Adenosine triphosphate hydrolysis mechanism in kinesin studied by combined quantum-mechanical/molecular-mechanical metadynamics simulations

Journal of the American Chemical Society

Volumn 135, Issue 24, 2013, Pages 8908-8919

  McGrath, Matthew J ^a   Kuo, I F Will ^b   Hayashi, Shigehiko ^a   Takada, Shoji ^a  

^a KYOTO UNIVERSITY   (Japan)

^b LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE HYDROLYSIS; DISPERSION-CORRECTED DENSITY FUNCTIONAL; FREE ENERGY SURFACE; HYDROGEN-BONDED CHAINS; HYDROLYSIS REACTION; METADYNAMICS SIMULATIONS; QUANTUM MECHANICAL; QUANTUM MECHANICS/MOLECULAR MECHANICS;

ADENOSINETRIPHOSPHATE; FREE ENERGY; HYDROGEN BONDS; MECHANISMS; MOLECULAR MODELING; PHOSPHATES;

HYDROLYSIS;

ADENOSINE TRIPHOSPHATE; KINESIN 5; WATER;

ARTICLE; ATOM; DENSITY FUNCTIONAL THEORY; DISPERSION; DISSOCIATION; ENERGY; ENZYME ACTIVE SITE; HYDROGEN BOND; HYDROLYSIS; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTON TRANSPORT; QUANTUM MECHANICS;

ADENOSINE TRIPHOSPHATE; CATALYTIC DOMAIN; HUMANS; HYDROLYSIS; KINESIN; MODELS, MOLECULAR;

EID: 84879390055     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja401540g     Document Type: Article

References (84)

1. Hirokawa, N.; Noda, Y.; Tanaka, Y.; Niwa, S. Nat. Rev. Mol. Cell Biol. 2009, 10, 682-696
2. Svoboda, K.; Schmidt, C. F.; Schnapp, B. J.; Block, S. M. Nature 1993, 365, 721-727
3. Yildiz, A.; Tomishige, M.; Vale, R. D.; Selvin, P. R. Science 2004, 303, 676-678
4. Kikkawa, M.; Sablin, E. P.; Okada, Y.; Yajima, H.; Fletterick, R. J.; Hirokawa, N. Nature 2001, 411, 439-445
5. Woehlke, G.; Ruby, A. K.; Hart, C. L.; Ly, B.; Hom-Booher, N.; Vale, R. D. Cell 1997, 90, 207-216
6. Åqvist, J.; Kolmodin, K.; Florián, J.; Warshel, A. Curr. Biol. 1999, 6, R71-R80
7. Schweins, T.; Langen, R.; Warshel, A. Nat. Struct. Biol. 1994, 1, 476-484
8. Schwarzl, S. M.; Smith, J. C.; Fischer, S. Biochemistry 2006, 45, 5830-5847
9. Li, G.; Cui, Q. J. Phys. Chem. B 2004, 108, 3342-3357
10. Grigorenko, B. L.; Nemukhin, A. V.; Shadrina, M. S.; Topol, I. A.; Burt, S. K. Proteins: Struct., Funct., Bioinf. 2007, 66, 456-466
11. Dittrich, M.; Hayashi, S.; Schulten, K. Biophys. J. 2003, 85, 2253-2266
12. Dittrich, M.; Hayashi, S.; Schulten, K. Biophys. J. 2004, 87, 2954-2967
13. Hayashi, S.; Ueno, H.; Shaikh, A. R.; Umemura, M.; Kamiya, M.; Ito, Y.; Ikeguchi, M.; Komoriya, Y.; Iino, R.; Noji, H. J. Am. Chem. Soc. 2012, 134, 8447-8454
14. Grigorenko, B. L.; Rogov, A. V.; Topol, I. A.; Burt, S. K.; Martinez, H. M.; Nemukhin, A. V. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 7057-7061
15. Grigorenko, B. L.; Kaliman, I. A.; Nemukhin, A. V. J. Mol. Graphics Modell. 2011, 31, 1-4
16. Prasad, B. R.; Plotnikov, N. V.; Warshel, A. J. Phys. Chem. B 2013, 117, 153-163
17. Onishi, H.; Mochizuki, N.; Morales, M. F. Biochemistry 2004, 43, 3757-3763
18. Beke-Somfai, T.; Lincoln, P.; Nordén, B. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4828-4833
19. 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. Science 2000, 287, 1615-1622
20. Isaev, A.; Scheiner, S. J. Phys. Chem. B 2001, 105, 6420-6426
21. Fisher, Z.; Prada, J. A. H.; Tu, C.; Duda, D.; Yoshioka, C.; An, H.; Govindasamy, L.; Silverman, D. N.; McKenna, R. Biochemistry 2005, 44, 1097-1105
22. Takahashi, H.; Hashimoto, H.; Nitta, T. J. Chem. Phys. 2003, 119, 7964-7971
23. Loerting, T.; Liedl, K. R. J. Phys. Chem. A 2001, 105, 5137-5145
24. Olsson, M. H. M.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6500-6505
25. Braun-Sand, S.; Burykin, A.; Chu, Z. T.; Warshel, A. J. Phys. Chem. B 2005, 109, 583-592 (PMID 1685105)
26. Braun-Sand, S.; Strajbl, M.; Warshel, A. Biophys. J. 2004, 87, 2221-2239
27. Kato, M.; Pisliakov, A. V.; Warshel, A. Proteins: Struct., Funct., Bioinf. 2006, 64, 829-844
28. Parke, C. L.; Wojcik, E. J.; Kim, S.; Worthylake, D. K. J. Biol. Chem. 2010, 285, 5859-5867
29. Jun, B.; Kim, S. J. Biol. Chem. 2010, 285, 11073-11077
30. Valentine, M. T.; Gilbert, S. P. Curr. Opin. Cell Biol. 2007, 19, 75-81
31. Kashina, A. S.; Rogers, G. C.; Scholey, J. M. Biochim. Biophys. Acta 1997, 1357, 257-271
32. Peterman, E. J. G.; Scholey, J. M. Curr. Biol. 2009, 19, R1089-R1094
33. Endow, S. A.; Kull, F. J.; Liu, H. J. Cell Sci. 2010, 123, 3420-3424
34. Tanenbaum, M. E.; Medema, R. H. Dev. Cell 2010, 19, 797-806
35. Krzysiak, T. C.; Grabe, M.; Gilbert, S. P. J. Biol. Chem. 2008, 283, 2078-2087
36. Turner, J.; Anderson, R.; Guo, J.; Beraud, C.; Fletterick, R.; Sakowicz, R. J. Biol. Chem. 2001, 276, 25496-25502
37. Kull, F. J.; Endow, S. A. J. Cell Sci. 2002, 115, 15-23
38. Lin, H.; Truhlar, D. Theor. Chem. Acc. 2007, 117, 185-199
39. Kamerlin, S. C. L.; Haranczyk, M.; Warshel, A. J. Phys. Chem. B 2009, 113, 1253-1272
40. Laio, A.; Parrinello, M. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12562-12566
41. Boero, M.; Ikeda, T.; Ito, E.; Terakura, K. J. Am. Chem. Soc. 2006, 128, 16798-16807
42. Glaves, R.; Mathias, G.; Marx, D. J. Am. Chem. Soc. 2012, 134, 6995-7000
43. Eswar, N.; Marti-Renom, M. A.; Webb, B.; Madhusudhan, M. S.; Eramian, D.; Shen, M.; Pieper, U.; Sali, A. Current Protocols in Bioinformatics, Supplement 15; John Wiley & Sons: New York, 2006.
44. Humphrey, W.; Dalke, A.; Schulten, K. J. Mol. Graphics 1996, 14, 33-38
45. Pavelites, J. J.; Gao, J.; Bash, P. A.; MacKerell, A. D., Jr. J. Comput. Chem. 1997, 18, 221-239
46. MacKerell, A. D., Jr. J. Phys. Chem. B 1998, 102, 3586-3616
47. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J. Chem. Phys. 1983, 79, 926-935
48. Pecoraro, V. L.; Hermes, J. D.; Cleland, W. W. Biochemistry 1984, 23, 5262-5271
49. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. J. Chem. Theory Comput. 2008, 4, 435-447
50. Miyamoto, S.; Kollman, P. A. J. Comput. Chem. 1992, 13, 952-962
51. Hess, B. J. Chem. Theory Comput. 2008, 4, 116-122
52. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. J. Chem. Phys. 1984, 81, 3684-3690
53. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. J. Chem. Phys. 1995, 103, 8577-8593
54. Laino, T.; Mohamed, F.; Laio, A.; Parrinello, M. J. Chem. Theory Comput. 2005, 1, 1176-1184
55. Hu, L.; Söderhjelm, P.; Ryde, U. J. Chem. Theory Comput. 2011, 7, 761-777
56. CP2K Developers, Open Source Molecular Dynamics. http://www.cp2k.org
57. Kohn, W.; Sham, L. J. Phys. Rev. 1965, 140, A1133-A1138
58. VandeVondele, J.; Krack, M.; Mohamed, F.; Parrinello, M.; Chassaing, T.; Hutter, J. Comput. Phys. Commun. 2005, 167, 103-128
59. Becke, A. D. Phys. Rev. A 1988, 38, 3098-3100
60. Lee, C.; Yang, W.; Parr, R. G. Phys. Rev. B 1988, 37, 785-789
61. Grimme, S.; Antony, J.; Ehrlich, S.; Krieg, H. J. Chem. Phys. 2010, 132 154104
62. Antony, J.; Grimme, S. Phys. Chem. Chem. Phys. 2006, 8, 5287-5293
63. Harrison, C. B.; Schulten, K. J. Chem. Theory Comput. 2012, 8, 2328-2335
64. Klähn, M.; Braun-Sand, S.; Rosta, E.; Warshel, A. J. Phys. Chem. B 2005, 109, 15645-15650
65. Ensing, B.; de Vivo, M.; Liu, Z.; Moore, P.; Klein, M. L. Acc. Chem. Res. 2006, 39, 73-81
66. Laio, A.; Gervasio, F. L. Rep. Prog. Phys. 2008, 71 126601
67. Singh, S.; Chopra, M.; de Pablo, J. J. Annu. Rev. Chem. Biomol. Eng. 2012, 3, 369-394
68. Bussi, G.; Laio, A.; Parrinello, M. Phys. Rev. Lett. 2006, 96 090601
69. Kamerlin, S. C. L.; Warshel, A. Comput. Mol. Sci. 2011, 1, 30-45
70. Štajbl, M.; Shurki, A.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 14834-14839
71. Plotnikov, N. V.; Kamerlin, S. C. L.; Warshel, A. J. Phys. Chem. B 2011, 115, 7950-7962
72. Ensing, B.; Klein, M. L. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 6755-6759
73. Laio, A.; Rodriguez-Fortea, A.; Gervasio, F. L.; Ceccarelli, M.; Parrinello, M. J. Phys. Chem. B 2005, 109, 6714-6721
74. Raiteri, P.; Laio, A.; Gervasio, F. L.; Micheletti, C.; Parrinello, M. J. Phys. Chem. B 2006, 110, 3533-3539
75. Bonomi, M.; Barducci, A.; Parrinello, M. J. Comput. Chem. 2009, 30, 1615-1621
76. Frushicheva, M. P.; Cao, J.; Warshel, A. Biochemistry 2011, 50, 3849-3858
77. Cochran, J. C.; Gilbert, S. P. Biochemistry 2005, 44, 16633-16648
78. Cochran, J. C.; Krzysiak, T. C.; Gilbert, S. P. Biochemistry 2006, 45, 12334-12344
79. Warshel, A.; Sussman, F.; Hwang, J.-K. J. Mol. Biol. 1988, 201, 139-159
80. Nemukhin, A. V.; Grigorenko, B. L.; Lushchekina, S. V.; Varfolomeev, S. D. Russ. Chem. Rev. 2012, 81, 1011-1025
81. Goyal, P.; Ghosh, N.; Phatak, P.; Clemens, M.; Gaus, M.; Elstner, M.; Cui, Q. J. Am. Chem. Soc. 2011, 133, 14981-14997
82. Yang, Y.; Cui, Q. J. Phys. Chem. A 2009, 113, 12439-12446
83. Yang, Y.; Yu, H.; Cui, Q. J. Mol. Biol. 2008, 381, 1407-1420
84. Mukherjee, S.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 20550-20555