Temperature dependence of the kinetic isotope effects in thymidylate synthase. a theoretical study

Journal of the American Chemical Society

Volumn 133, Issue 17, 2011, Pages 6692-6702

  Kanaan, Natalia ^a   Ferrer, Silvia ^a   Martí, Sergio ^a   Garcia Viloca, Mireia ^b   Kohen, Amnon ^c   Moliner, Vicent ^a,d  

^a UNIVERSITAT JAUME I   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c University of Iowa ^*  (United States)

^d LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BARRIER HEIGHTS; BATH TEMPERATURES; BOND-BREAKING; CATALYZED REACTIONS; CHEMICAL TRANSFORMATIONS; CONFIGURATIONAL SPACES; E. COLI; ENSEMBLE-AVERAGED; EXPERIMENTAL DATA; HYDRIDE TRANSFERS; KINETIC ISOTOPE EFFECTS; PHYSICAL NATURE; PROTEIN MOTION; RATE-LIMITING STEPS; REACTION COORDINATES; RELATIVE MOVEMENT; TEMPERATURE DEPENDENCE; TEMPERATURE RANGE; THEORETICAL FRAMEWORK; THEORETICAL STUDY; THERMAL FLUCTUATIONS; THIOETHER BONDS; THYMIDYLATE SYNTHASE; TRANSFER REACTION; TRANSITION-STATE; VARIATIONAL TRANSITION-STATE THEORY;

AMINO ACIDS; CARRIER MOBILITY; CATALYSIS; ENZYMES; ESCHERICHIA COLI; ISOTOPES; METADATA; MOLECULAR MODELING; QUANTUM THEORY; TEMPERATURE DISTRIBUTION; TRITIUM;

REACTION KINETICS;

ARGININE; CYSTEINE; ISOTOPE; PANTOPRAZOLE; SULFIDE; THYMIDYLATE SYNTHASE; TRITIUM;

ARTICLE; CATALYSIS; CHEMICAL BOND; CONCEPTUAL FRAMEWORK; MOLECULAR MECHANICS; QUANTUM MECHANICS; SIMULATION; TEMPERATURE DEPENDENCE;

ESCHERICHIA COLI; ISOTOPES; KINETICS; MODELS, MOLECULAR; QUANTUM THEORY; TEMPERATURE; THERMODYNAMICS; THYMIDYLATE SYNTHASE;

EID: 79955424715     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja1114369     Document Type: Article

References (92)

1. Agrawal, N.; Hong, B. Y.; Mihai, C.; Kohen, A. Biochemistry 2004, 43, 1998-2006
2. Carreras, C. W.; Santi, D. V. Annu. Rev. Biochem. 1995, 64, 721-762
3. Kanaan, N.; Martí, S.; Moliner, V.; Kohen, A. Biochemistry 2007, 46, 3704-3713
4. Kanaan, N.; Martí, S.; Moliner, V.; Kohen, A. J. Phys. Chem. A 2009, 113, 2176-2182
5. Allemann, R. K.; Scrutton, N. S. Quantum Tunnelling in Enzyme-Catalysed Reactions; Royal Society of Chemistry: Cambridge (UK), 2009.
6. Klinman, J. P. Nature Chem. 2010, 2, 907-909
7. Kohen, A. In Isotope Effects in Chemistry and Biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis-CRC Press: Boca Raton, FL, 2006, pp 743 - 764.
8. Marcus, R. A. Faraday Discuss. 1982, 74, 7-15
9. Marcus, R. A. J. Phys. Chem. B 2007, 111, 6643-6654
10. Marcus, R. A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322
11. Nagel, Z. D.; Klinman, J. P. Chem. Rev. 2006, 106, 3095-3118
12. Nagel, Z. D.; Klinman, J. P. Nat. Chem. Biol. 2009, 5, 543-550
13. Castillo, R.; Roca, M.; Soriano, A.; Moliner, V.; Tuñón, I. J. Phys. Chem. B 2008, 112, 529-534
14. Kanaan, N.; Roca, M.; Tuñón, I.; Martí, S.; Moliner, V. Phys. Chem. Chem. Phys. 2010, 12, 11657-11664
15. Roca, M.; Moliner, V.; Tuñón, I.; Hynes, J. T. J. Am. Chem. Soc. 2006, 128, 6186-6193
16. Roca, M.; Oliva, M.; Castillo, R.; Moliner, V.; Tuñón, I. Chemistry 2010, 16, 11399-11411
17. Ruiz-Pernía, J. J.; Tuñón, I.; Moliner, V.; Hynes, J. T.; Roca, M. J. Am. Chem. Soc. 2008, 130, 7477-7488
18. Gertner, B. J.; Wilson, K. R.; Hynes, J. T. J. Chem. Phys. 1989, 90, 3537-3558
19. Grote, R. F.; Hynes, J. T. J. Chem. Phys. 1980, 73, 2715-2732
20. Alhambra, C.; Corchado, J.; Sánchez, M. L.; Garcia-Viloca, M.; Gao, J.; Truhlar, D. G. J. Phys. Chem. B 2001, 105, 11326-11340
21. Truhlar, D. G.; Gao, J. L.; Alhambra, C.; Garcia-Viloca, M.; Corchado, J.; Sánchez, M. L.; Villa, J. Acc. Chem. Res. 2002, 35, 341-349
22. Truhlar, D. G.; Gao, J. L.; Garcia-Viloca, M.; Alhambra, C.; Corchado, J.; Sánchez, M. L.; Poulsen, T. D. Int. J. Quantum Chem. 2004, 100, 1136-1152
23. Antoniou, D.; Basner, J.; Núñez, S.; Schwartz, S. D. Chem. Rev. 2006, 106, 3170-3187
24. Antoniou, D.; Schwartz, S. D. J. Phys. Chem. B 2001, 105, 5553-5558
25. Cui, Q. A.; Karplus, M. J. Phys. Chem. B 2002, 106, 7927-7947
26. Schramm, V. L. Arch. Biochem. Biophys. 2005, 433, 13-26
27. Bolhuis, P. G.; Chandler, D.; Dellago, C.; Geissler, P. L. Annu. Rev. Phys. Chem. 2002, 53, 291-318
28. Dellago, C.; Bolhuis, P. G.; Chandler, D. J. Chem. Phys. 1998, 108, 9236-9245
29. Schwartz, S. D.; Schramm, V. L. Nat. Chem. Biol. 2009, 5, 552-559
30. Basner, J. E.; Schwartz, S. D. J. Am. Chem. Soc. 2005, 127, 13822-13831
31. Crehuet, R.; Field, M. J. J. Phys. Chem. B 2007, 111, 5708-5718
32. Saen-oon, S.; Quaytman-Machleder, S.; Schramm, V. L.; Schwartz, S. D. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 16543-16548
33. Major, D. T.; Gao, J. L. J. Chem. Theory Comput. 2007, 3, 949-960
34. Major, D. T.; Heroux, A.; Orville, A. M.; Valley, M. P.; Fitzpatrick, P. F.; Gao, J. L. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20734-20739
35. Olsson, M. H. M.; Siegbahn, P. E. M.; Warshel, A. J. Am. Chem. Soc. 2004, 126, 2820-2828
36. Liu, H. B.; Warshel, A. J. Phys. Chem. B 2007, 111, 7852-7861
37. Levy, R. M.; Gallicchio, E. Annu. Rev. Phys. Chem. 1998, 49, 531-567
38. Villa, J.; Strajbl, M.; Glennon, T. M.; Sham, Y. Y.; Chu, Z. T.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 11899-11904
39. Finer-Moore, J. S.; Montfort, W. R.; Stroud, R. M. Biochemistry 1990, 29, 6977-6986
40. Montfort, W. R.; Perry, K. M.; Fauman, E. B.; Finer-Moore, J. S.; Maley, G. F.; Hardy, L.; Maley, F.; Stroud, R. M. Biochemistry 1990, 29, 6964-6977
41. Perry, K. M.; Fauman, E. B.; Finer-Moore, J. S.; Montfort, W. R.; Maley, G. F.; Maley, F.; Stroud, R. M. Proteins: Struct., Funct., Genet. 1990, 8, 315-333
42. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. J. Comput. Chem. 1983, 4, 187-217
43. Antosiewicz, J.; McCammon, J. A.; Gilson, M. K. J. Mol. Biol. 1994, 238, 415-436
44. Field, M. J.; Amara, P.; David, L.; Rinaldo, D. Personal communication.
45. Warshel, A.; Levitt, M. J. Mol. Biol. 1976, 103, 227-249
46. Gao, J. L.; Amara, P.; Alhambra, C.; Field, M. J. J. Phys. Chem. A 1998, 102, 4714-4721
47. Maley, F.; Pedersenlane, J.; Changchien, L. M. Biochemistry 1995, 34, 1469-1474
48. Saxl, R. L.; Changchien, L. M.; Hardy, L. W.; Maley, F. Biochemistry 2001, 40, 5275-5282
49. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. J. Am. Chem. Soc. 1985, 107, 3902-3909
50. MacKerell, A. D. J. Phys. Chem. B 1998, 102, 3586-3616
51. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J. Chem. Phys. 1983, 79, 926-935
52. Verlet, L. Phys. Rev. 1967, 159, 98-103
53. Stroud, R. M.; Finer-Moore, J. S. FASEB J. 1993, 7, 671-677
54. Kumar, S.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A.; Rosenberg, J. M. J. Comput. Chem. 1992, 13, 1011-1021
55. Torrie, G. M.; Valleau, J. P. J. Comput. Phys. 1977, 23, 187-199
56. Garcia-Viloca, M.; Alhambra, C.; Corchado, J. C.; Sánchez, M. L. S.; Villa, J.; Gao, J.; Truhlar, D. G. CHARMMRATE, 2.0; University of Minnesota: Minneapolis, 2002.
57. Garcia-Viloca, M.; Alhambra, C.; Truhlar, D. G.; Gao, J. J. Chem. Phys. 2001, 114, 9953-9958
58. Garcia-Viloca, M.; Alhambra, C.; Truhlar, D. G.; Gao, J. L. J. Comput. Chem. 2003, 24, 177-190
59. Press, W. H.; Teukolsky, S. A.; Vetterling, W. T.; Flannery, B. P. Numerical Recipes in C. The Art of Scientific Computing; Cambridge University Press: Cambridge (UK), 2002.
60. Kuppermann, A.; Truhlar, D. G. J. Am. Chem. Soc. 1971, 93, 1840-1851
61. Marcus, R. A. J. Chem. Phys. 1968, 49, 2610-2616
62. Shavitt, I. J. Chem. Phys. 1968, 49, 4048-4056
63. Garrett, B. C.; Redmon, M. J.; Steckler, R.; Truhlar, D. G.; Baldridge, K. K.; Bartol, D.; Schmidt, M. W.; Gordon, M. S. J. Phys. Chem. 1988, 92, 1476-1488
64. Kanaan, N.; Roca, M.; Tuñón, I.; Martí, S.; Moliner, V. J. Phys. Chem. B 2010, 114, 13593-13600
65. Garrett, B. C.; Truhlar, D. G. J. Chem. Phys. 1983, 79, 4931-4938
66. Miller, W. H. Adv. Chem. Phys. 1974, 25, 69
67. Garrett, B. C.; Truhlar, D. G. J. Phys. Chem. 1979, 83, 2921-2926
68. Liu, Y. P.; Lynch, G. C.; Truong, T. N.; Lu, D. H.; Truhlar, D. G.; Garrett, B. C. J. Am. Chem. Soc. 1993, 115, 2408-2415
69. Lu, D.-H.; Truong, T. N.; Melissas, V.S.; Lynch, G. C.; Liu, Y.-P.; Garrett, B. C.; Steckler, R.; Isaacson, A. D.; Rai, S. N.; Hancock, G. C.; Lauderdale, J. G.; Joseph, T.; Truhlar, D. G. Comput. Phys. Commun. 1992, 71, 235-262
70. Fernández-Ramos, A.; Truhlar, D. G. J. Chem. Phys. 2001, 114, 1491-1496
71. Garrett, B. C.; Abusalbi, N.; Kouri, D. J.; Truhlar, D. G. J. Chem. Phys. 1985, 83, 2252-2258
72. Garrett, B. C.; Truhlar, D. G.; Wagner, A. F.; Dunning, T. H. J. Chem. Phys. 1983, 78, 4400-4413
73. Masgrau, L.; Roujeinikova, A.; Johannissen, L. O.; Hothi, P.; Basran, J.; Ranaghan, K. E.; Mulholland, A. J.; Sutcliffe, M. J.; Scrutton, N. S.; Leys, D. Science 2006, 312, 237-241
74. Ranaghan, K. E.; Masgrau, L.; Scrutton, N. S.; Sutcliffe, M. J.; Mulholland, A. J. ChemPhysChem 2007, 8, 1816-1835
75. Pu, J. Z.; Ma, S. H.; Gao, J. L.; Truhlar, D. G. J. Phys. Chem. B 2005, 109, 8551-8556
76. Gorris, H. H.; Walt, D. R. J. Am. Chem. Soc. 2009, 131, 6277-6282
77. Lu, H. P.; Xie, X. S. Nature 1997, 385, 143-146
78. Xue, Q. F.; Yeung, E. S. Nature 1995, 373, 681-683
79. Hong, B.; Haddad, M.; Maley, F.; Jensen, J. H.; Kohen, A. J. Am. Chem. Soc. 2006, 128, 5636-5637
80. Field, M. J. A Practical Introduction to the Simulation of Molecular Systems; Cambridge University Press: Cambridge (UK), 2007.
81. Machleder, S. Q.; Pineda, J.; Schwartz, S. D. J. Phys. Org. Chem. 2010, 23, 690-695
82. Hatcher, E.; Soudackov, A. V.; Hammes-Schiffer, S. J. Am. Chem. Soc. 2007, 129, 187-196
83. Knapp, M. J.; Rickert, K.; Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 3865-3874
84. Alhambra, C.; Corchado, J. C.; Sánchez, M. L.; Gao, J. L.; Truhlar, D. G. J. Am. Chem. Soc. 2000, 122, 8197-8203
85. Webb, S. P.; Agarwal, P. K.; Hammes-Schiffer, S. J. Phys. Chem. B 2000, 104, 8884-8894
86. Pang, J. Y.; Pu, J. Z.; Gao, J. L.; Truhlar, D. G.; Allemann, R. K. J. Am. Chem. Soc. 2006, 128, 8015-8023
87. Faulder, P. F.; Tresadern, G.; Chohan, K. K.; Scrutton, N. S.; Sutcliffe, M. J.; Hillier, I. H.; Burton, N. A. J. Am. Chem. Soc. 2001, 123, 8604-8605
88. Pang, J. Y.; Hay, S.; Scrutton, N. S.; Sutcliffe, M. J. J. Am. Chem. Soc. 2008, 130, 7092-7097
89. Ferrer, S.; Tuñón, I.; Martí, S.; Moliner, V.; Garcia-Viloca, M.; González-Lafont, A.; Lluch, J. M. J. Am. Chem. Soc. 2006, 128, 16851-16863
90. Loveridge, E. J.; Tey, L. H.; Allemann, R. K. J. Am. Chem. Soc. 2010, 132, 1137-1143
91. Pu, J. Z.; Gao, J. L.; Truhlar, D. G. Chem. Rev. 2006, 106, 3140-3169
92. Lans, I.; Peregrina, J. R.; Medina, M.; Garcia-Viloca, M.; González-Lafont, A.; Lluch, J. M. J. Phys. Chem. B 2010, 114, 3368-3379