Protein crystallography from the perspective of technology developments

Crystallography Reviews

Volumn 21, Issue 1-2, 2015, Pages 122-153

  Su, Xiao Dong ^a   Zhang, Heng ^a   Terwilliger, Thomas C ^b   Liljas, Anders ^c   Xiao, Junyu ^a   Dong, Yuhui ^d  

^a PEKING UNIVERSITY   (China)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c LUND UNIVERSITY   (Sweden)

^d INSTITUTE OF HIGH ENERGY PHYSICS   (China)

Author keywords

computer programs and graphics; protein crystallization; recombinant DNA techniques; structural genomics (SG); synchrotron radiation (SR); X ray crystallography; X ray free electron laser (XFEL)

Indexed keywords

CRYSTAL SYMMETRY; DNA; ELECTRONS; FREE ELECTRON LASERS; GENETIC ENGINEERING; MINERALS; RECOMBINANT PROTEINS; SYNCHROTRON RADIATION; SYNCHROTRONS; X RAY APPARATUS;

MACROMOLECULAR CRYSTALLOGRAPHY; PROTEIN CRYSTALLIZATION; PROTEIN CRYSTALLOGRAPHY; RECOMBINANT DNA; STRUCTURAL GENOMICS; TECHNICAL ADVANCEMENT; TECHNOLOGY DEVELOPMENT; X-RAY FREE ELECTRON LASERS;

X RAY CRYSTALLOGRAPHY;

EID: 84926221008     PISSN: 0889311X     EISSN: 14763508     Source Type: Journal    
DOI: 10.1080/0889311X.2014.973868     Document Type: Review

References (210)

1. Friedrich W, Knipping P, Laue M. Interferenz-Erscheinungen bei Röntgenstrahlen. Sitz Bayer Akad Wiss. 1912; 42: 303-322
2. Bragg WH. X-rays and crystals. Nature. 1912; 90: 219
3. Bragg WH, Bragg WL. The reflection of X-rays by crystals. Proc Roy Soc Lond A. 1913; 88: 428-438
4. Bragg WL. The structure of some crystals as indicated by their diffraction of X-rays. Proc Roy Soc Lond A. 1913; 89: 248-277
5. Thomas JM. William Lawrence Bragg: the pioneer of X-ray crystallography and his pervasive influence. Angew Chem Int ed Engl. 2012; 51: 12946-12958
6. Jaskolski M, Dauter Z, Wlodawer A. A brief history of macromolecular crystallography, illustrated by a family tree and its Nobel fruits. FEBS J. 2014; 281: 3985-4009
7. Helliwell JR. Macromolecular crystallography with synchrotron radiation. Cambridge: Cambridge University Press; 2005
8. Helliwell JR. Synchrotron-radiation instrumentation, methods and scientific utilization. In: Arnold E, Himmel DM, Rossmann MG, editors. International Tables for Crystallography Volume F: Crystallography of biological macromolecules, 2nd ed., Ch. 8.1. Heidelberg: Springer; 2012. p. 189-204
9. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC. A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature. 1958; 181: 662-666
10. Kendrew JC, Dickerson RE, Strandberg BE, Hart RG, Davies DR, Phillips DC, Shore VC. Structure of myoglobin: a three-dimensional Fourier synthesis at 2 A. resolution. Nature. 1960; 185: 422-427
11. Perutz MF, Rossmann MG, Cullis AF, Muirhead H, Will G, North AC. Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by X-ray analysis. Nature. 1960; 185: 416-422
12. Chang AC, Cohen SN. Genome construction between bacterial species in vitro: replication and expression of Staphylococcus plasmid genes in Escherichia coli. Proc Natl Acad Sci USA. 1974; 71: 1030-1034
13. Cohen SN. DNA cloning: a personal view after 40 years. Proc Natl Acad Sci USA. 2013; 110: 15521-15529. Epub 2013/09/18
14. Cohen SN, Chang AC, Boyer HW, Helling RB. Construction of biologically functional bacterial plasmids in vitro. Proc Natl Acad Sci USA. 1973; 70: 3240-3244. Epub 1973/11/01
15. Hunefeld FL. Der Chemismus in der tierescher Organization. Leipzig: FA Brockhouse; 1840
16. Kolliker A, Zeit F. Wissensch Zoologic 1849;1:266-266
17. Leydig F, Zeit F. Wissensch Zoologic 1849;1:116-116
18. Relchert KE. Muller's Archiv fur Anat. Physiol und Wissensch Medicin. 1849: 197-251
19. Funke OZ. Über das milzvenenblut. Z Rat Med. 1851; 1: 172-218
20. Lehmann CC. Lehrbuch der Physlologlschen Cherme. 2nd ed. Leipzig: Wilhelm Engelmann; 1853
21. Hartig T. Ueber das Klebermehl. Bot Zeitung. 1855; 13: 881
22. Osborne TB. Crystallized vegetable proteids. Amer Chem J. 1892; 14: 662-689
23. Hofmeister T. Über die Darstellung von krystallisirtem Eiralbumin und die Krystallisirbarkeit colloider Stoffe. Z Physiol Chem. 1890; 14: 165
24. Hopkins FG, Pincus SN. Observations on the crystallisation of animal proteins. J Physiol. 1898; 23: 130-136
25. Sumner JB. The isolation and crystallization of the enzyme urease: preliminary paper. J Biol Chem. 1926; 69: 435-441
26. Abel JJ. Crystalline Insulin. Proc Natl Acad Sci USA. 1926; 12: 132-136
27. Abel JJ, Geiling EMK, Roultier OA, Bell FM, Wintersteiner O. Crystalline insulin. J Pharmacol Exp Ther. 1927; 31: 65-85
28. Northrop JH. Crystalline pepsin. Science (New York, NY). 1929; 69: 580
29. Stanley WM. Isolation of a crystalline protein possessing the properties of tobacco-mosaic virus. Science (New York, NY). 1935; 81: 644-645
30. Sumner JB, Dounce AL. Crystalline catalase. Science (New York, NY). 1937; 85: 366-367. Epub 1937/04/09
31. Bernal JD, Crowfoot DC. X-ray photographs of crystalline pepsin. Nature. 1934; 133: 794-795
32. Perutz M. Early days of protein crystallography. 1985/01/01 ed. New York: Methods Enzymol; 1985
33. Watson JD, Crick FH. Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature. 1953; 171: 737-738
34. Blake CC, Koenig DF, Mair GA, North AC, Phillips DC, Sarma VR. Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Angstrom resolution. Nature. 1965; 206: 757-761. Epub 1965/05/22
35. Johnson LN, Phillips DC. Structure of some crystalline lysozyme-inhibitor complexes determined by X-ray analysis at 6 Angstrom resolution. Nature. 1965; 206: 761-763. Epub 1965/05/22
36. Blow D. So do we understand how enzymes work? Structure (London, England: 1993). 2000; 8: R77-R81. Epub 2000/05/10
37. Poljak RJ, Amzel LM, Chen BL, Phizackerley RP, Saul F. The three-dimensional structure of the fab' fragment of a human myeloma immunoglobulin at 2.0-angstrom resolution. Proc Natl Acad Sci USA. 1974; 71: 3440-3444. Epub 1974/09/01
38. Poljak RJ, Amzel LM, Chen BL, Phizackerley RP, Saul F. Structure and specificity of antibody molecules. Phil Tran Roy Soc Lond Ser B Biol Sci. 1975; 272: 43-51. Epub 1975/11/06
39. Epp O, Lattman EE, Schiffer M, Huber R, Palm W. The molecular structure of a dimer composed of the variable portions of the Bence-Jones protein REI refined at 2.0-A resolution. Biochemistry. 1975; 14: 4943-4952. Epub 1975/11/04
40. Sarma R, Zaloga G. Structure studies on styrene-treated immunoglobulin crystals. J Mol Biol. 1975; 98: 479-484. Epub 1975/11/05
41. Jack A, Ladner JE, Klug A. Crystallographic refinement of yeast phenylalanine transfer RNA at 2-5A resolution. J Mol Biol. 1976; 108: 619-649. Epub 1976/12/25
42. Sussman JL, Kim S. Three-dimensional structure of a transfer RNA in two crystal forms. Science (New York, NY). 1976; 192: 853-858. Epub 1976/05/28
43. Boutet S, Lomb L, Williams GJ, Barends TR, Aquila A, Doak RB, Weierstall U, DePonte DP, Steinbrener J, Shoeman RL, Messerschmidt M, Barty A, White TA, Kassemeyer S, Kirian RA, Seibert MM, Montanez PA, Kenney C, Herbst R, Hart P, Pines J, Haller G, Gruner SM, Philipp HT, Tate MW, Hromalik M, Koerner LJ, van Bakel N, Morse J, Ghonsalves W, Arnlund D, Bogan MJ, Caleman C, Fromme R, Hampton CY, Hunter MS, Johansson LC, Katona G, Kupitz C, Liang M, Martin AV, Nass K, Redecke L, Stellato F, Timneanu N, Wang D, Zatsepin NA, Schafer D, Defever J, Neutze R, Fromme P, Spence JC, Chapman HN, Schlichting I. High-resolution protein structure determination by serial femtosecond crystallography. Science (New York, NY). 2012; 337: 362-364. Epub 2012/06/02
44. Hirata K, Shinzawa-Itoh K, Yano N, Takemura S, Kato K, Hatanaka M, Muramoto K, Kawahara T, Tsukihara T, Yamashita E, Tono K, Ueno G, Hikima T, Murakami H, Inubushi Y, Yabashi M, Ishikawa T, Yamamoto M, Ogura T, Sugimoto H, Shen JR, Yoshikawa S, Ago H. Determination of damage-free crystal structure of an X-ray-sensitive protein using an XFEL. Nat Meth. 2014; 11: 734-736. Epub 2014/05/13
45. Fisher SJ, Blakeley MP, Cianci M, McSweeney S, Helliwell JR. Protonation-state determination in proteins using high-resolution X-ray crystallography: effects of resolution and completeness. Acta Crystallogr D Biol Crystallogr. 2012; 68: 800-809. Epub 2012/07/04
46. Helliwell JR. Biochemistry. How to solve protein structures with an X-ray laser. Science (New York, NY). 2013; 339: 146-147. Epub 2013/01/12
47. Willstätter R. Problems and methods in enzyme research. Ithaca: Cornell University Press; 1927
48. McPherson A. Preparation and analysis of protein crystals. New York: Wiley and Sons; 1982
49. Bergfors TM. Protein crystallization. 2nd ed. La Jolla (CA): International University Line; 2009
50. Jancarik J, Kim S-H. Sparse matrix sampling: a screening method for crystallization of proteins. J Appl Crystallogr. 1991; 24: 409-411
51. Giegé R. A historical perspective on protein crystallization from 1840 to the present day. FEBS J. 2013; 280: 6456-6497
52. Miller WH. A treatise on crystallography. Cambridge: Printed at the Pitt Press for J. & JJ Deighton; 1839
53. Bravais A. Mémoire sur les systèmes formés par les points distribués régulièrement sur un plan ou dans l'espace. J Ecole Polytech. 1850; 19: 1-128
54. Burckhardt JJ. Zur Geschichte der Entdeckung der 230 Raumgruppen. Arch Hist Exact Sci. 1967; 4: 235-246
55. Hahn T. International tables for crystallography, volume A: space-group symmetry. 5th ed. Berlin: Springer-Verlag; 2002
56. Fourier J. Theorie analytique de la chaleur, par M. Fourier: Chez Firmin Didot, père et fils; 1822
57. Sayre D. The squaring method: a new method for phase determination. Acta Cryst. 1952; 5: 60-65 10.1107/S0365110X52000137
58. Cooley JW, Tukey JW. An algorithm for the machine calculation of complex Fourier series. Math Comput. 1965; 19: 297-301
59. Collaborative Computational Project Number 4 (CCP4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 1994; 50: 760-763. Epub 1994/09/01
60. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011; 67: 235-242 10.1107/S0907444910045749
61. Ten Eyck LF. Crystallographic fast Fourier transforms. Acta Crystallogr A Crys Phys Diffract Theor Gen Crystallogr. 1973; 29: 183-191
62. Ten Eyck LF. Efficient structure-factor calculation for large molecules by the fast Fourier transform. Acta Crystallogr A Crys Phys Diffract Theor Gen Crystallogr. 1977; 33: 486-492 doi: 10.1107/S0567739477001211
63. Agarwal RC. A new least-squares refinement technique based on the fast Fourier transform algorithm. Acta Crystallogr A Cryst Phys Diffract Theor Gen Crystallogr. 1978; 34: 791-809 doi: 10.1107/S0567739478001618
64. Green DW, Ingram VM, Perutz MF. The structure of hemoglobin. IV. Sign determination by the isomorphous replacement method. Proc R Soc London A. 1954; 225: 287-307
65. Blow DM, Crick FHC. The treatment of errors in the isomorphous replacement method. Acta Cryst. 1959; 12: 794-802 doi: 10.1107/S0365110X59002274
66. Rossmann MG. The position of anomalous scatterers in protein crystals. Acta Cryst. 1961; 14: 383-388 10.1107/S0365110X61001297
67. Matthews BW. The extension of the isomorphous replacement method to include anomalous scattering measurements. Acta Cryst. 1966; 20: 82-86
68. Otwinowski Z. Isomorphous replacement and anomalous scattering. Proceedings of the CCP4 Study Weekend; 1991 Jan 25-26; SERC Daresbury Laboratory, Warrington, UK
69. de La Fortelle E, Bricogne G. SHARP: A maximum-likelihood heavy-atom parameter refinement program for the MIR and MAD methods. Meth Enzymol. 1997; 276: 472-494 -6879(97)76073-7
70. Terwilliger TC, Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr. 1999; 55: 849-861
71. Furey W, Swaminathan S. PHASES-95: a program package for processing and analyzing diffraction data from macromolecules. Meth Enzymol. 1997; 277: 590-620 -6879(97)77033-2
72. Hendrickson WA, Horton JR, LeMaster DM. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 1990; 9: 1665-1672. Epub 1990/05/01
73. Hendrickson WA. Maturation of MAD phasing for the determination of macromolecular structures. J Synch Radiat. 1999; 6: 845-851
74. Ramakrishnan V, Biou V. Treatment of multiwavelength anomalous diffraction data as a special case of multiple isomorphous replacement. Meth Enzymol. 1997; 276: 538-557
75. Storoni LC, McCoy AJ, Read RJ. Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr. 2004; 60: 432-438
76. Hendrickson WA, Teeter MM. Structure of the hydrophobic protein crambin determined directly from the anomalous scattering of sulphur. Nature. 1981; 290: 107-113
77. Wang BC. Resolution of phase ambiguity in macromolecular crystallography. Meth Enzymol. 1985; 115: 90-112. Epub 1985/01/01
78. Dauter Z, Adamiak DA. Anomalous signal of phosphorus used for phasing DNA oligomer: importance of data redundancy. Acta Crystallogr D Biol Crystallogr. 2001; 57: 990-995 10.1107/S0907444901006382
79. Ramagopal UA, Dauter M, Dauter Z. Phasing on anomalous signal of sulfurs: what is the limit? Acta Crystallogr D Biol Crystallogr. 2003; 59: 1020-1027
80. Liu ZJ, Vysotski ES, Chen CJ, Rose JP, Lee J, Wang BC. Structure of the Ca2+-regulated photoprotein obelin at 1.714;Å resolution determined directly from its sulfur substructure. Prot Sci. 2000; 9: 2085-2093 10.1110/ps.9.11.2085
81. Ren H, Wang L, Bennett M, Liang Y, Zheng X, Lu F, Li L, Nan J, Luo M, Eriksson S. The crystal structure of human adenylate kinase 6: an adenylate kinase localized to the cell nucleus. Proc Natl Acad Sci USA. 2005; 102: 303-308
82. Yang C, Pflugrath J, Courville D, Stence C, Ferrara JD. Away from the edge: SAD phasing from the sulfur anomalous signal measured in-house with chromium radiation. Acta Crystallogr D Biol Crystallogr. 2003; 59: 1943-1957 10.1107/S0907444903018547
83. Rossmann MG. The molecular replacement method. New York: Gordon & Breach; 1972
84. Crowther RA, Amos LA. Three-dimensional image reconstructions of some small spherical viruses. Cold Spring Harb Symp Quant Biol. 1972; 36: 489-494. Epub 1972/01/01 10.1101/SQB.1972.036.01.062
85. Crowther R. The fast rotation function. Int Sci Rev Ser. 1972; 13: 173-178
86. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr A Found Crystallogr. 1994; 50: 157-163
87. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Crystallogr. 1997; 30: 1022-1025 doi: 10.1107/S0021889897006766
88. Kissinger CR, Gehlhaar DK, Fogel DB. Rapid automated molecular replacement by evolutionary search. Acta Crystallogr D Biol Crystallogr. 1999; 55: 484-491 10.1107/S0907444998012517
89. Glykos NM, Kokkinidis M. Multidimensional molecular replacement. Acta Crystallogr D Biol Crystallogr. 2001; 57: 1462-1473
90. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007; 40: 658-674
91. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002; 58: 1948-1954. Epub 2002/10/24
92. Das R, Baker D. Macromolecular modeling with Rosetta. Annu Rev Biochem. 2008; 77: 363-382 10.1146/annurev.biochem.77.062906.171838
93. DiMaio F, Terwilliger TC, Read RJ, Wlodawer A, Oberdorfer G, Wagner U, Valkov E, Alon A, Fass D, Axelrod HL. Improved molecular replacement by density-and energy-guided protein structure optimization. Nature. 2011; 473: 540-543
94. Mukherjee A, Helliwell J, Main P. The use of MULTAN to locate the positions of anomalous scatterers. Acta Crystallogr A Found Crystallogr. 1989; 45: 715-718 10.1107/S0108767389006239
95. Sheldrick GM, Gould RO. Structure solution by iterative peaklist optimization and tangent expansion in space group P1. Acta Crystallogr B Struct Sci. 1995; 51: 423-431 10.1107/S0108768195003661
96. Miller R, Gallo SM, Khalak H, Weeks C. SnB: crystal structure determination via shake-and-bake. J Appl Crystallogr. 1994; 27: 613-621
97. Foadi J, Woolfson M, Dodson E, Wilson K, Jia-xing Y, Chao-de Z. A flexible and efficient procedure for the solution and phase refinement of protein structures. Acta Crystallogr D Biol Crystallogr. 2000; 56: 1137-1147 10.1107/S090744490000932X
98. de Graaff RA, Hilge M, van der Plas JL, Abrahams JP. Matrix methods for solving protein substructures of chlorine and sulfur from anomalous data. Acta Crystallogr D Biol Crystallogr. 2001; 57: 1857-1862
99. Wang J, Chen J, Gu Y, Zheng C, Jiang F, Fan H, Terwilliger T, Hao Q. SAD phasing by combination of direct methods with the SOLVE/RESOLVE procedure. Acta Crystallogr D Biol Crystallogr. 2004; 60: 1244-1253 10.1107/S0907444904010674
100. Yao DQ, Huang S, Wang JW, Gu YX, Zheng CD, Fan HF, Watanabe N, Tanaka I. SAD phasing by OASIS-2004: case studies of dual-space fragment extension. Acta Crystallogr D Biol Crystallogr. 2006; 62: 883-890
101. He Y, Yao D-Q, Gu Y-X, Lin Z-J, Zheng C-D, Fan H-F. OASIS and molecular-replacement model completion. Acta Crystallogr D Biol Crystallogr. 2007; 63: 793-799 10.1107/S0907444907023451
102. Bricogne G. Methods and programs for direct-space exploitation of geometric redundancies. Acta Crystallogr A Crys Phys Diffract, Theor Gen Crystall. 1976; 32: 832-847 10.1107/S0567739476001691
103. Zhang K, Main P. The use of Sayre's equation with solvent flattening and histogram matching for phase extension and refinement of protein structures. Acta Crystallogr A Found Crystallogr. 1990; 46: 377-381
104. Cowtan K. DM: an automated procedure for phase improvement by density modification. Joint CCP4 ESF-EACBM Newslett Prot Crystallogr. 1994; 31: 34-38
105. Terwilliger TC. Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr. 2000; 56: 965-972 10.1107/S0907444900005072
106. Abrahams J, Leslie A. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogra D Biol Crystall. 1996; 52: 30-42 10.1107/S0907444995008754
107. Jones TA. A graphics model building and refinement system for macromolecules. J Appl Crystallogr. 1978; 11: 268-272 10.1107/S0021889878013308
108. Jones TA, Zou J-Y, Cowan St, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A Found Crystallogr. 1991; 47: 110-119
109. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D. 2004; 60: 2126-2132 doi: 10.1107/S0907444904019158
110. McRee DE. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J Struct Biol. 1999; 125: 156-165
111. Oldfield T. From maps to molecules in minutes. Acta Crystallogr A. 2000; 56: s27
112. Gurusaran M, Shankar M, Nagarajan R, Helliwell JR, Sekar K. Do we see what we should see? Describing non-covalent interactions in protein structures including precision. IUCrJ. 2014; 1: 74-81. Epub 2014/07/31
113. Perrakis A, Morris R, Lamzin VS. Automated protein model building combined with iterative structure refinement. Nat Struct Biol. 1999; 6: 458-463. Epub 1999/05/20
114. Cowtan K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr. 2006; 62: 1002-1011
115. Isaacs N, Agarwal R. Experience with fast Fourier least squares in the refinement of the crystal structure of rhombohedral 2-zinc insulin at 1.5 A resolution. Acta Crystallogr A Crys Phys Diffract Theor Gen Crystallogr. 1978; 34: 782-791
116. Konnert J. A restrained-parameter structure-factor least-squares refinement procedure for large asymmetric units. Acta Crystallogr A. 1976; 32: 614-617
117. Konnert JH, Hendrickson WA. A restrained-parameter thermal-factor refinement procedure. Acta Crystallogr A. 1980; 36: 344-350
118. Tronrud DE, Ten Eyck LF, Matthews BW. An efficient general-purpose least-squares refinement program for macromolecular structures. Acta Crystallogr A. 1987; 43: 489-501
119. Brunger AT, Kuriyan J, Karplus M. Crystallographic R factor refinement by molecular dynamics. Science (New York, NY). 1987; 235: 458-460. Epub 1987/01/23 10.1126/science.235.4787.458
120. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D. 1998; 54: 905-921 10.1107/S0907444998003254
121. Brunger AT. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 1992; 355: 472-475. Epub 1992/01/30
122. Sheldrick GM, Schneider TR. SHELXL: high-resolution refinement. Meth Enzymol. 1997; 277: 319-343. Epub 1997/01/01
123. Cruickshank D. Remarks about protein structure precision. Acta Crystallogr D Biol Crystallogr. 1999; 55: 583-601 10.1107/S0907444998012645
124. Blow D. Rearrangement of Cruickshank's formulae for the diffraction-component precision index. Acta Crystallogr D Biol Crystallogr. 2002; 58: 792-797
125. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D. 1997; 53: 240-255
126. Bricogne G, Irwin J. Maximum-likelihood refinement of incomplete models with BUSTER+ TNT. Macromolecular Refinement Proceedings of the CCP4 Study Weekend at Chester College. 1996;1996:85-92
127. Zwart PH, Afonine PV, Grosse-Kunstleve RW, Hung L-W, Ioerger TR, McCoy AJ, McKee E, Moriarty NW, Read RJ, Sacchettini JC. Automated structure solution with the PHENIX suite. Structural Proteomics. New York: Springer; 2008. p. 419-435
128. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD. Towards automated crystallographic structure refinement with phenix. refine. Acta Crystallogr D Biol Crystallogr. 2012; 68: 352-367
129. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr. 1993; 26: 283-291 10.1107/S0021889892009944
130. Hooft R, Vriend G, Sander C, Abola EE. Errors in protein structures. Nature. 1996; 381: 272
131. Vaguine AA, Richelle J, Wodak SJ. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D. 1999; 55: 191-205 10.1107/S0907444998006684
132. Davis IW, Murray LW, Richardson JS, Richardson DC. MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucl Acid Res. 2004; 32: W615-W619. Epub 2004/06/25
133. Arndt UW. Personal X-ray reflections. Meth Enzymol. 2003; 368: 21-42. Epub 2003/12/17
134. Arndt UW, Long JVP, Duncumb P. A microfocus X-ray tube used with focusing collimators. J Appl Crystallogr. 1998; 31: 936-944
135. Holmes KC, Rosenbaum G. How x-ray diffraction with synchrotron radiation got started. J Synch Radiat. 1998; 5: 147-153
136. Phillips JC, Wlodawer A, Yevitz MM, Hodgson KO. Applications of synchrotron radiation to protein crystallography: preliminary results. Proc Natl Acad Sci USA. 1976; 73: 128-132. Epub 1976/01/01
137. Buerger MJ. The precession method in x-ray crystallography. New York: Wiley; 1964
138. Arndt UW, Phillips DC. The linear diffractometer. Acta Crystallogr. 1961; 14: 807-818
139. Arndt UW, Willis BTM. Single-crystal diffractometry. London: Cambridge University Press; 1966
140. Schleputz C, Herger R, Willmott P, Patterson B, Bunk O, Bronnimann C, Henrich B, Hulsen G, Eikenberry E. Improved data acquisition in grazing-incidence X-ray scattering experiments using a pixel detector. Acta Crystallogr A Found Crystallogr. 2005; 61: 418-425
141. Trueb P, Sobott B, Schnyder R, Loeliger T, Schneebeli M, Kobas M, Rassool R, Peake D, Broennimann C. Improved count rate corrections for highest data quality with PILATUS detectors. J Synch Radiat. 2012; 19: 347-351
142. Hasegawa K, Hirata K, Shimizu T, Shimizu N, Hikima T, Baba S, Kumasaka T, Yamamoto M. Development of a shutterless continuous rotation method using an X-ray CMOS detector for protein crystallography. J Appl Crystallogr. 2009; 42: 1165-1175
143. Otwinowski Z, Minor W. [20] Processing of X-ray diffraction data collected in oscillation mode. In: Carter CW Jr., editor. Methods in enzymology. Vol. 276. Academic Press; 1997. p. 307-326
144. Leslie A. Jnt CCP4/ESF-EACBM Newsl. Protein Crystallogr. 1992; 26: 27-33
145. Kabsch W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J Appl Crystallogr. 1988; 21: 916-924
146. Pflugrath J. The finer things in X-ray diffraction data collection. Acta Crystallogr D. 1999; 55: 1718-1725 10.1107/S090744499900935X
147. Howard A. Data processing in macromolecular crystallography. In: Bourne PE, Watenpaugh KD., editors. Chapter in: crystallographic computing 7: proceedings from the macromolecular crystallographic computing school, 1996. Oxford: Oxford University Press; 2000
148. Campbell JW. Lauegen, an X-windows-based program for the processing of Laue X-ray-diffraction data. J Appl Crystallogr. 1995; 28: 228-236
149. Hope H. Cryocrystallography of biological macromolecules: a generally applicable method. Acta Crystallogr B. 1988; 44: 22-26
150. Teng T-Y. Mounting of crystals for macromolecular crystallography in a free-standing thin film. J Appl Crystallogr. 1990; 23: 387-391
151. Jackson DA, Symons RH, Berg P. Biochemical method for inserting new genetic information into DNA of Simian Virus 40: circular SV40 DNA molecules containing lambda phage genes and the galactose operon of Escherichia coli. Proc Natl Acad Sci. 1972; 69: 2904-2909
152. Ducruix A, Giegé R. Crystallization of nucleic acids and proteins: a practical approach. Oxford: IRL Press at Oxford University Press; 1992
153. Davies DR, Segal D. [25] Protein crystallization: micro techniques involving vapor diffusion. Meth Enzymol. 1971; 22: 266-269
154. Landau EM, Rosenbusch JP. Lipidic cubic phases: a novel concept for the crystallization of membrane proteins. Proc Natl Acad Sci. 1996; 93: 14532-14535
155. Chiu ML, Nollert P, Loewen MeC, Belrhali H, Pebay-Peyroula E, Rosenbusch JP, Landau EM. Crystallization in cubo: general applicability to membrane proteins. Acta Crystallogr D Biol Crystallogr. 2000; 56: 781-784 10.1107/S0907444900004716
156. Chayen NE, Shaw Stewart P, Maeder D, Blow D. An automated system for micro-batch protein crystallization and screening. J Appl Crystallogr. 1990; 23: 297-302 10.1107/S0021889890003260
157. Weselak M, Patch MG, Selby TL, Knebel G, Stevens RC. Robotics for automated crystal formation and analysis. Meth Enzymol. 2003; 368: 45-76
158. Aricescu AR, Assenberg R, Bill RM, Busso D, Chang VT, Davis SJ, Dubrovsky A, Gustafsson L, Hedfalk K, Heinemann U, Jones IM, Ksiazek D, Lang C, Maskos K, Messerschmidt A, Macieira S, Peleg Y, Perrakis A, Poterszman A, Schneider G, Sixma TK, Sussman JL, Sutton G, Tarboureich N, Zeev-Ben-Mordehai T, Jones EY. Eukaryotic expression: developments for structural proteomics. Acta Crystallogr D Biol Crystallogr. 2006; 62: 1114-1124. Epub 2006/09/27
159. Lee JK, Stroud RM. Unlocking the eukaryotic membrane protein structural proteome. Curr Opin Struct Biol. 2010; 20: 464-470. Epub 2010/08/27
160. Nettleship JE, Assenberg R, Diprose JM, Rahman-Huq N, Owens RJ. Recent advances in the production of proteins in insect and mammalian cells for structural biology. J Struct Biol. 2010; 172: 55-65. Epub 2010/02/16
161. Macauley-Patrick S, Fazenda ML, McNeil B, Harvey LM. Heterologous protein production using the Pichia pastoris expression system. Yeast. 2005; 22: 249-270. Epub 2005/02/11
162. Boer E, Steinborn G, Kunze G, Gellissen G. Yeast expression platforms. Appl Microbiol Biotechnol. 2007; 77: 513-523. Epub 2007/10/10
163. Long SB, Campbell EB, Mackinnon R. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science (New York, NY). 2005; 309: 897-903. Epub 2005/07/09
164. Long SB, Tao X, Campbell EB, MacKinnon R. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature. 2007; 450: 376-382. Epub 2007/11/16
165. Vaughn JL, Goodwin RH, Tompkins GJ, McCawley P. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro. 1977; 13: 213-217. Epub 1977/04/01
166. Smith GE, Summers MD, Fraser MJ. Production of human beta interferon in insect cells infected with a baculovirus expression vector. Mol Cell Biol. 1983; 3: 2156-2165. Epub 1983/12/01
167. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VR, Sanishvili R, Fischetti RF, Schertler GF, Weis WI, Kobilka BK. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature. 2007; 450: 383-387. Epub 2007/10/24
168. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, Stevens RC. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science (New York, NY). 2007; 318: 1258-1265. Epub 2007/10/27
169. Brillet K, Pereira CA, Wagner R. Expression of membrane proteins in Drosophila Melanogaster S2 cells: production and analysis of a EGFP-fused G protein-coupled receptor as a model. Meth Mol Biol. 2010; 601: 119-133. Epub 2010/01/26
170. Aricescu AR, Owens RJ. Expression of recombinant glycoproteins in mammalian cells: towards an integrative approach to structural biology. Curr Opin Struct Biol. 2013; 23: 345-356. Epub 2013/04/30
171. Yang H, Rudge DG, Koos JD, Vaidialingam B, Yang HJ, Pavletich NP. mTOR kinase structure, mechanism and regulation. Nature. 2013; 497: 217-223. Epub 2013/05/03
172. Yokoyama S. Protein expression systems for structural genomics and proteomics. Curr Opin Chem Biol. 2003; 7: 39-43
173. Kimura-Soyema T, Shirouzu M, Yokoyama S. Cell-free membrane protein expression. Cell-Free Protein Synthesis. New York: Springer; 2014. p. 267-273
174. Heinemann U. Structural genomics in Europe: slow start, strong finish? Nat Struct Mol Biol. 2000; 7: 940-942
175. Terwilliger TC. Structural genomics in North America. Nat Struct Mol Biol. 2000; 7: 935-939
176. Yokoyama S, Hirota H, Kigawa T, Yabuki T, Shirouzu M, Terada T, Ito Y, Matsuo Y, Kuroda Y, Nishimura Y. Structural genomics projects in Japan. Nat Struct Mol Biol. 2000; 7: 943-945
177. Burley SK, Almo SC, Bonanno JB, Capel M, Chance MR, Gaasterland T, Lin D, Šali A, Studier FW, Swaminathan S. Structural genomics: beyond the human genome project. Nat Genet. 1999; 23: 151-157
178. Collins FS, Morgan M, Patrinos A. The human genome project: lessons from large-scale biology. Science (New York, NY). 2003; 300: 286-290
179. Consortium GP. A map of human genome variation from population-scale sequencing. Nature. 2010; 467: 1061-1073
180. Siva N. 1000 Genomes project. Nat Biotechnol. 2008; 26: 256
181. Stevens RC, Yokoyama S, Wilson IA. Global efforts in structural genomics. Science (New York, NY). 2001; 294: 89-92 doi: 10.1126/science.1066011
182. Lesley SA, Kuhn P, Godzik A, Deacon AM, Mathews I, Kreusch A, Spraggon G, Klock HE, McMullan D, Shin T. Structural genomics of the Thermotoga maritima proteome implemented in a high-throughput structure determination pipeline. Proc Natl Acad Sci. 2002; 99: 11664-11669
183. Li L, Nan J, Li D, Brostromer E, Wang Z, Liu C, Hou Q, Fan X, Ye Z, Su XD. Structural genomics studies of human caries pathogen Streptococcus mutans. J Struct Funct Genom. 2014. Epub 2014/01/30
184. Chance MR, Fiser A, Sali A, Pieper U, Eswar N, Xu G, Fajardo JE, Radhakannan T, Marinkovic N. High-throughput computational and experimental techniques in structural genomics. Genome Res. 2004; 14: 2145-2154 10.1101/gr.2537904
185. Joachimiak A. High-throughput crystallography for structural genomics. Curr Opini Struct Biol. 2009; 19: 573-584
186. Jeon WB, Aceti DJ, Bingman CA, Vojtik FC, Olson AC, Ellefson JM, McCombs JE, Sreenath HK, Blommel PG, Seder KD. High-throughput purification and quality assurance of Arabidopsis thaliana proteins for eukaryotic structural genomics. J Struct Funct Genom. 2005; 6: 143-147
187. Montelione GT, Zheng D, Huang YJ, Gunsalus KC, Szyperski T. Protein NMR spectroscopy in structural genomics. Nat Struct Mol Biol. 2000; 7: 982-985
188. Adams MW, Dailey HA, DeLucas LJ, Luo M, Prestegard JH, Rose JP, Wang B-C. The southeast collaboratory for structural genomics: a high-throughput gene to structure factory. Acc Chem Res. 2003; 36: 191-198
189. Goh C-S, Lan N, Douglas SM, Wu B, Echols N, Smith A, Milburn D, Montelione GT, Zhao H, Gerstein M. Mining the structural genomics pipeline: identification of protein properties that affect high-throughput experimental analysis. J Mol Biol. 2004; 336: 115-130
190. Elsliger M-A, Deacon AM, Godzik A, Lesley SA, Wooley J, Wuthrich K, Wilson IA. The JCSG high-throughput structural biology pipeline. Acta Crystallogr F. 2010; 66: 1137-1142 10.1107/S1744309110038212
191. Hui R, Edwards A. High-throughput protein crystallization. J Struct Biol. 2003; 142: 154-161
192. Zheng B, Roach LS, Ismagilov RF. Screening of protein crystallization conditions on a microfluidic chip using nanoliter-size droplets. J Am Chem Soc. 2003; 125: 11170-11171
193. Santarsiero BD, Yegian DT, Lee CC, Spraggon G, Gu J, Scheibe D, Uber DC, Cornell EW, Nordmeyer RA, Kolbe WF, Jin J, Jones AL, Jaklevic JM, Schultz PG, Stevens RC. An approach to rapid protein crystallization using nanodroplets. J Appl Crystallogr. 2002; 35: 278-281
194. Berry IM, Dym O, Esnouf RM, Harlos K, Meged R, Perrakis A, Sussman JL, Walter TS, Wilson J, Messerschmidt A. SPINE high-throughput crystallization, crystal imaging and recognition techniques: current state, performance analysis, new technologies and future aspects. Acta Crystallogra D Biol Crystallogr. 2006; 62: 1137-1149. Epub 2006/09/27
195. Cohen AE, Ellis PJ, Miller MD, Deacon AM, Phizackerley RP. An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot. J Appl Crystallogr. 2002; 35: 720-726 10.1107/S0021889802016709
196. Snell G, Cork C, Nordmeyer R, Cornell E, Meigs G, Yegian D, Jaklevic J, Jin J, Stevens RC, Earnest T. Automated sample mounting and alignment system for biological crystallography at a synchrotron source. Structure (London, England: 1993). 2004; 12: 537-545
197. Gonzalez A, Moorhead P, McPhillips S, Song J, Sharp K, Taylor J, Adams P, Sauter N, Soltis S. Web-ice: integrated data collection and analysis for macromolecular crystallography. J Appl Crystallogr. 2008; 41: 176-184 10.1107/S0021889807057822
198. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M. HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr. 2006; 62: 859-866. Epub 2006/07/21
199. Liu G, Shen Y, Atreya HS, Parish D, Shao Y, Sukumaran DK, Xiao R, Yee A, Lemak A, Bhattacharya A, Acton TA, Arrowsmith CH, Montelione GT, Szyperski T. NMR data collection and analysis protocol for high-throughput protein structure determination. Proc Natl Acad Sci USA. 2005; 102: 10487-10492. Epub 2005/07/20
200. Gabanyi MJ, Adams PD, Arnold K, Bordoli L, Carter LG, Flippen-Andersen J, Gifford L, Haas J, Kouranov A, McLaughlin WA, Micallef DI, Minor W, Shah R, Schwede T, Tao YP, Westbrook JD, Zimmerman M, Berman HM. The structural biology knowledgebase: a portal to protein structures, sequences, functions, and methods. J Struct Funct Genom. 2011; 12: 45-54. Epub 2011/04/08
201. Su XD, Liang Y, Li L, Nan J, Brostromer E, Liu P, Dong Y, Xian D. A large-scale, high-efficiency and low-cost platform for structural genomics studies. Acta Crystallogr D Biol Crystallogr. 2006; 62: 843-851. Epub 2006/07/21 10.1107/S0907444906024395
202. Brostromer E, Nan J, Su XD. An automated image-collection system for crystallization experiments using SBS standard microplates. Acta Crystallogr D, Biol Crystallogr. 2007; 63: 119-125. Epub 2007/01/24
203. Ajdić D, McShan WM, McLaughlin RE, Savić G, Chang J, Carson MB, Primeaux C, Tian R, Kenton S, Jia H. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci. 2002; 99: 14434-14439
204. Neutze R, Moffat K. Time-resolved structural studies at synchrotrons and X-ray free electron lasers: opportunities and challenges. Curr Opin Struct Biol. 2012; 22: 651-659
205. Chapman HN, Fromme P, Barty A, White TA, Kirian RA, Aquila A, Hunter MS, Schulz J, DePonte DP, Weierstall U, Doak RB, Maia FR, Martin AV, Schlichting I, Lomb L, Coppola N, Shoeman RL, Epp SW, Hartmann R, Rolles D, Rudenko A, Foucar L, Kimmel N, Weidenspointner G, Holl P, Liang M, Barthelmess M, Caleman C, Boutet S, Bogan MJ, Krzywinski J, Bostedt C, Bajt S, Gumprecht L, Rudek B, Erk B, Schmidt C, Homke A, Reich C, Pietschner D, Struder L, Hauser G, Gorke H, Ullrich J, Herrmann S, Schaller G, Schopper F, Soltau H, Kuhnel KU, Messerschmidt M, Bozek JD, Hau-Riege SP, Frank M, Hampton CY, Sierra RG, Starodub D, Williams GJ, Hajdu J, Timneanu N, Seibert MM, Andreasson J, Rocker A, Jonsson O, Svenda M, Stern S, Nass K, Andritschke R, Schroter CD, Krasniqi F, Bott M, Schmidt KE, Wang X, Grotjohann I, Holton JM, Barends TR, Neutze R, Marchesini S, Fromme R, Schorb S, Rupp D, Adolph M, Gorkhover T, Andersson I, Hirsemann H, Potdevin G, Graafsma H, Nilsson B, Spence JC. Femtosecond X-ray protein nanocrystallography. Nature. 2011; 470: 73-77. Epub 2011/02/05
206. Seibert MM, Ekeberg T, Maia FR, Svenda M, Andreasson J, Jönsson O, Odić D, Iwan B, Rocker A, Westphal D. Single mimivirus particles intercepted and imaged with an X-ray laser. Nature. 2011; 470: 78-81
207. Chapman HN, Barty A, Bogan MJ, Boutet S, Frank M, Hau-Riege SP, Marchesini S, Woods BW, Bajt S, Benner WH. Femtosecond diffractive imaging with a soft-X-ray free-electron laser. Nat Phys. 2006; 2: 839-843
208. Redecke L, Nass K, DePonte DP, White TA, Rehders D, Barty A, Stellato F, Liang M, Barends TR, Boutet S. Natively inhibited Trypanosoma brucei Cathepsin B structure determined by using an X-ray laser. Science (New York, NY). 2013; 339: 227-230 10.1126/science.1229663
209. Barends TR, Foucar L, Botha S, Doak RB, Shoeman RL, Nass K, Koglin JE, Williams GJ, Boutet S, Messerschmidt M. De novo protein crystal structure determination from X-ray free-electron laser data. Nature. 2014; 505: 244-247
210. Qu K, Zhou L, Dong Y-H. An improved integration method in serial femtosecond crystallography. Acta Crystallogr D. 2014; 70: 1202-1211