Water and Biomolecules pp 97-121

Part of the Biological and Medical Physics, Biomedical book series (BIOMEDICAL)

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Protein Folding and Binding: Effective Potentials, Replica Exchange Simulations, and Network Models

  • A. K. Felts
  • M. Andrec
  • E. Gallicchio
  • R. M. Levy

Abstract

Advances in computational biophysics depend on the development of accurate effective potentials and powerful sampling methods to traverse rugged energy landscapes. We have developed an approach that makes use of the combined power of replica exchange simulations and a network model for kinetics. We carry out replica exchange simulations to generate a very large set of states using an all-atom effective potential function and construct a kinetic model for the folding, using an ansatz that allows kinetic transitions between states based on structural similarity. We are also using replica exchange simulations to study the binding of ligands to proteins such as cytochrome P450. A better understanding of the relationship between the physical kinetics of the systems being studied to their “kinetics” in the replica exchange ensemble is needed to use this new technology to maximum advantage. To illustrate some of the challenges, we will discuss the results using a network model to “simulate” replica exchange simulations of protein folding.

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References

  1. 1.
    W.A. Eaton, V. Muñoz, S.J. Hagen, G.S. Jas, L.J. Lapidus, E.R. Henry, J. Hofrichter, Annu. Rev. Biophys. Biomol. Struct. 29, 327 (2000)PubMedCrossRefGoogle Scholar
  2. 2.
    J.K. Myers, T.G. Oas, Annu. Rev. Biochem. 71, 783 (2002)PubMedCrossRefGoogle Scholar
  3. 3.
    A.R. Dinner, A. Šali, L.J. Smith, C.M. Dobson, M. Karplus, Trends Biochem.Sci. 25, 331 (2000)PubMedCrossRefGoogle Scholar
  4. 4.
    J. Rumbley, L. Hoang, L. Mayne, S.W. Englander, Proc. Natl. Acad. Sci. USA 98, 105 (2001)PubMedCrossRefGoogle Scholar
  5. 5.
    A.R. Fersht, V. Daggett, Cell 108, 573 (2002)PubMedCrossRefGoogle Scholar
  6. 6.
    M. Vendruscolo, E. Paci, Curr. Opin. Struct. Biol. 13, 82 (2003)PubMedCrossRefGoogle Scholar
  7. 7.
    T. Lazaridis, M. Karplus, J. Mol. Biol. 288, 477 (1999)PubMedCrossRefGoogle Scholar
  8. 8.
    D. Petrey, B. Honig, Protein Sci. 9, 2181 (2000)PubMedCrossRefGoogle Scholar
  9. 9.
    T. Lazaridis, M. Karplus, Curr. Opin. Struct. Biol. 10, 139 (2000)PubMedCrossRefGoogle Scholar
  10. 10.
    B.D. Bursulaya, C.L. Brooks III, J. Phys. Chem. B 104, 12378 (2000)CrossRefGoogle Scholar
  11. 11.
    B.N. Dominy, C.L. Brooks III, J. Comput. Chem. 23, 147 (2002)PubMedCrossRefGoogle Scholar
  12. 12.
    Y. Liu, D.L. Beveridge, Proteins: Struct. Funct. Genet. 46, 128 (2002)CrossRefGoogle Scholar
  13. 13.
    M. Feig, C.L. Brooks III, Proteins: Struct. Funct. Genet. 49, 232 (2002)CrossRefGoogle Scholar
  14. 14.
    A.K. Felts, E. Gallicchio, A. Wallqvist, R.M. Levy, Proteins: Struct. Funct. Genet. 48, 404 (2002)CrossRefGoogle Scholar
  15. 15.
    Y.M. Rhee, V.S. Pande, Biophys. J. 84, 775 (2003)PubMedCrossRefGoogle Scholar
  16. 16.
    R.M. Levy, E. Gallicchio, Annu. Rev. Phys. Chem. 49, 531 (1998)PubMedCrossRefGoogle Scholar
  17. 17.
    A.R. Dinner, T. Lazaridis, M. Karplus, Proc. Natl. Acad. Sci. USA 96, 9068 (1999)PubMedCrossRefGoogle Scholar
  18. 18.
    B. Zagrovic, E.J. Sorin, V. Pande, J. Mol. Biol. 313, 151 (2001)PubMedCrossRefGoogle Scholar
  19. 19.
    R. Zhou, B.J. Berne, Proc. Natl. Acad. Sci. USA 99, 12777 (2002)PubMedCrossRefGoogle Scholar
  20. 20.
    R. Zhou, Proteins: Struct. Funct. Genet. 53, 148 (2003)CrossRefGoogle Scholar
  21. 21.
    B. Roux, T. Simonson, Biophys. Chem. 78, 1 (1999)PubMedCrossRefGoogle Scholar
  22. 22.
    D. Bashford, D.A. Case, Annu. Rev. Phys. Chem. 51, 129 (2000)PubMedCrossRefGoogle Scholar
  23. 23.
    T. Simonson, Curr. Opin. Struct. Biol. 11, 243 (2001)PubMedCrossRefGoogle Scholar
  24. 24.
    J. Zhu, Y. Shi, H. Liu, J. Phys. Chem. B 106, 4844 (2002)CrossRefGoogle Scholar
  25. 25.
    M. Król, J. Comput. Chem. 24, 531 (2003)PubMedCrossRefGoogle Scholar
  26. 26.
    A. Suenaga, J. Mol. Struct. (Theochem) 634, 235 (2003)CrossRefGoogle Scholar
  27. 27.
    E. Gallicchio, R.M. Levy, J. Comput. Chem. 25, 479 (2004)PubMedCrossRefGoogle Scholar
  28. 28.
    B. Marten, K. Kim, C. Cortis, R.A. Friesner, R.B. Murphy, M.N. Ringnalda, D. Sitkoff, B. Honig, J. Phys. Chem. 100, 11775 (1996)CrossRefGoogle Scholar
  29. 29.
    D. Qiu, P.S. Shenkin, F.P. Hollinger, W.C. Still, J. Phys. Chem. A 101, 3005 (1997)CrossRefGoogle Scholar
  30. 30.
    N. Froloff, A. Windemuth, B. Honig, Protein Sci. 6, 1293 (1997)PubMedCrossRefGoogle Scholar
  31. 31.
    C.J. Cramer, D. Truhlar, Chem. Rev. 99, 2161 (1999)PubMedCrossRefGoogle Scholar
  32. 32.
    E. Gallicchio, L.Y. Zhang, R.M. Levy, J. Comp. Chem. 23, 517 (2002)CrossRefGoogle Scholar
  33. 33.
    M.S. Lee, M. Feig, F.R. Salsbury Jr., C.L. Brooks III, J. Comp. Chem. 24(11), 1348 (2003)CrossRefGoogle Scholar
  34. 34.
    J. Tomasi, M. Persico, Chem. Rev. 94, 2027 (1994)CrossRefGoogle Scholar
  35. 35.
    C.M. Cortis, R.A. Friesner, J. Comp. Chem. 18, 1591 (1997)CrossRefGoogle Scholar
  36. 36.
    W. Rocchia, S. Sridharan, A. Nicholls, E. Alexov, A. Chiabrera, B. Honig, J. Comp. Chem. 23, 128 (2002)CrossRefGoogle Scholar
  37. 37.
    W.C. Still, A. Tempczyk, R.C. Hawley, T. Hendrickson, J. Am. Chem. Soc. 112, 6127 (1990)CrossRefGoogle Scholar
  38. 38.
    A. Onufriev, D. Bashford, D.A. Case, J. Phys. Chem. B 104, 3712 (2000)CrossRefGoogle Scholar
  39. 39.
    A. Ghosh, C.S. Rapp, R.A. Friesner, J. Phys. Chem. B 102, 10983 (1998)CrossRefGoogle Scholar
  40. 40.
    L. Zhang, E. Gallicchio, R. Friesner, R.M. Levy, J. Comp. Chem. 22, 591 (2001)CrossRefGoogle Scholar
  41. 41.
    M. Schaefer, C. Froemmel, J. Mol. Biol. 216, 1045 (1990)PubMedCrossRefGoogle Scholar
  42. 42.
    G.D. Hawkins, C.J. Cramer, D.G. Truhlar, J. Phys. Chem. 100, 19824 (1996)CrossRefGoogle Scholar
  43. 43.
    M. Schaefer, M. Karplus, J. Phys. Chem. 100, 1578 (1996)CrossRefGoogle Scholar
  44. 44.
    B.N. Dominy, C.L. Brooks III, J. Phys. Chem. B 103, 3765 (1999)CrossRefGoogle Scholar
  45. 45.
    V. Tsui, D.A. Case, Biopolymers 56, 275 (2000)PubMedCrossRefGoogle Scholar
  46. 46.
    A. Ben-Naim, Hydrophobic Interactions (Plenum Press, New York, 1980)Google Scholar
  47. 47.
    W. Kauzmann, Adv. Prot. Chem. 14, 1 (1959)CrossRefGoogle Scholar
  48. 48.
    K.A. Dill, Biochemistry 29, 7133 (1990)PubMedCrossRefGoogle Scholar
  49. 49.
    P.L. Privalov, G.I. Makhatadze, J. Mol. Biol. 232, 660 (1993)PubMedCrossRefGoogle Scholar
  50. 50.
    B. Honig, A.S. Yang, Ad. Prot. Chem. 46, 27 (1995)CrossRefGoogle Scholar
  51. 51.
    J.M. Sturtevant, Proc. Natl. Acad. Sci. USA 74, 2236 (1977)PubMedCrossRefGoogle Scholar
  52. 52.
    D.H. Williams, M.S. Searle, J.P. Mackay, U. Gerhard, R.A. Maplestone, Proc. Natl. Acad. Sci. USA 90, 1172 (1993)PubMedCrossRefGoogle Scholar
  53. 53.
    X. Siebert, G. Hummer, Biochemistry 41, 2965 (2002)Google Scholar
  54. 54.
    T. Ooi, M. Oobatake, G. Nemethy, A. Sheraga, Proc. Natl. Acad. Sci. USA 84, 3086 (1987)PubMedCrossRefGoogle Scholar
  55. 55.
    M.R. Lee, Y. Duan, P.A. Kollman, Proteins 39(4), 309 (2000)PubMedCrossRefGoogle Scholar
  56. 56.
    P.H. Hünenberger, V. Helms, N. Narayana, S.S. Taylor, J.A. McCammon, Biochemistry 38(8), 2358 (1999)PubMedCrossRefGoogle Scholar
  57. 57.
    T. Simonson, A.T. Brünger, J. Phys. Chem. 98, 4683 (1994)CrossRefGoogle Scholar
  58. 58.
    D. Sitkoff, K.A. Sharp, B. Honig, J. Phys. Chem. 98, 1978 (1994)CrossRefGoogle Scholar
  59. 59.
    C.S. Rapp, R.A. Friesner, Proteins: Struct. Funct. Genet. 35, 173 (1999)CrossRefGoogle Scholar
  60. 60.
    F. Fogolari, G. Esposito, P. Viglino, H. Molinari, J. Comp. Chem. 22, 1830 (2001)CrossRefGoogle Scholar
  61. 61.
    E. Pellegrini, M.J. Field, J. Phys. Chem. A 106, 1316 (2002)CrossRefGoogle Scholar
  62. 62.
    C. Curutchet, C.J. Cramer, D.G. Truhlar, M.F. Ruiz-Lòpez, D. Rinaldi, M. Orozco, F.J. Luque, J. Comp. Chem. 24, 284 (2003)CrossRefGoogle Scholar
  63. 63.
    A. Wallqvist, D.G. Covell, J. Phys. Chem. 99, 13118 (1995)CrossRefGoogle Scholar
  64. 64.
    E. Gallicchio, M.M. Kubo, R.M. Levy, J. Phys. Chem. B 104, 6271 (2000)CrossRefGoogle Scholar
  65. 65.
    R.M. Levy, L.Y. Zhang, E. Gallicchio, A.K. Felts, J. Am. Chem. Soc. 25(31), 9523 (2003)CrossRefGoogle Scholar
  66. 66.
    M. Nina, D. Beglov, B. Roux, J. Phys. Chem. B 101, 5239 (1997)CrossRefGoogle Scholar
  67. 67.
    Y. Sugita, Y. Okamoto, Chem. Phys. Lett. 314, 141 (1999)CrossRefGoogle Scholar
  68. 68.
    A. Mitsutake, Y. Sugita, Y. Okamoto, Biopolymers 60, 96 (2001)PubMedCrossRefGoogle Scholar
  69. 69.
    S. Gnanakaran, H. Nymeyer, J. Portman, K.Y. Sanbonmatsu, A.E. García, Curr. Opin. Struct. Biol. 13, 168 (2003)PubMedCrossRefGoogle Scholar
  70. 70.
    A.E. García, K.Y. Sanbonmatsu, Proteins: Struct. Funct. Genet. 42, 345 (2001)CrossRefGoogle Scholar
  71. 71.
    R. Zhou, B.J. Berne, R. Germain, Proc. Natl. Acad. Sci. USA 98, 14931 (2001)PubMedCrossRefGoogle Scholar
  72. 72.
    R.H. Swendsen, J.S. Wang, Phys. Rev. Lett. 57, 2607 (1986)PubMedCrossRefGoogle Scholar
  73. 73.
    K. Hukushima, K. Nemoto, J. Phys. Soc. Jpn. 65, 1604 (1996)CrossRefGoogle Scholar
  74. 74.
    H. Nymeyer, S. Gnanakaran, A.E. García, Meth. Enzymol. 383, 119 (2004)PubMedCrossRefGoogle Scholar
  75. 75.
    A.K. Felts, Y. Harano, E. Gallicchio, R.M. Levy, Proteins: Struct. Funct. Bioin-form. 56, 310 (2004)CrossRefGoogle Scholar
  76. 76.
    M. Cecchini, F. Rao, M. Seeber, A. Caflisch, J. Chem. Phys. 121, 10748 (2004)PubMedCrossRefGoogle Scholar
  77. 77.
    H.H.G. Tsai, M. Reches, C.J. Tsai, K. Gunasekaran, E. Gazit, R. Nussinov, Proc. Natl. Acad. Sci. USA 102, 8174 (2005)PubMedCrossRefGoogle Scholar
  78. 78.
    A. Baumketner, J.E. Shea, Biophys. J. 89, 1493 (2005)PubMedCrossRefGoogle Scholar
  79. 79.
    G.M. Verkhivker, P.A. Rejto, D. Bouzida, S. Arthurs, A.B. Colson, S.T. Freer, D.K. Gehlhaar, V. Larson, B.A. Luty, T. Marrone, P.W. Rose, Chem. Phys. Lett. 337, 181 (2001)CrossRefGoogle Scholar
  80. 80.
    K.P. Ravindranathan, E. Gallicchio, R.A. Friesner, A.E. McDermott, R.M. Levy, J. Am. Chem. Soc. 128, 5786 (2006)PubMedCrossRefGoogle Scholar
  81. 81.
    F. Rao, A. Caflisch, J. Chem. Phys. 119, 4035 (2003)CrossRefGoogle Scholar
  82. 82.
    M.M. Seibert, A. Patriksson, B. Hess, D. van der Spoel, J. Mol. Biol. 354, 173 (2005)PubMedCrossRefGoogle Scholar
  83. 83.
    D.A. Kofke, J. Chem. Phys. 117, 6911 (2002)CrossRefGoogle Scholar
  84. 84.
    A. Kone, D.A. Kofke, J. Chem. Phys. 122, 206101 (2005)PubMedCrossRefGoogle Scholar
  85. 85.
    C. Predescu, M. Predescu, C.V. Ciobanu, J. Chem. Phys. 120, 4119 (2004)PubMedCrossRefGoogle Scholar
  86. 86.
    C. Predescu, M. Predescu, C.V. Ciobanu, J. Phys. Chem. B 109, 4189 (2005)PubMedCrossRefGoogle Scholar
  87. 87.
    N. Rathore, M. Chopra, J.J. de Pablo, J. Chem. Phys. 122, 024111 (2005)PubMedCrossRefGoogle Scholar
  88. 88.
    S. Trebst, M. Troyer, U.H.E. Hansmann, J. Chem. Phys. 124, 174903 (2006)PubMedCrossRefGoogle Scholar
  89. 89.
    D.M. Zuckerman, E. Lyman, J. Chem. Theory Comput. 2, 1200 (2006)CrossRefGoogle Scholar
  90. 90.
    D.M. Zuckerman, J. Chem. Theory Comput. 2, 1693 (2006)CrossRefGoogle Scholar
  91. 91.
    D.A.C. Beck, G.W.N. White, V. Daggett, J. Struct. Biol. 157, 514 (2007)PubMedCrossRefGoogle Scholar
  92. 92.
    S.I. Segawa, M. Sugihara, Biopolymers 23, 2473 (1984)PubMedCrossRefGoogle Scholar
  93. 93.
    M. Oliveberg, Y.J. Tan, A.R. Fersht, Proc. Natl. Acad. Sci. USA 92, 8926 (1995)PubMedCrossRefGoogle Scholar
  94. 94.
    V. Muñoz, P.A. Thompson, J. Hofrichter, W.A. Eaton, Nature 390, 196 (1997)PubMedCrossRefGoogle Scholar
  95. 95.
    M. Karplus, J. Phys. Chem. B 104, 11 (2000)CrossRefGoogle Scholar
  96. 96.
    P. Ferrara, J. Apostolakis, A. Caflisch, J. Phys. Chem. B 104, 5000 (2000)CrossRefGoogle Scholar
  97. 97.
    W.Y. Yang, M. Gruebele, Biochemistry 43, 13018 (2004)PubMedCrossRefGoogle Scholar
  98. 98.
    M.L. Scalley, D. Baker, Proc. Natl. Acad. Sci. USA 94, 10636 (1997)PubMedCrossRefGoogle Scholar
  99. 99.
    J.D. Bryngelson, P.G. Wolynes, J. Phys. Chem. 93, 6902 (1989)CrossRefGoogle Scholar
  100. 100.
    M. Andrec, A.K. Felts, E. Gallicchio, R.M. Levy, Proc. Natl. Acad. Sci. USA 102, 6801Google Scholar
  101. 101.
    A.K. Felts, E. Gallicchio, D. Chekmarev, K.A. Paris, R.A. Friesner, R.M. Levy, J. Chem. Theory Comput. 4, 855 (2008)PubMedCrossRefGoogle Scholar
  102. 102.
    W. Zheng, M. Andrec, E. Gallicchio, R.M. Levy, Proc. Natl. Acad. Sci. USA 104, 15340 (2007)PubMedCrossRefGoogle Scholar
  103. 103.
    W. Zheng, M. Andrec, E. Gallicchio, R.M. Levy, J. Phys. Chem. B 112, 6083 (2008)PubMedCrossRefGoogle Scholar
  104. 104.
    Y.N. Vorobjev, J.C. Almagro, J. Hermans, Proteins: Struc. Func. Gen. 32, 399 (1998)CrossRefGoogle Scholar
  105. 105.
    W.L. Jorgensen, D.S. Maxwell, J. Tirado-Rives, J. Am. Chem. Soc. 118, 11225 (1996)CrossRefGoogle Scholar
  106. 106.
    G.A. Kaminski, R.A. Friesner, J. Tirado-Rives, W.L. Jorgensen, J. Phys. Chem. B 105, 6474 (2001)CrossRefGoogle Scholar
  107. 107.
    J.L. Banks, H.S. Beard, Y. Cao, A.E. Cho, W. Damm, R. Farid, A.K. Felts, T.A. Halgren, D.T. Mainz, J.R. Maple, R. Murphy, D.M. Philipp, M.P. Repasky, L.Y. Zhang, B.J. Berne, R.A. Friesner, E. Gallicchio, R.M. Levy, J. Comput. Chem. 26, 1752 (2005)PubMedCrossRefGoogle Scholar
  108. 108.
    W.L. Jorgensen, N.A. McDonald, Theochem 424, 145 (1998)CrossRefGoogle Scholar
  109. 109.
    W.L. Jorgensen, N.A. McDonald, J. Phys. Chem. B 102, 8094 (1998)Google Scholar
  110. 110.
    R.C. Rizzo, W.L. Jorgensen, J. Am. Chem. Soc. 121, 4827 (1999)CrossRefGoogle Scholar
  111. 111.
    E.K. Watkins, W.L. Jorgensen, J. Phys Chem. A 105, 4118 (2001)CrossRefGoogle Scholar
  112. 112.
    D.J. Weininger, J. Chem. Info. Comput. Sci. 28, 31 (1988)Google Scholar
  113. 113.
    J.A. Wagoner, N.A. Baker, Proc. Natl. Acad. Sci. USA 103, 8331 (2006)PubMedCrossRefGoogle Scholar
  114. 114.
    R. Geney, M. Layten, R. Gomperts, V. Hornak, C. Simmerling, J. Chem. Theory Comput. 2, 115 (2006)CrossRefGoogle Scholar
  115. 115.
    S.B. Ozkan, K.A. Dill, I. Bahar, Protein Sci. 11, 1958 (2002)PubMedCrossRefGoogle Scholar
  116. 116.
    F. Rao, A. Caflisch, J. Mol. Biol. 342, 299 (2004)PubMedCrossRefGoogle Scholar
  117. 117.
    N. Singhal, C.D. Snow, V.S. Pande, J. Chem. Phys. 121, 415 (2004)PubMedCrossRefGoogle Scholar
  118. 118.
    W.C. Swope, J.W. Pitera, F. Suits, J. Phys. Chem. B 108, 6571 (2004)CrossRefGoogle Scholar
  119. 119.
    W.C. Swope, J.W. Pitera, F. Suits, M. Pitman, M. Eleftheriou, B.G. Fitch, R.S. Germain, A. Rayshubski, T.L.C. Ward, Y. Zhestkov, R. Zhou, J. Phys. Chem. B 108, 6582 (2004)CrossRefGoogle Scholar
  120. 120.
    D.S. Chekmarev, T. Ishida, R.M. Levy, J. Phys. Chem. B 108, 19487 (2004)CrossRefGoogle Scholar
  121. 121.
    D.A. Evans, D.J. Wales, J. Chem. Phys. 121, 1080 (2004)PubMedCrossRefGoogle Scholar
  122. 122.
    D.T. Gillespie, Markov Processes: An Introduction for Physical Scientists (Academic Press, Boston, 1992)Google Scholar
  123. 123.
    M.P. Jacobson, D.L. Pincus, C.S. Rapp, T.J.F. Day, B. Honig, D.E. Shaw, R.A. Friesner, Proteins: Struct. Funct. Bioinform. 55, 351 (2004)CrossRefGoogle Scholar
  124. 124.
    K. Zhu, D.L. Pincus, S. Zhao, R.A. Friesner, Proteins: Struct. Funct. Bioinform. 65, 438 (2006)CrossRefGoogle Scholar
  125. 125.
    J.A. Hartigan, M.A. Wong, Appl. Stat. 28, 100 (1979)CrossRefGoogle Scholar
  126. 126.
    A. Fiser, R.K.G. Do, A. Sali, Protein Sci. 9, 1753 (2000)PubMedCrossRefGoogle Scholar
  127. 127.
    Z.X. Xiang, C.S. Soto, B. Honig, Proc. Natl. Acad. Sci. USA 99, 7432 (2002)PubMedCrossRefGoogle Scholar
  128. 128.
    F.J. Blanco, G. Rivas, L. Serrano, Nat. Struc. Biol. 1, 584 (1994)CrossRefGoogle Scholar
  129. 129.
    F.J. Blanco, L. Serrano, Eur. J. Biochem. 230, 634 (1995)PubMedCrossRefGoogle Scholar
  130. 130.
    V. Muñoz, E.R. Henry, J. Hofrichter, W.A. Eaton, Proc. Natl. Acad. Sci. USA 95, 5872 (1998)PubMedCrossRefGoogle Scholar
  131. 131.
    V. Muñoz, L. Serrano, J. Mol. Biol. 245, 275 (1995)PubMedCrossRefGoogle Scholar
  132. 132.
    A. Bierzynski, P.S. Kim, R.L. Baldwin, Proc. Natl. Acad. Sci. USA 79, 2470 (1982)PubMedCrossRefGoogle Scholar
  133. 133.
    C. Mitchinson, R.L. Baldwin, Proteins: Struct. Funct. Genet. 1, 23 (1986)CrossRefGoogle Scholar
  134. 134.
    B.I. Dahiyat, S.L. Mayo, Science 278, 82 (1997)PubMedCrossRefGoogle Scholar
  135. 135.
    K. Zhu, M.R. Shirts, R.A. Friesner, J. Chem. Theory Comput. 3, 2108 (2007)CrossRefGoogle Scholar
  136. 136.
    P.I.W. de Bakker, M.A. DePristo, D.F. Burke, T.L. Blundell, Proteins: Struct. Funct. Bioinform. 51, 21 (2003)CrossRefGoogle Scholar
  137. 137.
    M.A. DePristo, P.I.W. de Bakker, S.C. Lovell, T.L. Blundell, Proteins: Struct. Funct. Bioinform. 51, 44 (2003)Google Scholar
  138. 138.
    A. Ghosh, C.S. Rapp, R.A. Friesner, J. Phys. Chem. B 102, 10983 (1998)CrossRefGoogle Scholar
  139. 139.
    M. Andrec, D.A. Snyder, Z. Zhou, J. Young, G.T. Montelione, R.M. Levy, Proteins: Struct. Funct. Bioinform. 69, 449 (2007)CrossRefGoogle Scholar
  140. 140.
    D.K. Klimov, D. Thirumalai, Proc. Natl. Acad. Sci. USA 97, 2544 (2000)PubMedCrossRefGoogle Scholar
  141. 141.
    V. Pande, D.S. Rokhsar, Proc. Natl. Acad. Sci. USA 96, 9062 (1999)PubMedCrossRefGoogle Scholar
  142. 142.
    B. Ma, R. Nussinov, J. Mol. Biol. 296, 1091 (2000)PubMedCrossRefGoogle Scholar
  143. 143.
    P.G. Bolhuis, Proc. Natl. Acad. Sci. USA 100, 12129 (2003)PubMedCrossRefGoogle Scholar
  144. 144.
    E. Gallicchio, M. Andrec, A.K. Felts, R.M. Levy, J. Phys. Chem. B 109, 6722 (2005)PubMedCrossRefGoogle Scholar
  145. 145.
    P.R.O. Montellano, Cytochrome P450: Structure, Mechanism and Biochemistry, 2nd edn. (Plenum Press, New York, 1995)Google Scholar
  146. 146.
    V. Guallar, R.A. Friesner, J. Am. Chem. Soc. 126, 8501 (2004)PubMedCrossRefGoogle Scholar
  147. 147.
    D.C. Haines, D.R. Tomchick, M. Machius, J.A. Peterson, Biochemistry 40, 13456 (2001)PubMedCrossRefGoogle Scholar
  148. 148.
    P.A. Williams, J. Cosme, A. Ward, H.C. Angova, D.M. Vinkovic, H. Jhoti, Nature 424, 464 (2003)PubMedCrossRefGoogle Scholar
  149. 149.
    P.A. Williams, J. Cosme, D.M. Vinkovic, A. Ward, H.C. Angove, P.J. Day, C. Vonrhein, I.J. Tickle, H. Jhoti, Science 305, 683 (2004)PubMedCrossRefGoogle Scholar
  150. 150.
    G.A. Schoch, J.K. Yano, M.R. Wester, K.J. Griffin, C.D. Stout, E.F. Johnson, J. Biol. Chem. 279, 9497 (2004)PubMedCrossRefGoogle Scholar
  151. 151.
    T. Jovanovic, R. Farid, R.A. Friesner, A.E. McDermott, J. Am. Chem. Soc. 127, 13548 (2005)PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  • A. K. Felts
    • 1
  • M. Andrec
    • 1
  • E. Gallicchio
    • 1
  • R. M. Levy
    • 1
  1. 1.Department of Chemistry and Chemical BiologyBioMaPS Institute for Quantitative Biology Rutgers UniversityPiscatawayUSA

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