Significant reduction in errors associated with nonbonded contacts in protein crystal structures: Automated all-atom refinement with PrimeX

Acta Crystallographica Section D: Biological Crystallography

Volumn 68, Issue 8, 2012, Pages 935-952

  Bell, Jeffrey A ^a   Ho, Kenneth L ^a   Farid, Ramy ^a  

^a SCHRÖDINGER INC   (United States)

Author keywords

clashes; electrostatics; force fields; H atoms; hydrogen bonds; model quality; molecular geometry; nonbonded contacts; refinement; restraints; riding H atoms; van der Waals radii

Indexed keywords

LIGAND; PROTEIN;

ALGORITHM; ARTICLE; BIOLOGY; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER PROGRAM; COMPUTER SIMULATION; CRYSTALLIZATION; DRUG DESIGN; ELECTRON; HYDROGEN BOND; METHODOLOGY; PROTEIN DATABASE; REPRODUCIBILITY; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; DRUG DESIGN; ELECTRONS; HYDROGEN BONDING; LIGANDS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEINS; REPRODUCIBILITY OF RESULTS; SOFTWARE; STATIC ELECTRICITY;

EID: 84864882089     PISSN: 09074449     EISSN: 13990047     Source Type: Journal    
DOI: 10.1107/S0907444912017453     Document Type: Article

References (151)

1. Abu Tarboush, N., Jensen, L. M., Feng, M., Tachikawa, H., Wilmot, C. M. & Davidson, V. L. (2010). Biochemistry, 49, 9783-9791.
2. Adams, P. D., Pannu, N. S., Read, R. J. & Brünger, A. T. (1997). Proc. Natl Acad. Sci. USA, 94, 5018-5023.
3. Adams, C. J., Pike, A. C., Maniam, S., Sharpe, T. D., Coutts, A. S., Knapp, S., La Thangue, N. B. & Bullock, A. N. (2012). Proc. Natl. Acad. Sci. USA, 109, 3778-3783.
4. Afonine, P. V., Grosse-Kunstleve, R.W. & Adams, P. D. (2005). CCP4 Newsl. 42, contribution 8.
5. Afonine, P. V., Grosse-Kunstleve, R. W., Chen, V. B., Headd, J. J., Moriarty, N. W., Richardson, J. S., Richardson, D. C., Urzhumtsev, A., Zwart, P. H. & Adams, P. D. (2010). J. Appl. Cryst. 43, 669-676.
6. Ali, A., Reddy, G. S., Nalam, M. N., Anjum, S. G., Cao, H., Schiffer, C. A. & Rana, T. M. (2010). J. Med. Chem. 53, 7699-7708.
7. Allen, F. H. (2002). Acta Cryst. B58, 380-388.
8. Artz, J. D., Wernimont, A. K., Dunford, J. E., Schapira, M., Dong, A., Zhao, Y., Lew, J., Russell, R. G., Ebetino, F. H., Oppermann, U. & Hui, R. (2011). J. Biol. Chem. 286, 3315-3322.
9. Attolino, E., Calderone, V., Dragoni, E., Fragai, M., Richichi, B., Luchinat, C. & Nativi, C. (2010). Eur. J. Med. Chem. 45, 5919-5925.
10. Banks, J. L. et al. (2005). J. Comput. Chem. 26, 1752-1780.
11. Begley, D. W., Hartley, R. C., Davies, D. R., Edwards, T. E., Leonard, J. T., Abendroth, J., Burris, C. A., Bhandari, J., Myler, P. J., Staker, B. L. & Stewart, L. J. (2011). J. Struct. Funct. Genomics, 12, 63-76.
12. Bell, J. A., Cao, Y., Gunn, J. R., Day, T., Gallicchio, E., Zhou, Z., Levy, R. & Farid, R. (2012). International Tables for Crystallography, Vol. F, edited by E. Arnold, D. M. Himmel & M. G. Rossmann, pp. 534-538. Chichester: John Wiley & Sons.
13. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N. & Bourne, P. E. (2000). Nucleic Acids Res. 28, 235-242.
14. Biswas, T., Small, J., Vandal, O., Odaira, T., Deng, H., Ehrt, S. & Tsodikov, O. V. (2010). Structure, 18, 1353-1363.
15. Blaszczyk, J., Li, Y., Shi, G., Yan, H. & Ji, X. (2003). Biochemistry, 42, 1573-1580.
16. Bondi, A. (1964). J. Phys. Chem. 68, 441-451.
17. Bönisch, H., Schmidt, C. L., Bianco, P. & Ladenstein, R. (2005). Acta Cryst. D61, 990-1004.
18. Borshchevskiy, V., Molseeva, E., Kuklin, A., Büldt, G., Hato, M. & Gordeliy, V. (2010). J. Cryst. Growth, 312, 3326-3330.
19. Bosch, D. E., Kimple, A. J., Sammond, D. W., Muller, R. E., Miley, M. J., Machius, M., Kuhlman, B., Willard, F. S. & Siderovski, D. P. (2011). J. Biol. Chem. 286, 3351-3358.
20. Bricogne, G., Blanc, E., Brandl,M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O. S., Vonrhein, C. & Womack, T. O. (2011). BUSTER. Cambridge: Global Phasing Ltd. Brünger, A. T. (1989). Acta Cryst. A45, 42-50.
21. Brünger, A. T. (1992). X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. New Haven: Yale University Press.
22. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T. &Warren, G. L. (1998). Acta Cryst. D54, 905-921.
23. Brünger, A. T., Clore, G. M., Gronenborn, A. M. & Karplus, M. (1986). Proc. Natl Acad. Sci. USA, 83, 3801-3805.
24. Brünger, A. T. & Karplus, M. (1988). Proteins, 4, 148-156.
25. Brünger, A. T., Karplus, M. & Petsko, G. A. (1989). Acta Cryst. A45, 50-61.
26. Capkauskaite?, E., Baranauskiene?, L., Golovenko, D., Manakova, E., Gražulis, S., Tumkevicius, S. & Matulis, D. (2010). Bioorg. Med. Chem. 18, 7357-7364.
27. Carrillo, D. R., Parthier, C., Jänckel, N., Grandke, J., Stelter, M., Schilling, S., Boehme, M., Neumann, P., Wolf, R., Demuth, H. U., Stubbs,M. T. & Rahfeld, J. U. (2010). J. Biol. Chem. 391, 1419-1428.
28. Chatwell, L., Holla, A., Kaufer, B. B. & Skerra, A. (2008). Mol. Immunol. 45, 1981-1994.
29. Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S. & Richardson, D. C. (2010). Acta Cryst. D66, 12-21.
30. Chen, Z., Pelc, L. A. & De Cera, E. (2010). Proc. Natl Acad. Sci. USA, 107, 19278-19283.
31. Chen, B., Sysoeva, T. A., Chowdhury, S., Guo, L., De Carlo, S., Hanson, J. A., Yang, H. & Nixon, B. T. (2010). Structure, 18, 1420-1430.
32. Chufán, E. E., Prigge, S. T., Siebert, X., Eipper, B. A., Mains, R. E. & Amzel, L. M. (2010). J. Am. Chem. Soc. 132, 15565-15572.
33. Clasquin, M. F., Melamud, E., Singer, A., Gooding, J. R., Xu, X., Dong, A., Cui, H., Campagna, S. R., Savchenko, A., Yakunin, A. F., Rabinowitz, J. D. & Caudy, A. A. (2011). Cell, 145, 969-980.
34. Compton, J. R., Legler, P. M., Clingan, B. V., Olson, M. A. & Millard, C. B. (2011). Proteins, 79, 1048-1060.
35. Cook, W. J., Smith, C. D., Senkovich, O., Holder, A. A. & Chattopadhyay, D. (2010). Acta Cryst. F66, 1426-1431.
36. Corminboeuf, O., Bezencon, O., Grisostomi, C., Remen , L., Richard- Bildstein, S., Bur, D., Prade, L., Hess, P., Strickner, P., Fischli, W., Steiner, B. & Treiber, A. (2010). Bioorg. Med. Chem. Lett. 20, 6286-6290.
37. Coulson, C. A. & Thomas, M. W. (1971). Acta Cryst. B27, 1354-1359.
38. Crawley, S. W., Gharaei, M. S., Ye, Q., Yang, Y., Raveh, B., London
39. N., Schueler-Furman, O., Jia, Z. & Cote, G. P. (2011). J. Biol. Chem. 286, 2607-2616.
40. Dasgupta, J., Blenkowska-Haba, M., Ortega, M. E., Patel, H. D., Bodevin, S., Spillmann, D., Bishop, B., Sapp, M. & Chen, X. S. (2011). J. Biol. Chem. 286, 2617-2624.
41. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., Snoeyink, J., Richardson, J. S. & Richardson, D. C. (2007). Nucleic Acid Res. 35,W375-W383.
42. Diebold, M. L., Koch, M., Loeliger, E., Cura, V., Winston, F., Cavarelli, J. & Romier, C. (2010). EMBO J. 29, 3979-3991.
43. Eidam, O., Romagnoli, C., Caselli, E., Babaoglu, K., Pohlhaus, D. T., Karpiak, J., Bonnet, R., Shoichet, B. K. & Prati, F. (2010). J. Med. Chem. 53, 7852-7863.
44. Empadinhas, N., Pereira, P. J., Albuquerque, L., Costa, J., SaMoura, B., Marques, A. T., Macedo-Ribeiro, S. & da Costa, M. S. (2011). Mol. Microbiol. 79, 76-93.
45. Engh, R. A. & Huber, R. (1991). Acta Cryst. A47, 392-400.
46. Esposito, L., Vitagliano, L., Sica, F., Sorrentino, G., Zagari, A. & Mazzarella, L. (2000). J. Mol. Biol. 297, 713-732.
47. Feng, Z., Westbrook, J. & Berman, H. M. (1998). NUCheck. Report NDB-407, Rutgers University, New Brunswick, New Jersey, USA.
48. Fenn, T. D., Ringe, D. & Petsko, G. A. (2004). Biochemistry, 43, 6464-6474.
49. Fenn, T. D. & Schnieders, M. J. (2011). Acta Cryst. D67, 957-965.
50. Fenn, T. D., Schnieders, M. J., Brunger, A. T. & Pande, V. S. (2010). Biophys. J. 98, 2984-2992.
51. Fenn, T. D., Schnieders, M. J., Mustyakimov, M., Wu, C., Langan, P., Pande, V. S. & Brunger, A. T. (2011). Structure, 19, 523-533.
52. Fokina, O., Chellamuthu, V.-R., Forchhammer, K. & Zeth, K. (2010). Proc. Natl Acad. Sci. USA, 107, 19760-19765.
53. Fuhrmann, C. N., Daugherty, M. D. & Agard, D. A. (2006). J. Am. Chem. Soc. 128, 9086-9102.
54. Gallicchio, E., Zhang, L. Y. & Levy, R. M. (2002). J. Comput. Chem. 23, 517-529.
55. Ghosh, A., Rapp, C. S. & Friesner, R. A. (1998). J. Phys. Chem. B, 102, 10983-10990.
56. Hakanpää, J., Linder, M., Popov, A., Schmidt, A. & Rouvinen, J. (2006). Acta Cryst. D62, 356-367.
57. Hall, G., Bradshaw, T. D., Laughton, C. A., Stevens, M. F. & Emsley, J. (2011). Protein Sci. 20, 210-215.
58. Han, L., Monné, M., Okumura, H., Schwend, T., Cherry, A. L., Flot, D., Matsuda, T. & Jovine, L. (2010). Cell, 143, 404-415.
59. Hardegger, L. A., Kuhn, B., Spinnier, B., Anselm, L., Ecabert, R., Stihle, M., Gsell, B., Thoma, R., Diez, J., Benz, J., Plancher, J. M., Hartmann, G., Banner, D. W., Haap, W. & Diederich, F. (2011). Agnew. Chem. Int. Ed. Engl. 50, 314-318.
60. Harmat, V., Domokos, K., Menyhárd, D. K., Palló , A., Szeltner, Z., Szamosi, I., Beke-Somfai, T., Naray-Szabó, G. & Polgár, L. (2011). J. Biol. Chem. 286, 1987-1998.
61. Hee, C. S., Gao, S., Loll, B., Miller, M. M., Uchanska-Ziegler, B., Daumke, O. & Ziegler, A. (2010). PLoS Biol. 8, e1000557.
62. Heldman, N., Vonshak, O., Sevier, C. S., Vitu, E., Mehlman, T. & Fass, D. (2010). Protein Sci. 19, 1863-1876.
63. Hendrickson, W. A. (1985). Methods Enzymol. 115, 252-270.
64. Hooft, R. W. W., Sander, C. & Vriend, G. (1996). Proteins, 26, 363-376.
65. Hooft, R.W.W., Vriend, G., Sander, C. & Abola, E. E. (1996). Nature (London), 381, 272.
66. Husain, N., Obranic, S., Koscinski, L., Seetharaman, J., Babic, F., Bujnicki, J. M., Maravic Vlahovicek, G. & Sivaraman, J. (2011). Nucleic Acids Res. 39, 1903-1918.
67. Jacques, D. A., Langley, D. B., Hynson, R. M., Whitten, A. E., Kwan, A., Guss, J. M. & Trewhella, J. (2011). J. Mol. Biol. 405, 214-226.
68. Jiang, J.-S. & Brünger, A. T. (1994). J. Mol. Biol. 243, 100-115.
69. Joosten, R. P. et al. (2009). J. Appl. Cryst. 42, 376-384.
70. Joosten, R. P., Joosten, K., Cohen, S. X., Vriend, G. & Perrakis, A. (2011). Bioinformatics, 27, 3392-3398.
71. Jorgensen, W. L., Maxwell, D. S. & Tirado-Rives, J. (1996). J. Am. Chem. Soc. 118, 11225-11236.
72. Kaminski, G., Friesner, R. A., Tirado-Rives, J. & Jorgensen, W. L. (2001). J. Phys. Chem. B, 105, 6474-6487.
73. Ke, W., Sampson, J. M., Ori, C., Prati, F., Drawz, S. M., Bethel, C. R., Bonomo, R. A. & van den Akker, F. (2011). Antimicrob. Agents Chemother. 55, 174-183.
74. Khan, H., Barna, T., Harris, R. J., Bruce, N. C., Barsukov, I., Munro, A. W., Moody, P. C. & Scrutton, N. S. (2004). J. Biol. Chem. 279, 30563-30572.
75. Khan, M. Q., Sweeting, B., Mulligan, V. K., Arslan, P. E., Cashman, N. R., Pai, E. F. & Chakrabartty, A. (2010). Proc. Natl Acad. Sci. USA, 107, 19808-19813.
76. Knight, J. L., Zhou, Z., Gallicchio, E., Himmel, D. M., Friesner, R. A., Arnold, E. & Levy, R. M. (2008). Acta Cryst. D64, 383-396.
77. Ko, T.-P., Robinson, H., Gao, Y.-G., Cheng, C.-H., DeVries, A. L. & Wang, A. H.-J. (2003). Biophys. J. 84, 1228-1237.
78. Konnert, J. H. (1976). Acta Cryst. A32, 614-617.
79. Konnert, J. H. & Hendrickson, W. A. (1980). Acta Cryst. A36, 344-350.
80. Koparde, V. N., Scarsdale, J. N. & Kellogg, G. E. (2011). PLoS One, 6, e15920.
81. Kumar, J. & Mayer, M. L. (2010). J. Mol. Biol. 404, 680-696.
82. Kumar, D. V., Rai, R., Brameld, K. A., Somoza, J. R., Rajagopalan, R., Janc, J. W., Xia, Y. M., Ton, T. L., Shaghafi, M. B., Hu, H., Lehoux, I., To, N., Young,W. B. & Green, M. J. (2011). Bioorg. Med. Chem. Lett. 21, 82-87.
83. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). J. Appl. Cryst. 26, 283-291.
84. Lee, Y. T., Glazer, E. C., Wilson, R. F., Stout, C. D. & Goodin, D. B. (2011). Biochemistry, 50, 693-703.
85. Lejon, S., Thong, S. Y., Murthy, A., AlQarni, S., Murzina, N. V., Blobel, G. A., Laue, E. D. & Mackay, J. P. (2011). J. Biol. Chem. 286, 1196-1203.
86. Li, J., Abel, R., Zhu, K., Cao, Y., Zhao, S. & Friesner, R. A. (2011). Proteins, 79, 2794-2812.
87. Li, H., Tong, S., Li, X., Shi, H., Ying, Z., Gao, Y., Ge, H., Niu, L. & Teng, M. (2011). Cell Res. 21, 1039-1051.
88. Liebschner, D., Elias,M., Moniot, S., Fournier, B., Scott, K., Jelsch, C., Guillot, B., Lecomte, C. & Chabriere, E. (2009). J. Am. Chem. Soc. 131, 7879-7886.
89. Lin, F.-Y., Liu, C.-I., Liu, Y.-L., Zhang, Y., Wang, K., Jeng, W. Y., Ko, T.-P., Cao, R., Wang, A. H.-J. & Oldfield, E. (2010). Proc. Natl Acad. Sci. USA, 107, 21337-21342.
90. Linge, J. P., Williams, M. A., Spronk, C. A., Bonvin, A. M. & Nilges, M. (2003). Proteins, 50, 496-506.
91. MacArthur, M. W. & Thornton, J. M. (1996). J. Mol. Biol. 264, 1180-1195.
92. Matsumoto, K., Okamoto, K., Ashizawa, N. & Nishino, T. (2010). J. Pharmacol. Exp. Ther. 336, 95-103.
93. Minasov, G., Wang, X. & Shoichet, B. K. (2002). J. Am. Chem. Soc. 124, 5333-5340.
94. Morin, A., Kaufmann, K. W., Fortenberry, C., Harp, J. M., Mizoue, L. S. & Meiler, J. (2011). Protein Eng. Des. Sel. 24, 503-516.
95. Morita, H., Wanibuchi, K., Nii, H., Kato, R., Sugio, S. & Abe, I. (2010). Proc. Natl Acad. Sci. USA, 107, 19778-19783.
96. Moulinier, L., Case, D. A. & Simonson, T. (2003). Acta Cryst. D59, 2094-2103.
97. Murakawa, T., Machida, Y. & Hayashi, H. (2011). J. Biol. Chem. 286, 2774-2784.
98. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F. & Vagin, A. A. (2011). Acta Cryst. D67, 355-367.
99. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. (1997). Acta Cryst. D53, 240-255.
100. Natesh, R., Manikandan, K., Bhanumoorthy, P., Viswamitra, M. A. & Ramakumar, S. (2003). Acta Cryst. D59, 105-117.
101. Neu, U.,Maginnis,M. S., Palma, A. S., Ströh, L. J., Nelson, C. D., Feizi, T., Atwood,W. J. & Stehle, T. (2010). Cell Host Microbe, 8, 309-319.
102. Nicodeme, E. et al. (2010). Nature (London), 468, 1119-1123.
103. Nilges, M., Gronenborn, A. M., Brunger, A. T. & Clore, G. M. (1988). Protein Eng. 2, 27-38.
104. Niu, W., Shu, Q., Chen, Z., Mathews, S., Di Cera, E. & Frieden, C. (2010). J. Phys. Chem. B, 114, 16156-16165.
105. Nozinovic, S., Fürtig, B., Jonker, H. R., Richter, C. & Schwalbe, H. (2010). Nucleic Acids Res. 38, 683-694.
106. Orita, I., Kita, A., Yurimoto, H., Kato, N., Sakai, Y. &Miki, K. (2010). Proteins, 78, 3488-3492.
107. Ouellet, H., Kells, P. M., Ortiz de Montellano, P. R. & Produst, L. M. (2011). Bioorg. Med. Chem. Lett. 21, 332-337.
108. Pannu, N. S. & Read, R. J. (1996). Acta Cryst. A52, 659-668.
109. Patterson, A., Price, N. C. & Nairn, J. (2010). Acta Cryst. F66, 1415-1420.
110. Paul, D., Chatterjee, A., Begley, T. P. & Ealick, S. E. (2010). Biochemistry, 49, 9922-9934.
111. Paz, S., Tizó n, L., Otero, J. M., Llamas-Saiz, A. L., Fox, G. C., van Raaij, M. J., Lamb, H., Hawkins, A. R., Lapthorn, A. J., Castedo, L. & Gonzalez-Bello, C. (2011). ChemMedChem, 6, 266-272.
112. Peters, C., Brejc, K., Belmont, L., Bodey, A. J., Lee, Y., Yu, M., Guo, J., Sakowicz, R., Hartman, J. & Moores, C. A. (2010). EMBO J. 29, 3437-3447.
113. Pizzo, E., Merlino, A., Turano, M., Russo Krauss, I., Coscia, F., Zanfardino, A., Varcamonti, M., Furia, A., Giancola, C., Mazzarella, L., Sica, F. & D'Alessio, G. (2010). Biochem. J. 433, 345-355.
114. Priestle, J. P. (2003). J. Appl. Cryst. 36, 34-42.
115. Privé, G. G., Anderson, D. H., Wesson, L., Cascio, D. & Eisenberg, D. (1999). Protein Sci. 8, 1400-1409.
116. Radford, R. J., Lawrenz, M., Nguyen, P. C., McCammon, J. A. & Akif Tezcan, F. (2011). Chem. Commun. 47, 313-315.
117. Read, R. J. (1986). Acta Cryst. A42, 140-149.
118. Read, R. J. et al. (2011). Structure, 19, 1395-1412.
119. Romano, K. P., Ali, A., Royer, W. E. & Schiffer, C. A. (2010). Proc. Natl Acad. Sci. USA, 107, 20986-20991.
120. Roosild, T. P., Castronovo, S., Healy, J., Miller, S., Pliotas, C., Rasmussen, T., Bartlett, W., Conway, S. J. & Booth, I. R. (2010). Proc. Natl Acad. Sci. USA, 107, 19784-19789.
121. Rowland, R. S. & Taylor, R. (1996). J. Phys. Chem. 100, 7384-7391.
122. Ryan, A. J., Ghuman, J., Zunszain, P. A., Chung, C. W. & Curry, S. (2011). J. Struct. Biol. 174, 84-91.
123. Sainsbury, L., Bird, L., Rao, V., Shepherd, S. M., Stuart, D. I., Hunter, W. N., Owens, R. J. & Ren, J. (2010). J. Mol. Biol. 405, 173-184.
124. Schmelz, S. (2010). PhD Thesis. University of St Andrews, Fife, Scotland.
125. Schnieders, M. J., Fenn, T. D. & Pande, V. S. (2011). J. Chem. Theory Comput. 7, 1141-1156.
126. Schröder, G. F., Levitt, M. & Brunger, A. T. (2010). Nature (London), 464, 1218-1222.
127. Sendovski, M., Kanteev, M., Shuster Ben-Yosef, V., Adir, N. & Fishman, A. (2010). Acta Cryst. F66, 1101-1103.
128. Sheldrick, G. M. & Schneider, T. R. (1997). Methods Enzymol. 277, 319-343.
129. Shinobu, A., Palm, G. J., Schierbeek, A. J. & Agmon, N. (2010). J. Am. Chem. Soc. 132, 11093-11102.
130. Spronk, C. A. E. M., Nabuurs, S. B., Krieger, E., Vriend, G. & Vuister, G. W. (2004). Prog. Nucl. Magn. Reson. Spectrosc. 45, 315-337.
131. Sun, M., Larivie re, L., Dengl, S., Mayer, A. & Cramer, P. (2010). J. Biol. Chem. 285, 41597-41603.
132. Sun, J. & Weis, W. I. (2011). J. Mol. Biol. 405, 519-530.
133. Swiecki, M., Scheaffer, S. M., Allaire, M., Fremont, D. H., Colonna, M. & Brett, T. J. (2011). J. Biol. Chem. 286, 2987-2997.
134. Takeda, K., Kusumoto, K., Hirano, Y. & Miki, K. (2010). J. Struct. Biol. 169, 135-144.
135. Thompson, M. K., Davis, M. F., de Serrano, V., Nicoletti, F. P., Howes, B. D., Smulevich, G. & Franzen, S. (2010). Biophys. J. 99, 1586-1595.
136. Tong, Y., Tempel, W., Wang, H., Yamada, K., Shen, L., Senisterra, G. A., MacKenzie, F., Chishti, A. H. & Park, H. W. (2010). Proc. Natl Acad. Sci. USA, 107, 20346-20351.
137. Touw, W. G. & Vriend, G. (2010). Acta Cryst. D66, 1341-1350.
138. Tronrud, D. E., Berkholz, D. S. & Karplus, P. A. (2010). Acta Cryst. D66, 834-842.
139. Vaguine, A. A., Richelle, J. & Wodak, S. J. (1999). Acta Cryst. D55, 191-205.
140. Wallace, B. D., Wang, H., Lane, K. T., Scott, J. E., Orans, J., Koo, J. S., Venkatesh, M., Jobin, C., Yeh, L.-A., Mani, S. & Redinbo, M. R. (2010). Science, 330, 831-835.
141. Wang, J., Dauter, M., Alkire, R., Joachimiak, A. & Dauter, Z. (2007). Acta Cryst. D63, 1254-1268.
142. Wang, Y. & Guo, H.-C. (2010). J. Mol. Biol. 403, 120-130.
143. Watenpaugh, K. D., Sieker, L. C., Herriott, J. R. & Jensen, L. H. (1973). Acta Cryst. B29, 943-956.
144. Weis, W. I., Brünger, A. T., Skehel, J. J. & Wiley, D. C. (1990). J. Mol. Biol. 212, 737-761.
145. Word, J. M., Lovell, S. C., LaBean, T. H., Taylor, H. C., Zalis, M. E., Presley, B. K., Richardson, J. S. & Richardson, D. C. (1999). J. Mol. Biol. 285, 1711-1733.
146. Xiang, Y., Huang, R.-H., Liu, X. Z., Zhang, Y. & Wang, D.-C. (2004). J. Struct. Biol. 148, 86-97.
147. Yang,W., Bell, S. G.,Wang, H., Zhou,W., Bartlam, M.,Wong, L.-L. & Rao, Z. (2010). Biochem. J. 433, 85-93.
148. Yang, F., West, A. P. Jr & Bjorkman, P. J. (2011). J. Struct. Biol. 174, 239-244.
149. Yoshida, H., Takeda, K., Izumori, K. & Kamitori, S. (2010). Protein Eng. Des. Sel. 23, 919-927.
150. Zhou, H., Brock, J., Casarotto, M. G., Oakley, A. J. & Board, P. G. (2011). J. Biol. Chem. 286, 4271-4279.
151. Zhu, K., Shirts, M. R. & Friesner, R. A. (2007). J. Chem. Theory Comput. 3, 2108-2119.