Theoretical investigation of the binding free energies and key substrate-recognition components of the replication fidelity of human DNA polymerase β

Journal of Physical Chemistry B

Volumn 106, Issue 22, 2002, Pages 5739-5753

  Florián, Jan ^a   Goodman, Myron F ^a   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REPLICATION FIDELITY;

BINDING ENERGY; COMPUTER SIMULATION; CONFORMATIONS; CRYSTAL STRUCTURE; FREE ENERGY; MOLECULAR DYNAMICS; SOLUTIONS; SUBSTITUTION REACTIONS; X RAY CRYSTALLOGRAPHY;

DNA;

EID: 0037030875     PISSN: 10895647     EISSN: None     Source Type: Journal    
DOI: 10.1021/jp020790u     Document Type: Article

References (72)

1. Kornberg, A.; Baker, T.A. DNA Replication; W.H. Freeman: New York, 1992.
2. Goodman, M.F.; Creighton, S.; Bloom, L.B.; Petruska, J. Crit. Rev. Biochem. Mol. Biol. 1993, 28, 83.
3. Petruska, J.; Goodman, M.F.; Boosalis, M.S.; Sowers, L.C.; Cheong, C.; I. Tinoco, J. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 6252.
4. Echols, H.; Goodman, M.F. Annu. Rev. Biochem. 1991, 60, 477.
5. Zhong, X.J.; Patel, S.S.; Werneburg, B.G.; Tsai, M.D. Biochemistry 1997, 1997, 11891.
6. Johnson, K.A. Annu. Rev. Biochem. 1993, 32, 685.
7. Arndt, J.W.; Gong, W.; Zhong, X.; Showalter, A.K.; Liu, J.; Dunlap, C.A.; Lin, Z.; Paxson, C.; Tsai, M.-D.; Chan, M.K. Biochemistry 2001, 40, 5368.
8. Galas, D.J.; Branscomb, E.W. . Mol. Biol. 1978, 88, 653.
9. Clayton, L.K.; Goodman, M.F.; Branscomb, E.W.; Galas, D. J. Biol. Chem. 1979, 254, 1902.
10. Davies, J.F.; Almassy, R.J.; Hostomska, Z.; Ferre, R.A.; Hostomsky, Z. Cell 1994, 76, 1123.
11. Pelletier, H.; Sawaya, M.R.; Kumar, A.; Wilson, S.H.; Kraut, J. Science 1994, 264, 1891.
12. Sawaya, M.R.; Pelletier, H.; Kumar, A.; Wilson, S.H.; Kraut, J. Science 1994, 264, 1930.
13. Abashkin, Y.G.; Erickson, J.W.; Burt, S.K. J. Phys. Chem. B 2001, 105, 287.
14. Fothergill, M.; Goodman, M.F.; Petruska, J.; Warshel, A. J. Am. Chem. Soc. 1995, 117, 11619.
15. Srivastava, D.K.; Vande Berg, B.J.; Prasad, R.; Molina, J.T.; Beard, W.A.; Tomkinson, A.E.; Wilson, S.H. J. Biol. Chem. 1998, 273, 21203.
16. Sawaya, M.R.; Prasad, R.; Wilson, S.H.; Kraut, J.; Pelletier, H. Biochemistry 1997, 36, 11205.
17. Kollman, P.A. Chem. Rev. 1993, 93, 2395.
18. Warshel, A. Computer Modeling of Chemical Reactions in Enzymes and Solutions; John Wiley & Sons: New York, 1991.
19. Straatsma, T.P.; McCammon, J.A. Annu. Rev. Phys. Chem. 1992, 43, 407.
20. Warshel, A.; Sussman, F.; Hwang, J.-K. J. Mol. Biol. 1988, 201, 139.
21. Florián, J.; Goodman, M.F.; Warshel, A. J. Phys. Chem. B 2000, 104, 10092.
22. Cubero, E.; Laughton, C.A.; Luque, F.J.; Orozco, M. J. Am. Chem. Soc. 2000, 122, 6891.
23. Lee, F.S.; Chu, Z.T.; Bolger, M.B.; Warshel, A. Prot. Eng. 1992, 5, 215.
24. Sham, Y.Y.; Chu, Z.T.; Tao, H.; Warshel, A. Proteins: Struct., Funct., Genet. 2000, 39, 393.
25. Marcus, R.A.; Sutin, N. Biochim. Biophys. Acta 1985, 811, 265.
26. Warshel, A.; Parson, W.W.Q. Rev. Biophy. 2001, 34, 563.
27. Zhou, H.X.; Szabo, A. J. Chem. Phys. 1995, 103, 3481.
28. King, G.; Warshel, A. J. Chem. Phys. 1990, 93, 8682.
29. Florián, J.; Warshel, A. J. Phys. Chem. B 1999, 103, 10282.
30. Cornell, W.D.; Cieplak, P.; Bayly, C.I.; Gould, I.R.; Merz, K.M. Jr. Ferguson D.M. Spellmeyer D.C. Fox T.; Caldwell, J.W.; Kollman, P.A. J. Am. Chem. Soc. 1995, 117, 5179.
31. Marelius, J.; Kolmodin, K.; Feierberg, I.; Åqvist, J. J. Mol. Graphics Model. 1999, 16, 213.
32. Cheatham, T.E., III; Miller, J.L.; Fox, T.; Darden, T.A.; Kollman, P.A. J. Am. Chem. Soc. 1995, 117, 4193.
33. Cubero, E.; Sherer, E.C.; Luque, F.J.; Orozco, M.; Laughton, C.A. J. Am. Chem. Soc. 1999, 121, 8653.
34. Jayaram, B.; Sprous, D.; Young, M.A.; Beveridge, D.L. J. Am. Chem. Soc. 1998, 120, 10629.
35. Spackova, N.; Berger, I.; Egli, M.; Sponer, J. J. Am. Chem. Soc. 1998, 120, 6147.
36. Kollman, P.A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S.H.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, 04 Cieplak, P.; Srinivasan, J.; Case, D.A.; Cheatham, T.E. Acc. Chem. Res. 2000, 33, 889.
37. Warshel, A.; Creighton, S., In Computer Simulation of Biomolecular Systems; van Gunsteren, W.F., Wiener, P.K., Eds.; ESCOM: Leiden, 1989; p 120.
38. SYBYL 6.6; Tripos, Inc.: 1699 South Hanley Rd., St. Louis, MO, 63144, 1999.
39. King, G.; Warshel, A. J. Chem. Phys. 1989, 91, 3647.
40. Sham, Y.Y.; Warshel, A. J. Chem. Phys. 1998, 109, 7940.
41. Lee, F.S.; Warshel, A. J. Chem. Phys. 1992, 97, 3100.
42. Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Gill, P.M.W.; Johnson, B.G.; Robb, M.A.; Cheeseman, J.R.; Keith, T.; Petersson, G.A.; Montgomery, J.A.; Raghavachari, K.; Al-Laham, M.A.; Zakrzewski, V.G.; Ortiz, J.V.; Foresman, J.B.; Cioslowski, J.; Stefanov, B.B.; Nanayakkara, A.; Challacombe, M.; Peng, C.Y.; Ayala, P.Y.; Chen, W.; Wong, M.W.; Andres, J.L.; Replogle, E.S.; Gomperts, R.; Martin, R.L.; Fox, D.J.; Binkley, J.S.; Defrees, D.J.; Baker, J.; Stewart, J.P.; Head-Gordon, M.; Gonzalez, C.; Pople, J.A. Gaussian94, revision D.2; Gaussian, Inc.: Pittsburgh, 1995.
43. Lee, F.S.; Chu, Z.T.; Warshel, A. J. Comput. Chem. 1993, 14, 161.
44. Boosalis, M.S.; Mosbaugh, D.W.; Hamatake, R.; Sugino, A.; Kunkel, T.A.; Goodman, M.F. J. Biol. Chem. 1989, 264, 11360.
45. Chagovetz, A.M.; Sweasy, J.B.; Preston, B.D. J. Biol. Chem. 1997, 272, 27501.
46. Werneburg, B.G.; Ahn, J.; Zhong, X.; Hondal, R.J.; Kraynov, V.S.; Tsai, M.-D. Biochemistry 1996, 35, 7041.
47. Sowers, L.C.; Shaw, B.R.; Veigl, M.L.; Sedwick, W.D. Mutat. Res. 1987, 177, 201.
48. Gao, X.; Patel, D. J. Am. Chem. Soc. 1988, 110, 8.
49. Hunter, W.N.; Brown, T.; Kennard, O. Nature 1986, 320, 552.
50. It should be noted that because at present the most theoretical calculations of complex biological systems do not give the right answers, the choice of the appropriate studied system is as important as the choice of the experimental conditions in the laboratory (for example, the choice of the right conditions for the crystallization of proteins). Some conditions give stable results whereas others do not. In our case, the conditions for facile experimental studies (substrate fidelity) and computer simulations (template fidelity, neutral anti-anti base pairs) differ. This does not mean, however, that either the experimental or theoretical results should be considered incapable of addresing important fidelity issues just because they are not complete enough.
51. Kiefer, J.R.; Mao, C.; Braman, J.C.; Beese, L.S. Nature 1998, 391, 304.
52. Baeyens, K.J.; Bondt, H.L.D.; Pardi, A.; Holbroo, S.R. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 12851.
53. Prive, G.G.; Heinemann, U.; Chandrasegaran, S.; Kan, L.S.; Kopka, M.L.; Dickerson, R.E. Science 1987, 238, 498.
54. Brown, T.; Hunter, W.N.; Kneale, G.; Kennard, O. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 2402.
55. Brown, T.; Leonard, G.A.; Booth, E.D.; Chambers, J. J. Mol. Struct. 1989, 207, 445.
56. Fazakerley, G.V.; Quignard, E.; Woisard, A.; Guschlbauer, W.; van der Marel, G.A.; van Boom, J.H.; Jones, M.; Radman, M. EMBO J. 1986, 5, 3697.
57. Allawi, H.T.; SantaLucia, J., Jr. Biochemistry 1997, 36, 10581.
58. Kennard, O. J. Biomol. Struct. Dyn. 1985, 3, 205.
59. Carroll, S.S.; Benkovic, S.J. Chem. Rev. 1990, 90, 1291.
60. Fersht, A.R. Enzyme Structure and Mechanism; W.H. Freeman and Company: New York, 1985.
61. Åqvist, J.; Medina, C.; Samuelson, J.E. Protein Eng. 1994, 7, 385.
62. Hansson, T.; Marelius, J.; Åqvist, J. J. Comput.-Aided Mol. Des. 1998, 12, 27.
63. Paulsen, M.D.; Ornstein, R.L. Protein Eng. 1996, 9, 567.
64. Jones-Hertzog, D.K.; Jorgensen, W.L. J. Med. Chem. 1997, 41, 55272.
65. Kunkel, T.A. J. Biol. Chem. 1985, 260, 5787.
66. (a) Hobza, P.; Sandorfy, C. J. Am. Chem. Soc. 1987, 109, 1302.
67. (b) Hrouda, V.; Florian, J.; Hobza, P. J. Phys. Chem. 1993, 97, 1542.
68. (c) Florián, J.; Leszczynski, J.; Scheiner, S. Mol. Phys. 1995, 84, 469.
69. (d) Sponer, J.; Leszczynski, J.; Hobza, P. J. Phys. Chem. 1996, 100, 1965.
70. Hobza, P.; Kabelac, M.; Sponer, J.; Mejzlik, P.; Vondrasek, J. J. Comput. Chem. 1997, 18, 1136.
71. Cabani, S.; Gianni, P.; Mollica, V.; Lepori, L. J. Solution Chem. 1981, 10, 563.
72. Wolfenden, R. Science 1983, 222, 1087.