New tools for the analysis and validation of cryo-EM maps and atomic models

Acta Crystallographica Section D: Structural Biology

Volumn 74, Issue 9, 2018, Pages 814-840

  Afonine, Pavel V ^a,b   Klaholz, Bruno P ^c   Moriarty, Nigel W ^a   Poon, Billy K ^a   Sobolev, Oleg V ^a   Terwilliger, Thomas C ^d,e   Adams, Paul D ^a,f   Urzhumtsev, Alexandre ^c,g  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b SHANGHAI UNIVERSITY   (China)

^c CNRS   (France)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

^e NEW MEXICO CONSORTIUM   (United States)

^f University of California   (United States)

^g UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Atomic models; cryo EM; Data quality; Model quality; Resolution; Validation

Indexed keywords

PROTEIN;

CHEMISTRY; CRYOELECTRON MICROSCOPY; HUMAN; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; PROTEIN DATABASE; SOFTWARE; X RAY CRYSTALLOGRAPHY;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEINS; SOFTWARE;

EID: 85053125915     PISSN: None     EISSN: 20597983     Source Type: Journal    
DOI: 10.1107/S2059798318009324     Document Type: Article

References (109)

1. Adams, P. D. et al. (2010). Acta Cryst. D66, 213–221.
2. Afanasyev, P., Seer-Linnemayr, C., Ravelli, R. B. G., Matadeen, R., De Carlo, S., Alewijnse, B., Portugal, R. V., Pannu, N. S., Schatz, M. & van Heel, M. (2017). IUCrJ, 4, 678–694.
3. Afonine, P. V., Grosse-Kunstleve, R. W., Adams, P. D. & Urzhumtsev, A. (2013). Acta Cryst. D69, 625–634.
4. 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.
5. Afonine, P. V., Headd, J. J., Terwilliger, T. C. & Adams, P. D. (2013). Comput. Crystallogr. Newsl. 4, 43–44.
6. Afonine, P. V., Moriarty, N. W., Mustyakimov, M., Sobolev, O. V., Terwilliger, T. C., Turk, D., Urzhumtsev, A. & Adams, P. D. (2015). Acta Cryst. D71, 646–666.
7. Afonine, P. V., Poon, B. K., Read, R. J., Sobolev, O. V., Terwilliger, T. C., Urzhumtsev, A. & Adams, P. D. (2018). Acta Cryst. D74, 531–544.
8. Afonine, P. V. & Urzhumtsev, A. (2004). Acta Cryst. A60, 19–32.
9. Atkinson, K. E. (1989). An Introduction to Numerical Analysis, 2nd ed. New York: John Wiley & Sons.
10. Barad, B. A., Echols, N., Wang, R. Y.-R., Cheng, Y., DiMaio, F., Adams, P. D. & Fraser, J. S. (2015). Nature Methods, 12, 943–946.
11. 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.
12. Bernstein, F. C., Koetzle, T. F., Williams, G. J., Meyer, E. F. Jr., Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). J. Mol. Biol. 112, 535–542.
13. Bhat, T. N. & Cohen, G. H. (1984). J. Appl. Cryst. 17, 244–248.
14. Brändén, C.-I. & Jones, T. A. (1990). Nature (London), 343, 687–689.
15. Brünger, A. T. (1992). Nature (London), 355, 472–475.
16. Brown, A., Long, F., Nicholls, R. A., Toots, J., Emsley, P. & Murshudov, G. (2015). Acta Cryst. D71, 136–153.
17. Cardone, G., Heymann, J. B. & Steven, A. C. (2013). J. Struct. Biol. 184, 226–236.
18. Chang, G., Roth, C. B., Reyes, C. L., Pornillos, O., Chen, Y.-J. & Chen, A. P. (2006). Science, 314, 1875.
19. Chang, L., Zhang, Z., Yang, J., McLaughlin, S. H. & Barford, D. (2015). Nature (London), 522, 450–454.
20. Chapman, M. S. (1995). Acta Cryst. A51, 69–80.
21. Chen, S., McMullan, G., Faruqi, A. R., Murshudov, G. N., Short, J. M., Scheres, S. H. W. & Henderson, R. (2013). Ultramicroscopy, 135, 24–35.
22. 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.
23. Chiu, W., Holton, J., Langan, P., Sauter, N. K., Schlichting, I., Terwilliger, T., Martin, J. L., Read, R. J. & Wakatsuki, S. (2017). Acta Cryst. D73, 381–383.
24. Coscia, F., Estrozi, L. F., Hans, F., Malet, H., Noirclerc-Savoye, M., Schoehn, G. & Petosa, C. (2016). Sci. Rep. 6, 30909.
25. DeLano, W. L. (2002). PyMOL. http://www.pymol.org.
26. Deptuch, G., Besson, A., Rehak, P., Szelezniak, M., Wall, J., Winter, M. & Zhu, Y. (2007). Ultramicroscopy, 107, 674–684.
27. Diamond, R. (1971). Acta Cryst. A27, 436–452.
28. DiMaio, F., Tyka, M. D., Baker, M. L., Chiu, W. & Baker, D. (2009). J. Mol. Biol. 392, 181–190.
29. Evans, P. R. & Murshudov, G. N. (2013). Acta Cryst. D69, 1204–1214.
30. Faruqi, A. R., Cattermole, D. M., Henderson, R., Mikulec, B. & Raeburn, C. (2003). Ultramicroscopy, 94, 263–276.
31. Frank, J. (2006). Three-Dimensional Electron Microscopy of Macromolecular Assemblies. Oxford University Press.
32. Goddard, T. D., Huang, C. C., Meng, E. C., Pettersen, E. F., Couch, G. S., Morris, J. H. & Ferrin, T. E. (2018). Protein Sci. 27, 14–25.
33. Gore, S., Velankar, S. & Kleywegt, G. J. (2012). Acta Cryst. D68, 478–483.
34. Grosse-Kunstleve, R. W. & Adams, P. D. (2002). J. Appl. Cryst. 35, 477–480.
35. Grosse-Kunstleve, R. W., Sauter, N. K. & Adams, P. D. (2004). IUCr Comput. Comm. Newsl. 3, 22–31.
36. Harauz, G. & van Heel, M. (1986). Optik, 73, 146–156.
37. Headd, J. J., Echols, N., Afonine, P. V., Grosse-Kunstleve, R.W., Chen, V. B., Moriarty, N. W., Richardson, D. C., Richardson, J. S. & Adams, P. D. (2012). Acta Cryst. D68, 381–390.
38. Heel van, M. (1987). Ultramicroscopy, 21, 95–100.
39. Heel van, M. (2013). Proc. Natl Acad. Sci. USA, 110, E4175–E4177.
40. Heel van, M., Keegstra, W., Schutter, W. & van Bruggen, E. F. J. (1982). The Structure and Function of Invertebrate Respiratory Proteins, edited by E. J. Wood, pp. 69–73. London: Harwood Academic Publishers.
41. Heel van, M. & Schatz, M. (2005). J. Struct. Biol. 151, 250–262.
42. Heel van, M. & Schatz, M. (2017). bioRxiv, 224402. https://doi.org/10.1101/224402.
43. Henderson, R. (2013). Proc. Natl Acad. Sci. USA, 110, 18037–18041.
44. Henderson, R. et al. (2012). Structure, 20, 205–214.
45. Herzik, M. A., Fraser, J. & Lander, G. C. (2017). bioRxiv, 128561. https://doi.org/10.1101/128561.
46. Heymann, J. B. & Belnap, D. M. (2007). J. Struct. Biol. 157, 3–18.
47. Hodel, A., Kim, S.-H. & Brünger, A. T. (1992). Acta Cryst. A48, 851–858.
48. Hryc, C. F., Chen, D.-H., Afonine, P. A., Jakana, J., Wang, Z., Haase- Pettingell, C., Jiang, W., Adams, P. D., King, J. A., Schmid, M. F. & Chiu, W. (2017). Proc. Natl Acad. Sci. USA, 114, 3103–3108.
49. Jakobi, A. J., Willmanns, M. & Sachse, C. (2017). Elife, 6, e27131.
50. Janssen, B. J. C., Read, R. J., Brünger, A. T. & Gros, P. (2007). Nature (London), 448, E1–E2.
51. Jaskolski, M., Gilski, M., Dauter, Z. & Wlodawer, A. (2007a). Acta Cryst. D63, 611–620.
52. Jaskolski, M., Gilski, M., Dauter, Z. & Wlodawer, A. (2007b). Acta Cryst. D63, 1282–1283.
53. Jiang, J.-S. & Brünger, A. T. (1994). J. Mol. Biol. 243, 100–115.
54. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Acta Cryst. A47, 110–119.
55. Joseph, A. P., Lagerstedt, I., Patwardhan, A., Topf, M. & Winn, M. (2017). J. Struct. Biol. 199, 12–26.
56. Karplus, P. A. & Diederichs, K. (2012). Science, 336, 1030–1033.
57. Karplus, P. A., Shapovalov, M. V., Dunbrack, R. L. & Berkholz, D. S. (2008). Acta Cryst. D64, 335–336.
58. Kleywegt, G. J. (2000). Acta Cryst. D56, 249–265.
59. Kleywegt, G. J. & Jones, T. A. (1995). Structure, 3, 535–540.
60. Kucukelbir, A. F. J., Sigworth, F. J. & Tagare, H. D. (2014). Nature Methods, 11, 63–65.
61. Kühlbrandt, W. (2014). Science, 343, 1443–1444.
62. Lakshminarasimhan, M., Madzelan, P., Nan, R., Milkovic, N. M. & Wilson, M. A. (2010). J. Biol. Chem. 285, 29651–29661.
63. Lang, P. T., Holton, J. M., Fraser, J. S. & Alber, T. (2014). Proc. Natl Acad. Sci. USA, 111, 237–242.
64. Lang, P. T., Ng, H. L., Fraser, J. S., Corn, J. E., Echols, N., Sales, M., Holton, J. M. & Alber, T. (2010). Protein Sci. 19, 1420–1431.
65. Lawson, C. L. et al. (2011). Nucleic Acids Res. 39, D456–D464.
66. Liao, H. Y. & Frank, J. (2010). Structure, 18, 768–775.
67. Loeffelholz von, O., Natchiar, S. K., Djabeur, N., Myasnikov, A. G., Kratzat, H., Ménétret, J.-F., Hazemann, I. & Klaholz, B. P. (2017). Curr. Opin. Struct. Biol. 46, 140–148.
68. Lunin, V. Y. & Woolfson, M. M. (1993). Acta Cryst. D49, 530–533.
69. Malhotra, A., Penczek, P., Agrawal, R. K., Gabashvili, I. S., Grassucci, R. A., Jünemann, R., Burkhardt, N., Nierhaus, K. H. & Frank, J. (1998). J. Mol. Biol. 280, 103–116.
70. Mao, Y., Castillo-Menendez, L. R. & Sodroski, J. G. (2013). Proc. Natl Acad. Sci. USA, 110, E4178–E4182.
71. Merk, A., Bartesaghi, A., Banerjee, S., Falconieri, V., Rao, P., Davis, M. I., Pragani, R., Boxer, M. B., Earl, L. A., Milne, J. L. S. & Subramaniam, S. (2016). Cell, 165, 1698–1707.
72. Milazzo, A. C., Leblanc, P., Duttweiler, F., Jin, L., Bouwer, J. C., Peltier, S., Ellisman, M., Bieser, F., Matis, H. S., Wieman, H., Denes, P., Kleinfelder, S. & Xuong, N.-H. (2005). Ultramicroscopy, 104, 152–159.
73. Moriarty, N. W. (2015). Comput. Crystallogr. Newsl. 6, 26.
74. Morffew, A. J. & Moss, D. S. (1983). Acta Cryst. A39, 196–199.
75. Neumann, P., Dickmanns, A. & Ficner, R. (2018). Structure, 26, 785–795.
76. Nguyen, T. H. D., Galej, W. P., Bai, X.-C., Oubridge, C., Newman, A. J., Scheres, S. H. W. & Nagai, K. (2016). Nature (London), 530, 298–302.
77. Orlov, I. et al. (2017). Biol. Cell, 109, 1–13.
78. Penczek, P. A. (2010). Methods Enzymol. 482, 73–100.
79. Peng, L.-M. (1998). Acta Cryst. A54, 481–485.
80. Peng, L.-M., Ren, G., Dudarev, S. L. & Whelan, M. J. (1996). Acta Cryst. A52, 257–276.
81. Pintilie, G., Chen, D.-H., Haase-Pettingell, C. A., King, J. A. & Chiu, W. (2016). Biophys. J. 110, 827–839.
82. Pintilie, G. & Chiu, W. (2012). Biopolymers, 97, 742–760.
83. Ramachandran, G. N., Ramakrishnan, C. & Sasisekharan, V. (1963). J. Mol. Biol. 7, 95–99.
84. Read, R. J. (1986). Acta Cryst. A42, 140–149.
85. Read, R. J. et al. (2011). Structure, 19, 1395–1412.
86. Rice, L. M., Shamoo, Y. & Brünger, A. T. (1998). J. Appl. Cryst. 31, 798–805.
87. Rosenthal, P. B. & Henderson, R. (2003). J. Mol. Biol. 333, 721–745.
88. Rosenthal, P. B. & Rubinstein, J. L. (2015). Curr. Opin. Struct. Biol. 34, 135–144.
89. Rupp, B. (2010). Biomolecular Crystallography. New York: Garland Science.
90. Saxton, W. O. & Baumeister, W. (1982). J. Microsc. 127, 127–138.
91. Sorzano, C. O. S., Vargas, J., Otón, J., Abrishami, V., de la Rosa-Trevín, J. M., del Riego, S., Fernández-Alderete, A., Martínez-Rey, C., Marabini, R. & Carazo, J. M. (2015). AIMS Biophys. 2, 8–20.
92. Stec, B. (2007). Acta Cryst. D63, 1113–1114.
93. Subramaniam, S. (2013). Proc. Natl Acad. Sci. USA, 110, E4172–E4174.
94. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Adams, P. D., Moriarty, N.W., Zwart, P., Read, R. J., Turk, D. & Hung, L.-W. (2007). Acta Cryst. D63, 597–610.
95. Terwilliger, T. C., Sobolev, O. V., Afonine, P. V. & Adams, P. D. (2018). Acta Cryst. D74, 545–559.
96. Tickle, I. J. (2007). Acta Cryst. D63, 1274–1281.
97. Tickle, I. J. (2012). Acta Cryst. D68, 454–467.
98. Urzhumtsev, A. G. (1992). Jnt CCP4/ESF–EACBM Newsl. Protein Crystallogr. 27, 31–32.
99. Urzhumtsev, A., Afonine, P. V., Lunin, V. Y., Terwilliger, T. C. & Adams, P. D. (2014). Acta Cryst. D70, 2593–2606.
100. Urzhumtseva, L., Afonine, P. V., Adams, P. D. & Urzhumtsev, A. (2009). Acta Cryst. D65, 297–300.
101. Urzhumtseva, L., Klaholz, B. & Urzhumtsev, A. (2013). Acta Cryst. D69, 1921–1934.
102. Volkmann, N. (2009). Acta Cryst. D65, 679–689.
103. Wang, J. & Moore, P. B. (2017). Protein Sci. 26, 122–129.
104. Whicher, J. R. & MacKinnon, R. (2016). Science, 353, 664–669.
105. Wlodawer, A. & Dauter, Z. (2017). Acta Cryst. D73, 379–380.
106. Wlodawer, A., Minor, W., Dauter, Z. & Jaskolski, M. (2008). FEBS J. 275, 1–21.
107. Yonekura, K., Matsuoka, R., Yamashita, Y., Yamane, T., Ikeguchi, M., Kidera, A. & Maki-Yonekura, S. (2018). IUCrJ, 5, 348–353.
108. Young, J. Y. et al. (2017). Structure, 25, 536–545.
109. Zhang, Z. & Chen, J. (2016). Cell, 167, 1586–1597.