Stabilization of different types of transition states in a single enzyme active site: QM/MM analysis of enzymes in the alkaline phosphatase superfamily

Journal of the American Chemical Society

Volumn 135, Issue 28, 2013, Pages 10457-10469

  Hou, Guanhua ^a   Cui, Qiang ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ENZYME ACTIVE SITES; PHOSPHATE MONOESTER; PHOSPHATE MONOESTERS; PHOSPHORYL TRANSFER; SOLVENT ACCESSIBILITY; STRUCTURAL DISTORTIONS; TRANSITION STATE STRUCTURE;

BINDING ENERGY; HAMILTONIANS;

PHOSPHATASES;

ALKALINE PHOSPHATASE; ORGANOPHOSPHATE; SOLVENT;

ARTICLE; CONTROLLED STUDY; DENSITY FUNCTIONAL THEORY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME STABILITY; ENZYME STRUCTURE; HYDROLYSIS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; PROTEIN MOTIF; QUANTUM MECHANICS; SIMULATION; WILD TYPE;

ALKALINE PHOSPHATASE; CATALYTIC DOMAIN; ENZYME STABILITY; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR STRUCTURE; QUANTUM THEORY;

EID: 84880385206     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja403293d     Document Type: Article

References (111)

1. Galperin, M.; Bairoch, A.; Koonin, E. Protein Sci. 1998, 7, 1829-1835
2. Galperin, M.; Hedrzejas, M. Proteins: Struct., Funct., Bioinf. 2001, 45, 318-324
3. Lassila, J.; Herschlag, D. Biochemistry 2008, 47, 12853-12859
4. van Loo, B.; Jonas, S.; Babtie, A. C.; Benjdia, A.; Berteau, O.; Hyvönen, M.; Hollfelder, F. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 2740-2745
5. Jonas, S.; Hollfelder, F. Pure Appl. Chem. 2009, 81, 731-742
6. Hou, G. H.; Cui, Q. J. Am. Chem. Soc. 2012, 134, 229-246
7. Lassila, J. K.; Zalatan, J. G.; Herschlag, D. Annu. Rev. Biochem. 2011, 80, 669-702
8. O'Brien, P.; Herschlag, D. J. Am. Chem. Soc. 1998, 120, 12369-12370
9. O'Brien, P.; Herschlag, D. J. Am. Chem. Soc. 1999, 121, 11022-11023
10. O'Brien, P.; Herschlag, D. Biochemistry 2001, 40, 5691-5699
11. Nikolic-Hughes, I.; Rees, D.; Herschlag, D. J. Am. Chem. Soc. 2004, 126, 11814-11819
12. Zalatan, J.; Herschlag, D. J. Am. Chem. Soc. 2006, 128, 1293-1303
13. Zalatan, J.; Fenn, T.; Brunger, A.; Herschlag, D. Biochemistry 2006, 45, 9788-9803
14. Zalatan, J.; Catrina, I.; Mitchell, R.; Grzyska, P.; O'Brien, P.; Herschlag, D. J. Am. Chem. Soc. 2007, 129, 9789-9798
15. Zalatan, J.; Fenn, A.; Herschlag, D. J. Mol. Biol. 2008, 384, 1174-1189
16. O'Brien, P.; Lassila, J.; Fenn, T.; Zalatan, J.; Herschlag, D. Biochemistry 2008, 47, 7663-7672
17. Fersht, A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding; W.H. Freeman and Company: New York, 1999.
18. Jencks, W. Catalysis in chemistry and enzymology; Dover Publications: New York, 1987.
19. López-Canut, V.; Marti, S.; Bertrán, J.; Moliner, V.; Tuñón, I. J. Phys. Chem. B 2009, 113, 7816-7824
20. López-Canut, V.; Roca, M.; Bertrán, J.; Moliner, V.; Tuñón, I. J. Am. Chem. Soc. 2010, 132, 6955-6963
21. López-Canut, V.; Roca, M.; Bertrán, J.; Moliner, V.; Tuñón, I. J. Am. Chem. Soc. 2011, 133, 12050-12062
22. Luo, J. H.; van Loo, B.; Kamerlin, S. C. L. Proteins: Struct., Funct., Bioinf. 2012, 80, 1211-1226
23. Luo, J. H.; van Loo, B.; Kamerlin, S. C. L. FEBS Lett. 2012, 586, 1622-1630
24. Åqvist, J.; Kolmodin, K.; Florián, J.; Warshel, A. Chem. Biol. 1999, 6, R71-R80
25. Nam, K.; Cui, Q.; Gao, J.; York, D. J. Chem. Theory Comput. 2007, 3, 486-504
26. Wong, K. Y.; Gao, J. L. Biochemistry 2007, 46, 13352-13369
27. Garcia-Viloca, M.; Alhambra, C.; Truhlar, D. G.; Gao, J. L. J. Am. Chem. Soc. 2002, 124, 7268-7269
28. Rosta, E.; Nowotny, M.; Yang, W.; Hummer, G. J. Am. Chem. Soc. 2011, 133, 8934-8941
29. Norotny, M.; Gaidamakov, S. A.; Crouch, R. J.; Yang, W. Cell 2005, 12, 1005-1016
30. Nowotny, M.; Yang, W. EMBO J. 2006, 25, 1924-1933
31. Yang, Y.; Yu, H.; York, D.; Elstner, M.; Cui, Q. J. Chem. Theory Comput. 2008, 4, 2067-2084
32. Elstner, M.; Cui, Q.; Munih, P.; Kaxiras, E.; Frauenheim, T.; Karplus, M. J. Comput. Chem. 2003, 24, 565-581
33. Chakravorty, D. K.; Wang, B.; Lee, C. W.; Giedroc, D. P.; Merz, K. M., Jr. J. Am. Chem. Soc. 2012, 134, 3367-3376
34. Riccardi, D.; Cui, Q. J. Phys. Chem. A 2007, 111, 5703-5711
35. Xu, D.; Guo, H.; Cui, Q. J. Am. Chem. Soc. 2007, 129, 10814-10822
36. Hou, G. QM/MM studies of phosphoryl transfer reactions in the alkaline phosphatase superfamily. Ph. D. Thesis, University of Wisconsin-Madison: Madison, WI, 2012.
37. Riccardi, D.; Zhu, X.; Goyal, P.; Yang, S.; Hou, G.; Cui, Q. Sci. China: Chem. 2012, 55, 3-18
38. Hou, G.; Zhu, X.; Elstner, M.; Cui J. Chem. Theory Comput. 2012, 8, 4293-4304
39. Brunger, A.; Karplus, M. Protein: Struct., Funct., Genet. 1988, 4, 148-156
40. Brooks, B.; Bruccoleri, R.; Olafson, B.; States, D.; Swaminathan, S.; Karplus, M. J. Comput. Chem. 1983, 4, 187-217
41. Brooks, C. L., III.; Karplus, M. J. Chem. Phys. 1983, 79, 6312-6325
42. MacKerell, A. J. Chem. Phys. 1998, 102, 3586-3616
43. Jorgensen, W.; Chandrasekhar, J.; Madura, J.; Impey, R.; Klein, M. J. Chem. Phys. 1983, 79, 926-935
44. Konig, P.; Hoffmann, M.; Frauenheim, T.; Cui, Q. J. Phys. Chem. B 2005, 109, 9082-9095
45. Hou, G. H.; Zhu, X.; Cui, Q. J. Chem. Theory Comput. 2010, 6, 2303-2314
46. Yang, Y.; Yu, H.; Cui, Q. J. Mol. Biol. 2008, 381, 1407-1420
47. Yang, Y.; Cui, Q. J. Phys. Chem. B 2009, 113, 4930-4933
48. Yang, Y.; Cui, Q. J. Phys. Chem. A 2009, 113, 12439-12446
49. Yang, Y.; Miao, Y. P.; Wang, B.; Cui, G. L.; Merz, K. M., Jr. Biochemistry 2012, 51, 2606-2618
50. Arantes, G.; Loos, M. Phys. Chem. Chem. Phys. 2006, 8, 347-353
51. Im, W.; Bernèche, S.; Roux, B. J. Chem. Phys. 2001, 114, 2924-2937
52. Schaefer, P.; Riccardi, D.; Cui, Q. J. Chem. Phys. 2005, 123, 014905
53. Riccardi, D.; Schaefer, P.; Yang, Y.; Yu, H.; Ghosh, H.; Prat-Resina, X.; König, P.; Li, G.; Xu, D.; Guo, H.; Elstner, M.; Cui, Q. J. Phys. Chem. B 2006, 110, 6458-6469
54. Brooks, C.; Karplus, M. J. Mol. Biol. 1989, 208, 159-181
55. Rychaert, J.; Ciccotti, G.; Berendsen, H. J. Comput. Phys. 1977, 23, 327-341
56. Im, W.; Beglov, D.; Roux, B. Comput. Phys. Commun. 1998, 111, 59-75
57. Lu, X.; Cui, Q. J. Phys. Chem. B 2013, 117, 2005-2018
58. Nina, M.; Beglov, D.; Roux, D. J. Phys. Chem. B 1997, 101, 5239-5248
59. Nina, M.; Im, W.; Roux, D. Biophys. Chem. 1999, 78, 89-96
60. Steinbach, P.; Brooks, B. J. Comput. Chem. 1994, 15, 667-683
61. Cui, Q.; Elstner, M.; Kaxiras, E.; Frauenheim, T.; Karplus, M. J. Phys. Chem. B 2001, 105, 569-585
62. Klopman, G. J. Am. Chem. Soc. 1964, 86, 4550-4557
63. Ohno, K. Theor. Chim. Acta 1964, 2, 219-227
64. Thiel, W. Adv. Chem. Phys. 1996, 93, 703-757
65. Elstner, M. J. Phys. Chem. A 2007, 111, 5614-5621
66. Yang, Y.; Yu, H.; York, D.; Cui, Q.; Elstner, M. J. Phys. Chem. A 2007, 111, 10861-10873
67. Das, D.; Eurenius, K. P.; Billings, E. M.; Sherwood, P.; Chatfield, D. C.; Hodoscek, M.; Brooks, B. R. J. Chem. Phys. 2002, 117, 10534-10547
68. Wang, B.; Truhlar, D. G. J. Chem. Theory Comput. 2010, 6, 3330-3342
69. Stone, A. J. The theory of intermolecular forces; Oxford University Press: Oxford, U.K., 1997.
70. Torrie, G. M.; Valleau, J. P. J. Chem. Phys. 1977, 23, 187-199
71. Kumar, S.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A.; Rosenberg, J. M. J. Comput. Chem. 1992, 13, 1011-1021
72. Becke, A. Phys. Rev. A 1988, 38, 3098-3100
73. Becke, A. J. Chem. Phys. 1993, 98, 5648-5652
74. Lee, C.; Yang, W.; Parr, R. Phys. Rev. B 1988, 37, 785-789
75. Truhlar, D. G.; Zhao, Y. Theor. Chem. Acc. 2008, 120, 215-241
76. Shao, Y. Phys. Chem. Chem. Phys. 2006, 27, 3172-3191
77. Brooks, B. R. J. Comput. Chem. 2009, 30, 1545-1614
78. Petersson, G.; Bennett, A.; Tensfeldt, T.; Allaham, M.; Shirley, W.; Mantzaris, J. J. Chem. Phys. 1988, 89, 2193-2218
79. Wu, R.; Lu, Z.; Cao, Z.; Zhang, Y. J. Am. Chem. Soc. 2011, 133, 6110-6113
80. Wu, R.; Wang, S.; Zhou, N.; Cao, Z.; Zhang, Y. J. Am. Chem. Soc. 2010, 132, 9471-9479
81. Xu, D. G.; Guo, H. J. Am. Chem. Soc. 2009, 131, 9780-9788
82. Rao, L.; Cui, Q.; Xu, X. J. Am. Chem. Soc. 2010, 132, 18092-18102
83. Marti, S.; Moliner, V.; Tuñón, I. J. Chem. Theory Comput. 2005, 1, 1008-1016
84. Claeyssens, F.; Harvey, J. N.; Manby, F. R.; Mata, R. A.; Mulholland, A. J.; Ranaghan, K. E.; Schutz, M.; Thiel, S.; Thiel, W.; Werner, H. J. Angew. Chem., Int. Ed. 2006, 45, 6856-6859
85. Trajbl, M.; Hong, G. Y.; Warshel, A. J. Phys. Chem. B 2002, 106, 13333-13343
86. Plotnikov, N. V.; Kamerlin, S. C. L.; Warshel, A. J. Phys. Chem. B 2011, 115, 7950-7962
87. Rod, T. H.; Ryde, U. J. Chem. Theory Comput. 2005, 1, 1240-1251
88. Heimdal, J.; Kaukonen, M.; Srnec, M.; Rulisek, L.; Ryde, U. ChemPhysChem. 2011, 12, 3337-3347
89. Retegan, M.; Martins-Costa, M.; Ruiz-Lopez, M. F. J. Chem. Phys. 2010, 133, 064103
90. Cook, P. F.; Cleland, W. W. Enzyme kinetics and mechanism; Garland Science: New York, 2007.
91. Cui, Q.; Karplus, M. J. Am. Chem. Soc. 2001, 122, 2284-2290
92. Zienau, J.; Cui, Q. J. Phys. Chem. B 2012, 116, 12522-12534
93. Andrews, L. D.; Deng, H.; Herschlag, D. J. Am. Chem. Soc. 2011, 133, 11621-11631
94. Rosta, E.; Kamerlin, S. C. L.; Warshel, A. Biochemistry 2008, 47, 3725-3735
95. Bobyr, E.; Lassila, J. K.; Wiersma-Koch, H. I.; Fenn, T. D.; Lee, J. J.; Nikolic-Hughes, I.; Hodgson, K. O.; Rees, D. C.; Hedman, B.; Herschlag, D. J. Mol. Biol. 2011, 415, 102-117
96. Gaus, M.; Cui, Q.; Elstner, M. J. Chem. Theory Comput. 2011, 7, 931-948
97. Nielsen, S. O.; Bulo, R. E.; Moore, P. B.; Ensing, B. Phys. Chem. Chem. Phys. 2010, 12, 12401-12414
98. Park, K.; Götz, A. W.; Walker, R. C.; Paesani, F. J. Chem. Theory Comput.. 2012, 8, 2868-2877
99. Jensen, R. A. Annu. Rev. Microbiol. 1976, 30, 409-425
100. O'Brien, P. J.; Herschlag, D. Chem. Biol. 1999, 6, R91-R105
101. Kazlauskas, R. J. Curr. Opin. Chem. Biol. 2005, 9, 195-201
102. Hult, K.; Berglund, P. Trends Biotechnol. 2007, 25, 231-238
103. Nobeli, I.; Favia, A. D.; Thornton, J. M. Nat. Biotechnol. 2009, 27, 157-167
104. Zalatan, J. G.; Herschlag, D. Nat. Chem. Biol. 2009, 5, 516-520
105. Khersonsky, O.; Tawfik, D. S. Annu. Rev. Biochem. 2010, 79, 471-505
106. Mohamed, M. F.; Hollfelder, F. Biochim. Biophys. Acta, Proteins Proteomics 2013, 1834, 417-424
107. Ben-David, M.; Wieczorek, G.; Elias, M.; Silman, I.; Sussman, J. L.; Tawfik, D. S. J. Mol. Biol. 2013, 425, 1028-1038
108. McWhirter, C.; Lund, E. A.; Tanifum, E. A.; Feng, G.; Sheikh, Q. I.; Hengge, A. C.; Williams, N. H. J. Am. Chem. Soc. 2008, 130, 13673-13682
109. Thornton, J. W. Nat. Rev. Genet. 2004, 5, 366-375
110. Harms, M. J.; Thornton, J. W. Curr. Opin. Struct. Biol. 2010, 20, 360-366
111. Huang, R. Q.; Hippauf, F.; Rohrbeck, D.; Haustein, M.; Wenke, K.; Feike, J.; Sorrelle, N.; Piechulla, B.; Barkman, T. J. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 2966-2971-2971