, J. C., Villa, J., and Truhlar, D. G. (1999) J. Am. Chem. Soc. 121, 2253.
69. Alhambra, C., Corchado, J. C., Sánchez, M. L., Villà, J., Gao, J., Truhlar, D. G. CHARMMRATE-version 1.0, a module of CHARMM-version 27.
70. Corchado, J. C., Chuang, Y.-Y., Fast, P. L., Vill, J., Hu, W.-P., Liu, Y.-P., Lynch, G. C., Nguyen, K. A., Jackels, C. F., Melissas, V. S., Lynch, B., Rossi, I., Coitio, E. L., Steckler, R., Garrett, B. C., Isaacson, A. D., and Truhlar, D. G. POLYRATE 8.5b, University of Minnesota, Minneapolis, MN, 1999.
71. Alhambra, C., Sanchez, M. L., Corchado, J., Gao, J., and Truhlar, D. G. (2002) Chem. Phys. Lett. 355, 388.
72. Fletcher, R. (1987) Practical Methods of Optimization, Wiley, New York.
73. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1986) Numerical Recipies, Cambridge University Press, Cambridge.
74. Garrett, B. C., Redmon, M. J., Steckler, R., Truhlar, D. G., Baldridge, K. K., Bartol, D., Schmidt, M. W., and Gordon, M. S. (1988) J. Phys. Chem. 92, 1476.
75. Wu, Y.-D., and Houk, K. N. (1987) J. Am. Chem. Soc. 109, 906.
76. Andres, J., Safont, V. S., Martins, J. B. L., Beltran, A., and Moliner, V. (1995) J. Mol. Struct, 330, 411.
77. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
78. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
79. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
80. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
81. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
82. Rickert, K. W., and Klinman, J. P. (1999) Biochemistry 38, 12218. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) J. Am. Chem. Soc. 123, 10421. Rubach, J. K., Ramaswamy, S., and Plapp, B. V. (2001) Biochemistry 40, 12686. Knapp, M. J., Rickert, K., and Klinman, J. P. (2002) J. Am. Chem. Soc. 124, 3865. Hothi, P., Basran, J., Sutcliff, M. J., and Scrutton, N. S. (2003) Biochemistry 42, 3966. Segraves, E. N., and Holman, T. R. (2003) Biochemistry 42, 5236.
83. Billeter, S. R., Webb, S. P., Iordanov, T., Agawal, P. K., and Hammes-Schiffer, S. (2001) J. Chem. Phys. 114, 6925.
84. Hammes-Schiffer, S. (2001) Int. Rev. Phys. Chem. 20, 591.
85. Billeter, S. R., Webb, S. P., Agarwal, P. K., Iordanov, T., and Hammes-Schiffer, S. (2001) J. Am. Chem. Soc. 123, 11262.
86. Nicoll, R. M., Hindle, S. A., MacKenzie, G., Hillier, I. H., and Burton, N. A. (2001) Theor. Chem. Acc. 106, 105.
87. Faulder, P. F., Tresadern, G., Chohan, K. K., Scrutton, N. S., Sutcliffe, M. J., Hillier, I. H., and Burton, N. A. (2001) J. Am. Chem. Soc. 123, 8604.
88. Garcia-Viloca, M., Alhambra, C., Truhlar, D. G., and Gao, J. (2002) J. Am. Chem. Soc. 124, 7268.
89. Cui, Q., Elstner, M., and Karplus, M. (2002) J. Am. Chem. Soc. 106, 2721. Cui, Q., and Karplus, M. (2002) J. Am. Chem. Soc. 124, 3093.
90. Cui, Q., Elstner, M., and Karplus, M. (2002) J. Am. Chem. Soc. 106, 2721. Cui, Q., and Karplus, M. (2002) J. Am. Chem. Soc. 124, 3093.
91. Tresadern, G., McNamara, J. P., Mohr, M., Wang, H., Burton, N. A., and Hillier, I. H. (2002) Chem. Phys. Lett. 358, 489. Tresadern, G., Nunez, S., Faulder, P. F., Wong, H., Hillier, I. H., and Burton, N. A. (2003) Faraday Discuss. 122, 223. Tresadern, G., Faulder P. F., Gleeson, M. P., Tai, Z., MacKenzie, G., Burton, N. A., and Hillier, I. H. (2003) Theor. Chem. Acc. 109, 108.
92. Tresadern, G., McNamara, J. P., Mohr, M., Wang, H., Burton, N. A., and Hillier, I. H. (2002) Chem. Phys. Lett. 358, 489. Tresadern, G., Nunez, S., Faulder, P. F., Wong, H., Hillier, I. H., and Burton, N. A. (2003) Faraday Discuss. 122, 223. Tresadern, G., Faulder P. F., Gleeson, M. P., Tai, Z., MacKenzie, G., Burton, N. A., and Hillier, I. H. (2003) Theor. Chem. Acc. 109, 108.
93. Tresadern, G., McNamara, J. P., Mohr, M., Wang, H., Burton, N. A., and Hillier, I. H. (2002) Chem. Phys. Lett. 358, 489. Tresadern, G., Nunez, S., Faulder, P. F., Wong, H., Hillier, I. H., and Burton, N. A. (2003) Faraday Discuss. 122, 223. Tresadern, G., Faulder P. F., Gleeson, M. P., Tai, Z., MacKenzie, G., Burton, N. A., and Hillier, I. H. (2003) Theor. Chem. Acc. 109, 108.
94. Sutcliffe, M. J., and Scrutton, N. S. (2002) Eur. J. Biochem. 269, 3096.
95. Li, L., Wright, P. E., Benkovic, S. J., and Falzone, C. J. (1992) Biochemistry 31, 7826.
96. Lavie, A., Allen, K.-N., Petsko, G. A., and Ringe, D. (1994) Biochemistry 33, 5469.
97. McMillan, F. M., Cahoon, M., White, A., Hedstrom, L., Petsko, G. A., and Ringe, D. (2000) Biochemistry 39, 4533.
98. Stroud, R. M., and Finer-Moore, J. S. (2003) Biochemistry 42, 239.
99. Yu, E. W., and Koshland, D. E., Jr. (2001) Proc. Natl. Acad. Sci. U.S.A. 98, 9517.
100. Gao, J. (2003) Curr. Opin. Struct. Biol. 13, 184.
101. Bash, P. A., Field, M. J., Davenport, R. C., Petsko, G. A., Ringe, D., and Karplus, M. (1991) Biochemistry 30, 5826.
102. Cui, Q., and Karplus, M. (2001) J. Am. Chem. Soc. 123, 2284.
103. Gao, J., Kuczera, K., Tidor, B., and Karplus, M. (1989) Science 244, 1069.
104. Zhu, X.-Q., Liu, Y., Zhao, B.-J., and Cheng, J.-P. (2001) J. Org. Chem. 66, 370.
105. Marcus, R. A. (1963) Annu. Rev. Phys. Chem. 15, 155.
106. Zusman, L. D. (1980) Chem. Phys. 49, 295.
107. Hynes, J. T. (1985) in Theory of Chemical Reaction Dynamics (Baer, M., Ed.) Vol. 4, p 171, CRC Press, Boca Raton.
108. Hwang, J.-K., King, G., Creighton, S., and Warshel, A. (1988) J. Am. Chem. Soc. 110, 5297.
109. Warshel, A. (1991) Computer Modeling of Chemical Reactions in Enzymes and Solutions, Wiley, New York.
110. Yadav, A., Jackson, R. M., Holbrook, J. J., and Warshel, A. (1991) J. Am. Chem. Soc. 113, 4800.
111. Muller, R. P., and Warshel, A. (1995) J. Phys. Chem. 99, 17516.
112. Zhou, H.-X., and Szabo, A. (1995) J. Chem. Phys. 103, 3481.
113. Ando, K., and Hynes, J. T. (1997) J. Phys. Chem. B 101, 104564.
114. Mo, Y., and Gao, J. (2000) J. Phys. Chem. A 104, 3012.
115. Villa, J., and Warshel, A. (2001) J. Phys. Chem. B 105, 7887.
116. Schenter, G. K., Garrett, B. C., and Truhlar, D. G. (2001) J. Phys. Chem. B 105, 9672.
117. van Gunsteren, W. F., Billeter, S. R., Eising, A. A., Hünenberger, P. H., Krüger, P., Mark, A. E., Scott, W. R. P., and Tironi, I. G. Biomolecular Simulation: The GROMOS96 Manual and User Guide; Biomos b.v., Zürich and Groningen, VdF Hochschulverlag, ETH Zürich: Zürich, 1996.
118. Warshel, A., and Bentzien, J. (1999) ACS Symp. Ser. 721, 489.