A brief history of macromolecular crystallography, illustrated by a family tree and its Nobel fruits

FEBS Journal

Volumn 281, Issue 18, 2014, Pages 3985-4009

  Jaskolski, Mariusz ^a   Dauter, Zbigniew ^b   Wlodawer, Alexander ^c  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

history of crystallography; macromolecular crystallography; nobel prizes; structural biology; structural crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEMOGLOBIN; MEMBRANE RECEPTOR; MYOGLOBIN; MACROMOLECULE; MEMBRANE PROTEIN;

CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; DNA STRUCTURE; DRUG DESIGN; ENERGY METABOLISM; ENZYME STRUCTURE; HUMAN; HYDROGEN BOND; MACROMOLECULAR CRYSTALLOGRAPHY; MEMBRANE CHANNEL; MOLECULAR IMAGING; NEUTRON; PROCESS DEVELOPMENT; REVIEW; RIBOSOME; RNA STRUCTURE; STRUCTURAL GENOMICS; STRUCTURE ANALYSIS; VIRUS MORPHOLOGY; X RAY DIFFRACTION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; HISTORY; MACROMOLECULE; PROTEIN CONFORMATION; ULTRASTRUCTURE; VIRION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; HISTORY, 20TH CENTURY; HUMANS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; RIBOSOMES; VIRION;

EID: 84909955199     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12796     Document Type: Review

References (215)

1. Röntgen WC, (1896) On a new kind of rays. Science 3, 227-231.
2. Röntgen WC, (1896) A new form of radiation. Science 3, 726-729.
3. Friedrich W, Knipping P, &, Laue M, (1912) Interferenz-Erscheinungen bei Röntgenstrahlen. Sitz Bayer Akad Wiss, 303-322.
4. Bragg WL, (1913) The diffraction of short electromagnetic waves by a crystal. Proc Camb Philos Soc 17, 43-57.
5. Bragg WH, (1912) X-rays and crystals. Nature 90, 219.
6. Bragg WH, &, Bragg WL, (1913) The reflection of X-rays by crystals. Proc Roy Soc Lond A 88, 428-438.
7. Bragg WH, (1913) The reflection of X-rays by crystals (II). Proc Roy Soc Lond A 89, 246-248.
8. Bragg WL, (1913) The structure of some crystals as indicated by their diffraction of X-rays. Proc R Soc Lond A 89, 248-277.
9. Bragg WH, &, Bragg WL, (1913) The structure of the diamond. Proc R Soc Lond A 89, 277-291.
10. Authier A, (2013) Early Days of X-ray Crystallography. Oxford University Press, Oxford, UK.
11. Giege R, (2013) A historical perspective on protein crystallization from 1840 to the present day. FEBS J 280, 6456-6497.
12. Hünefeld FL, (1840) Die Chemismus in der tierescher Organisation, p. 160, FA Brockhouse, Leipzig.
13. Reichert ET, &, Brown AP, (1909) The Differentiation and Specificity of Corresponding Proteins and their Vital Substances in Relation to Biological Classification and Organic Evolution. Carnegie Institution of Washington, Washington DC.
14. Perutz MF, Rossmann MG, Cullis AF, Muirhead H, Will G, &, North ACT, (1960) Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-Å resolution, obtained by X-ray analysis. Nature 185, 416-421.
15. Sumner JB, (1926) The isolation and crystallization of the enzyme urease. J Biol Chem 69, 435-441.
16. Bernal JD, &, Crowfoot D, (1934) X-ray photographs of crystalline pepsin. Nature 133, 794-795.
17. Cooper JB, Khan G, Taylor G, Tickle IJ, &, Blundell TL, (1990) X-ray analyses of aspartic proteinases. II. Three-dimensional structure of the hexagonal crystal form of porcine pepsin at 2.3 Å resolution. J Mol Biol 214, 199-222.
18. Andreeva NS, Fedorov AA, Gushchina AE, Riskulov RR, Shutskever NE, &, Safro MG, (1978) X-ray structural analysis of pepsin. V. Conformation of the main chain of the enzyme. Mol Biol (Mosk) 12, 922-936.
19. Bernal JD, (1939) Structure of proteins. Nature 143, 663-667.
20. Balasubramanian A, &, Ponnuraj K, (2010) Crystal structure of the first plant urease from jack bean: 83 years of journey from its first crystal to molecular structure. J Mol Biol 400, 274-283.
21. Crowfoot D, (1935) X-ray single crystal photographs of insulin. Nature 135, 591-592.
22. Adams MJ, Blundell TL, Dodson EJ, Dodson GG, Vijayan M, Baker EN, Harding MM, Hodgkin DC, Rimmer B, &, Sheat S, (1969) Structure of rhombohedral 2 zinc insulin crystals. Nature 224, 491-495.
23. Baker EN, Blundell TL, Cutfield JF, Cutfield SM, Dodson EJ, Dodson GG, Hodgkin DM, Hubbard RE, Isaacs NW, Reynolds CD, et al,. (1988) The structure of 2Zn pig insulin crystals at 1.5 Å resolution. Philos Trans R Soc Lond B Biol Sci 319, 369-456.
24. Menting JG, Whittaker J, Margetts MB, Whittaker LJ, Kong GK, Smith BJ, Watson CJ, Zakova L, Kletvikova E, Jiracek J, et al,. (2013) How insulin engages its primary binding site on the insulin receptor. Nature 493, 241-245.
25. Carlisle CH, &, Crowfoot D, (1945) The crystal structure of cholesteryl iodide. Proc R Soc Lond A 184, 64-83.
26. Crowfoot D, Bun CW, Rogers-Low BW, &, Turner-Jones A, (1949) X-ray crystallographic investigation of the structure of penicillin. In Chemistry of Penicillin (, Clarke H, Johnson T, Robinson JR, eds.) pp. 310-367. University Press, Princeton, NJ.
27. 12. Proc R Soc Lond A 242, 228-263.
28. Perutz M, (1997) Science is Not a Quiet Life. World Scientific Publishing Co., Singapore.
29. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, &, Phillips DC, (1958) A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181, 662-666.
30. Kendrew JC, Dickerson RE, Strandberg BE, Hart RG, Davies DR, Phillips DC, &, Shore VC, (1960) Structure of myoglobin. A three-dimensional Fourier synthesis at 2 Å resolution. Nature 185, 422-427.
31. Green DW, Ingram VM, &, Perutz MF, (1954) The structure of haemoglobin. IV. Sign determination by the isomorphous replacement method. Proc R Soc Lond A 225, 287-307.
32. Kendrew J, (1996) Protein crystallography and computing: recollections of the 50s. Acta Crystallogr A52, C-7.
33. Perutz MF, (1964) The hemoglobin molecule. Sci Am 211, 64-76.
34. Pauling L, (1992) How I became interested in the chemical bond: a reminiscence. In The Chemical Bond Structure and Dynamics (, Zewail A, ed.), pp. 3-16. Academic Press, San Diego.
35. Dickinson RG, &, Pauling L, (1923) The crystal structure of molybdenite. J Am Chem Soc 45, 1466-1471.
36. Pauling L, (1993) How my interest in proteins developed. Protein Sci 2, 1060-1063.
37. Edison AS, (2001) Linus Pauling and the planar peptide bond. Nat Struct Biol 8, 201-202.
38. Pauling L, Corey RB, &, Branson HR, (1951) The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci USA 37, 205-211.
39. Astbury WT, &, Street A, (1932) X-ray studies of the structure of hair, wool, and related fibres. Phil Trans Roy Soc Ser A 230, 75-101.
40. Astbury WT, &, Woods HJ, (1934) X-ray studies of the structure of hair, wool, and related fibres. II. The molecular structure and elastic properties of hair keratin. Phil Trans Roy Soc Ser A 232, 333-394.
41. Pauling L, &, Corey RB, (1951) The pleated sheet, a new layer configuration of polypeptide chains. Proc Natl Acad Sci USA 37, 251-256.
42. Pauling L, &, Corey RB, (1953) A proposed structure for the nucleic acids. Proc Natl Acad Sci USA 39, 84-97.
43. Lipscomb WA, Coppola JC, Hartsuck JA, Ludwig ML, Muirhead H, Searl J, &, Steitz TA, (1966) The structure of carboxypeptidase A: III. Molecular structure at 6 Å resolution. J Mol Biol 19, 423-441.
44. Reeke GN, Hartsuck JA, Ludwig ML, Quiocho FA, Steitz TA, &, Lipscomb WN, (1967) The structure of carboxypeptidase A, VI. Some results at 2.0 Å resolution, and the complex with glycyl-tyrosine at 2.8 Å resolution. Proc Natl Acad Sci USA 58, 2220-2226.
45. Warren SG, Edwards BF, Evans DR, Wiley DC, &, Lipscomb WN, (1973) Aspartate transcarbamoylase from Escherichia coli: electron density at 5.5 A resolution. Proc Natl Acad Sci USA 70, 1117-1121.
46. Szabo A, &, Karplus M, (1972) A mathematical model for structure-function relationships in hemoglobin. Biochem Biophys Res Commun 46, 855-860.
47. Kartha G, Bello J, &, Harker D, (1967) Tertiary structure of ribonuclease. Nature 213, 862-865.
48. Arndt UW, &, Wonacott AJ, (1977) The Rotation Method in Crystallography: Data Collection from Macromolecular Crystals. North Holland Pub. Co., Amsterdam.
49. Dauter Z, Jaskolski M, &, Wlodawer A, (2010) Impact of synchrotron radiation on macromolecular crystallography: a personal view. J Synchrotron Radiat 17, 433-444.
50. Rosenbaum G, Holmes KC, &, Witz J, (1971) Sychrotron radiation as a source for X-ray diffraction. Nature 230, 434-437.
51. Phillips JC, Wlodawer A, Yevitz MM, &, Hodgson KO, (1976) Applications of synchrotron radiation to protein crystallography: preliminary results. Proc Natl Acad Sci USA 73, 128-132.
52. Harmsen A, Leberman R, &, Schulz GE, (1976) Comparison of protein crystal diffraction patterns and absolute intensities from synchrotron and conventional X-ray sources. J Mol Biol 104, 311-314.
53. Chapman HN, Fromme P, Barty A, White TA, Kirian RA, Aquila A, Hunter MS, Schulz J, DePonte DP, Weierstall U, et al,. (2011) Femtosecond X-ray protein nanocrystallography. Nature 470, 73-77.
54. Hope H, (1988) Cryocrystallography of biological macromolecules: a generally applicable method. Acta Crystallogr D44, 22-26.
55. Barends TR, Foucar L, Botha S, Doak RB, Shoeman RL, Nass K, Koglin JE, Williams GJ, Boutet S, Messerschmidt M, et al,. (2013) De novo protein crystal structure determination from X-ray free-electron laser data. Nature 505, 244-247.
56. Patterson AL, (1934) A Fourier series method for the determination of the components of interatomic distances in crystals. Phys Rev 46, 372-376.
57. Lipson H, &, Beevers CA, (1935) The crystal structure of the alums. Proc R Soc Lond A 148, 664-680.
58. Robertson JM, (1936) An X-ray study of phtalocyanines. Part II. Quantitative structure determination of the metal-free compound. J Chem Soc 1936, 1195-1209.
59. Perutz MF, (1983) Review of 'Structural crystallography in chemistry and biology: benchmark papers in physical chemistry and chemical physics. Vol. 4'. Acta Crystallogr B39, 139-141.
60. Blow DM, &, Crick FH, (1959) The treatment of errors in the isomorphous replacement method. Acta Crystallogr 12, 794-802.
61. Ramachandran GN, &, Raman S, (1956) A new method for the structure analysis of non-centrosymmetric crystals. Curr Sci 25, 348-351.
62. Rossmann MG, (1961) The position of anomalous scatterers in protein crystals. Acta Crystallogr 14, 383-388.
63. Karle J, (1980) Some developments in anomalous dispersion for the structural investigation of macromolecular systems in biology. Int J Quantum Chem S7, 357-367.
64. Hendrickson WA, &, Teeter MM, (1981) Structure of the hydrophobic protein crambin determined directly from the anomalous scattering of sulfur. Nature 290, 107-113.
65. Kahn R, Fourme R, Bosshard R, Chiadmi M, Risler JL, Dideberg O, &, Wery JP, (1985) Crystal structure study of Opsanus tau parvalbumin by multiwavelength anomalous diffraction. FEBS Lett 179, 133-137.
66. Guss JM, Merritt EA, Phizackerley RP, Hedman B, Murata M, Hodgson KO, &, Freeman HC, (1988) Phase determination by multiple-wavelength X-ray diffraction: crystal structure of a basic 'blue' copper protein from cucumbers. Science 241, 806-811.
67. Yang W, Hendrickson WA, Crouch RJ, &, Satow Y, (1990) Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science 249, 1398-1405.
68. Hendrickson WA, Horton JR, &, LeMaster DM, (1990) Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three dimensional structure. EMBO J 9, 1665-1672.
69. Liu Q, Liu Q, &, Hendrickson WA, (2013) Robust structural analysis of native biological macromolecules from multi-crystal anomalous diffraction data. Acta Crystallogr D69, 1314-1332.
70. Sayre D, (1952) The squaring method: a new method for phase determination. Acta Crystallogr 5, 60-65.
71. Hauptman H, &, Karle J, (1953) Solution of the Phase Problem. ACA Monograph No. 3. Polycrystal Book Service, Pittsburgh, PA.
72. Germain G, &, Woolfson MM, (1971) The application of phase relationships to complex structures III. The optimum use of phase relationships. Acta Crystallogr A27, 368-376.
73. Sheldrick GM, (1990) Phase annealing in SHELX-90: direct methods for larger structures. Acta Crystallogr A46, 467-473.
74. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A64, 112-122.
75. Miller R, Gallo SM, Khalak HG, &, Weeks CM, (1994) SnB: crystal structure determination via Shake-and-Bake. J Appl Crystallogr 27, 613-621.
76. Hoppe W, (1957) Die 'Faltmolekülmethode'-eine neue Methode zur Bestimmung der Kristallstruktur bei ganz oder teilweise bekannter Molekülstruktur. Acta Crystallogr 10, 750-751.
77. Rossmann MG, &, Blow DM, (1962) The detection of sub-units within the crystallographic asymmetric unit. Acta Crystallogr 15, 24-31.
78. Rossmann MG, &, Blow DM, (1963) Determination of phases by the conditions of non-crystallographic symmetry. Acta Crystalogr 16, 39-45.
79. Rossmann MG, (1972) The Molecular Replacement Method, a Collection of Papers on the Use of Non-crystallographic Symmetry. Gordon & Breach, NY.
80. DiMaio F, Terwilliger TC, Read RJ, Wlodawer A, Oberdorfer G, Wagner U, Valkov E, Alon A, Fass D, Axelrod HL, et al,. (2011) Improved molecular replacement by density and energy guided protein structure optimization. Nature 473, 540-543.
81. Diamond R, &, Levitt M, (1971) A refinement of the structure of lysozyme. Biochem J 125, 92P.
82. Diamond R, (1971) A real-space refinement procedure for proteins. Acta Crystallogr A27, 436-452.
83. Watenpaugh KD, Sieker LC, Herriott JR, &, Jensen LH, (1972) The structure of a non-heme iron protein: rubredoxin at 1.5 Angstrom resolution. Cold Spring Harb Symp Quant Biol 36, 359-367.
84. Watenpaugh KD, Sieker LC, Herriott JR, &, Jensen LH, (1973) Refinement of the model of a protein: rubredoxin at 1.5 Å resolution. Acta Crystallogr B29, 943-956.
85. Sussman J, Holbrook SR, Church GM, &, Kim S-H, (1977) A structure factor least squares refinement procedure for macromolecular structures using constrained and restrained parameters. Acta Crystallogr A33, 800-804.
86. Konnert JH, &, Hendrickson WA, (1980) A restrained-parameter thermal-factor refinement procedure. Acta Crystallogr A36, 344-350.
87. Murshudov GN, Vagin AA, &, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D53, 240-255.
88. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, &, Adams PD, (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D68, 352-367.
89. de la Fortelle E, &, Bricogne G, (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol 276, 472-494.
90. Richards FM, (1985) Optical matching of physical models and electron density maps: early developments. Methods Enzymol 115, 145-154.
91. Jones TA, (1978) A graphics model building and refinement system for macromolecules. J Appl Crystallogr 11, 268-272.
92. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D60, 2126-2132.
93. Kalisman N, Schroder GF, &, Levitt M, (2013) The crystal structures of the eukaryotic chaperonin CCT reveal its functional partitioning. Structure 21, 540-549.
94. Dauter Z, Wlodawer A, Minor W, &, Jaskolski M, (2014) Avoidable errors in deposited macromolecular structures-an impediment to efficient data mining. IUCrJ in press.
95. Blake CC, Fenn RH, North AC, Phillips DC, &, Poljak RJ, (1962) Structure of lysozyme. A Fourier map of the electron density at 6 Å resolution obtained by X-ray diffraction. Nature 196, 1173-1176.
96. Blake CC, Koenig DF, Mair GA, North AC, Phillips DC, &, Sarma VR, (1965) Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Å resolution. Nature 206, 757-761.
97. Johnson LN, &, Phillips DC, (1965) Structure of some crystalline lysozyme-inhibitor complexes determined by X-ray analysis at 6 Å resolution. Nature 206, 761-763.
98. Matthews BW, Sigler PB, Henderson R, &, Blow DM, (1967) Three-dimensional structure of tosyl-alpha-chymotrypsin. Nature 214, 652-656.
99. Blow DM, (1976) Structure and mechanism of chemotrypsin. Acc Chem Res 9, 145-152.
100. Avey HP, Boles MO, Carlisle CH, Evans SA, Morris SJ, Palmer RA, Woolhouse BA, &, Shall S, (1967) Structure of ribonuclease. Nature 213, 557-562.
101. Wyckoff HW, Hardman KD, Allewell NM, Inagami T, Johnson LN, &, Richards FM, (1967) The structure of ribonuclease-S at 3.5 Å resolution. J Biol Chem 242, 3984-3988.
102. Fridborg K, Kannan KK, Liljas A, Lundin J, Strandberg B, Strandberg R, Tilander B, &, Wiren G, (1967) Crystal structure of human erythrocyte carbonic anhydrase C. 3. Molecular structure of the enzyme and of one enzyme-inhibitor complex at 5-5 Å resolution. J Mol Biol 25, 505-516.
103. Wright CS, Alden RA, &, Kraut J, (1969) Structure of subtilisin BPN' at 2.5 Å resolution. Nature 221, 235-242.
104. Drenth J, Hol WG, Jansonius JN, &, Koekoek R, (1972) Subtilisin Novo. The three-dimensional structure and its comparison with subtilisin BPN'. Eur J Biochem 26, 177-181.
105. Drenth J, Jansonius JN, Koekoek R, Swen HM, &, Wolthers BG, (1968) Structure of papain. Nature 218, 929-932.
106. Huber R, Kukla D, Ruhlmann A, Epp O, &, Formanek H, (1970) The basic trypsin inhibitor of bovine pancreas. I. Structure analysis and conformation of the polypeptide chain. Naturwissenschaften 57, 389-392.
107. Wlodawer A, Walter J, Huber R, &, Sjolin L, (1984) Structure of bovine pancreatic trypsin inhibitor. Results of joint neutron and X-ray refinement of crystal form II. J Mol Biol 180, 301-329.
108. Adams MJ, Ford GC, Koekoek R, Lentz PJ, McPherson A Jr, Rossmann MG, Smiley IE, Schevitz RW, &, Wonacott AJ, (1970) Structure of lactate dehydrogenase at 2.8 Å resolution. Nature 227, 1098-1103.
109. Hill E, Tsernoglou D, Webb L, &, Banaszak LJ, (1972) Polypeptide conformation of cytoplasmic malate dehydrogenase from an electron density map at 3.0 Å resolution. J Mol Biol 72, 577-589.
110. Branden CI, Eklund H, Nordstrom B, Boiwe T, Soderlund G, Zeppezauer E, Ohlsson I, &, Akeson A, (1973) Structure of liver alcohol dehydrogenase at 2.9 Å resolution. Proc Natl Acad Sci USA 70, 2439-2442.
111. Johnson LN, Madsen NB, Mosley J, &, Wilson KS, (1974) The crystal structure of phosphorylase beta at 6 Å resolution. J Mol Biol 90, 703-717.
112. Weber IT, Johnson LN, Wilson KS, Yeates DG, Wild DL, &, Jenkins JA, (1978) Crystallographic studies on the activity of glycogen phosphorylase b. Nature 274, 433-437.
113. Fletterick RJ, Sygusch J, Semple H, &, Madsen NB, (1976) Structure of glycogen phosphorylase a at 3.0 Å resolution and its ligand binding sites at 6 Å. J Biol Chem 251, 6142-6146.
114. Fletterick RJ, Sygusch J, Murray N, &, Madsen NB, (1976) Low-resolution structure of the glycogen phosphorylase a monomer and comparison with phosphorylase b. J Mol Biol 103, 1-13.
115. Protein Data Bank (1971) Crystallography: Protein Data Bank. Nat New Biol 233, 223.
116. Protein Data Bank (1973) Protein Data Bank. Acta Crystallogr B29, 1746.
117. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, &, Bourne PE, (2000) The Protein Data Bank. Nucleic Acids Res 28, 235-242.
118. Klug A, (2004) The discovery of the DNA double helix. J Mol Biol 335, 3-26.
119. Franklin RE, &, Gosling RG, (1953) Molecular configuration in sodium thymonucleate. Nature 171, 740-741.
120. Cochran W, Crick FH, &, Vand V, (1952) The structure of synthetic polypeptides. I. The transform of atoms on a helix. Acta Crystallogr 5, 581-586.
121. Watson JD, &, Crick FH, (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737-738.
122. Wilkins MHF, Stokes AR, &, Wilson HR, (1953) Molecular structure of deoxypentose nucleic acids. Nature 171, 738-740.
123. Vischer E, &, Chargaff E, (1948) The composition of the pentose nucleic acids of yeast and pancreas. J Biol Chem 176, 715-734.
124. Wing R, Drew H, Takano T, Broka C, Tanaka S, Itakura K, &, Dickerson RE, (1980) Crystal structure analysis of a complete turn of B-DNA. Nature 287, 755-758.
125. Viswamitra MA, Kennard O, Jones PG, Sheldrick GM, Salisbury S, Favello L, &, Shakked Z, (1978) DNA double helical fragment at atomic resolution. Nature 273, 687-688.
126. Conner BN, Takano T, Tanaka S, Itakura K, &, Dickerson RE, (1982) The molecular structure of d(ICpCpGpG), a fragment of right-handed double helical A-DNA. Nature 295, 294-299.
127. Shakked Z, Rabinovich D, Cruse WB, Egert E, Kennard O, Sala G, Salisbury SA, &, Viswamitra MA, (1981) Crystalline A-DNA: the X-ray analysis of the fragment d(G-G-T-A-T-A-C-C). Proc R Soc Lond B Biol Sci 213, 479-487.
128. Wang AH, Quigley GJ, Kolpak FJ, Crawford JL, van Boom JH, van der MG, &, Rich A, (1979) Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282, 680-686.
129. Drew HR, &, Dickerson RE, (1981) Conformation and dynamics in a Z-DNA tetramer. J Mol Biol 152, 723-736.
130. Drew HR, Dickerson RE, &, Itakura K, (1978) A salt-induced conformational change in crystals of the synthetic DNA tetramer d(CpGpCpG). J Mol Biol 125, 535-543.
131. Brzezinski K, Brzuszkiewicz A, Dauter M, Kubicki M, Jaskolski M, &, Dauter Z, (2011) High regularity of Z-DNA revealed by ultra high-resolution crystal structure at 0.55 Å. Nucleic Acids Res 39, 6238-6248.
132. Seeman NC, Rosenberg JM, Suddath FL, Kim JJ, &, Rich A, (1976) RNA double-helical fragments at atomic resolution. I. The crystal and molecular structure of sodium adenylyl-3,5-uridine hexahydrate. J Mol Biol 104, 109-144.
133. Rosenberg JM, Seeman NC, Day RO, &, Rich A, (1976) RNA double-helical fragments at atomic resolution. II. The crystal structure of sodium guanylyl-3,5-cytidine nonahydrate. J Mol Biol 104, 145-167.
134. 2. J Mol Biol 209, 459-474.
135. Ichikawa T, &, Sundaralingam M, (1972) X-ray diffraction study of a new crystal form of yeast phenylalanine tRNA. Nat New Biol 236, 174-175.
136. Stout CD, Mizuno H, Rubin J, Brennan T, Rao ST, &, Sundaralingam M, (1976) Atomic coordinates and molecular conformation of yeast phenylalanyl tRNA. An independent investigation. Nucleic Acids Res 3, 1111-1123.
137. Kim SH, Quigley GJ, Suddath FL, McPherson A, Sneden D, Kim JJ, Weinzierl J, &, Rich A, (1973) Three-dimensional structure of yeast phenylalanine transfer RNA: folding of the polynucleotide chain. Science 179, 285-288.
138. Suddath FL, Quigley GJ, McPherson A, Sneden D, Kim JJ, Kim SH, &, Rich A, (1974) Three-dimensional structure of yeast phenylalanine transfer RNA at 3.0 Å resolution. Nature 248, 20-24.
139. Quigley GJ, Suddath FL, McPherson A, Kim JJ, Sneden D, &, Rich A, (1974) The molecular structure of yeast phenylalanine transfer RNA in monoclinic crystals. Proc Natl Acad Sci USA 71, 2146-2150.
140. Robertus JD, Ladner JE, Finch JT, Rhodes D, Brown RS, Clark BF, &, Klug A, (1974) Structure of yeast phenylalanine tRNA at 3 Å resolution. Nature 250, 546-551.
141. Sussman JL, &, Kim SH, (1976) Idealized atomic coordinates of yeast phenylalanine transfer RNA. Biochem Biophys Res Commun 68, 89-96.
142. Pley HW, Flaherty KM, &, McKay DB, (1994) Three-dimensional structure of a hammerhead ribozyme. Nature 372, 68-74.
143. Scott WG, Finch JT, &, Klug A, (1995) The crystal structure of an all-RNA hammerhead ribozyme: a proposed mechanism for RNA catalytic cleavage. Cell 81, 991-1002.
144. Bawden FC, &, Pirie NW, (1937) The isolation and some properties of liquid crystalline substances from solanaceous plants infected with three strains of tobacco mosaic virus. Proc R Soc Lond B 123, 274-320.
145. Bernal JD, &, Fankuchen I, (1941) X-ray and crystallographic studies of plant virus preparations: I. Introduction and preparation of specimens. II. Modes of aggregation of the virus particles. J Gen Physiol 25, 111-146.
146. Bloomer AC, Champness JN, Bricogne G, Staden R, &, Klug A, (1978) Protein disk of tobacco mosaic virus at 2.8 Å resolution showing the interactions within and between subunits. Nature 276, 362-368.
147. Stubbs G, Warren S, &, Holmes K, (1977) Structure of RNA and RNA binding site in tobacco mosaic virus from 4 Å map calculated from X-ray fibre diagrams. Nature 267, 216-221.
148. Harrison SC, Olson AJ, Schutt CE, Winkler FK, &, Bricogne G, (1978) Tomato bushy stunt virus at 2.9 Å resolution. Nature 276, 368-373.
149. Abad-Zapatero C, Abdel-Meguid SS, Johnson JE, Leslie AG, Rayment I, Rossmann MG, Suck D, &, Tsukihara T, (1980) Structure of southern bean mosaic virus at 2.8 Å resolution. Nature 286, 33-39.
150. Rossmann MG, Arnold E, Erickson JW, Frankenberger EA, Griffith JP, Hecht HJ, Johnson JE, Kamer G, Luo M, Mosser AG, et al,. (1985) Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145-153.
151. Jones TA, &, Liljas L, (1984) Structure of satellite tobacco necrosis virus after crystallographic refinement at 2.5 Å resolution. J Mol Biol 177, 735-767.
152. Hogle JM, Chow M, &, Filman DJ, (1985) Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229, 1358-1365.
153. Acharya R, Fry E, Stuart D, Fox G, Rowlands D, &, Brown F, (1989) The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. Nature 337, 709-716.
154. Caspar DL, &, Klug A, (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27, 1-24.
155. Michel H, &, Oesterhelt D, (1980) Three-dimensional crystals of membrane proteins: bacteriorhodopsin. Proc Natl Acad Sci USA 77, 1283-1285.
156. Michel H, (1982) Three-dimensional crystals of a membrane protein complex. The photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 158, 567-572.
157. Deisenhofer J, Epp O, Miki K, Huber R, &, Michel H, (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180, 385-398.
158. Deisenhofer J, Epp O, Miki K, Huber R, &, Michel H, (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618-624.
159. Deisenhofer J, Epp O, Sinning I, &, Michel H, (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246, 429-457.
160. 1-ATPase from bovine heart mitochondria. Nature 370, 621.
161. Stock D, Leslie AG, &, Walker JE, (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700-1705.
162. + conduction and selectivity. Science 280, 69-77.
163. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, &, MacKinnon R, (2002) Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417, 515-522.
164. + channel. Nature 423, 33-41.
165. Ho JD, Yeh R, Sandstrom A, Chorny I, Harries WE, Robbins RA, Miercke LJ, &, Stroud RM, (2009) Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance. Proc Natl Acad Sci USA 106, 7437-7442.
166. Darst SA, Kubalek EW, &, Kornberg RD, (1989) Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electron crystallography. Nature 340, 730-732.
167. Darst SA, Edwards AM, Kubalek EW, &, Kornberg RD, (1991) Three-dimensional structure of yeast RNA polymerase II at 16 Å resolution. Cell 66, 121-128.
168. Cramer P, Bushnell DA, &, Kornberg RD, (2001) Structural basis of transcription: RNA polymerase II at 2.8 Å resolution. Science 292, 1863-1876.
169. Barbieri M, Pettazzoni P, Bersani F, &, Maraldi NM, (1970) Isolation of ribosome microcrystals. J Mol Biol 54, 121-124.
170. Wittmann HG, Mussig J, Piefke J, Gewitz HS, Rheinberger HJ, &, Yonath A, (1982) Crystallization of Escherichia coli ribosomes. FEBS Lett 146, 217-220.
171. Yonath A, Tesche B, Lorenz S, Mussig J, Erdmann VA, &, Wittmann HG, (1983) Several crystal forms of the Bacillus stearothermophilus 50 S ribosomal particles. FEBS Lett 154, 15-20.
172. Hope H, Frolow F, von Bohlen K, Makowski I, Kratky C, Halfon Y, Danz H, Webster P, Bartels KS, &, Wittmann HG, (1989) Cryocrystallography of ribosomal particles. Acta Crystallogr B45, 190-199.
173. Makowski I, Frolow F, Saper MA, Shoham M, Wittmann HG, &, Yonath A, (1987) Single crystals of large ribosomal particles from Halobacterium marismortui diffract to 6 Å. J Mol Biol 193, 819-822.
174. Ban N, Nissen P, Hansen J, Moore PB, &, Steitz TA, (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905-920.
175. Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, &, Ramakrishnan V, (2000) Structure of the 30S ribosomal subunit. Nature 407, 327-339.
176. Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, Bashan A, Bartels H, Agmon I, Franceschi F, et al,. (2000) Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102, 615-623.
177. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, &, Noller HF, (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science 292, 883-896.
178. Borovinskaya MA, Pai RD, Zhang W, Schuwirth BS, Holton JM, Hirokawa G, Kaji H, Kaji A, &, Cate JH, (2007) Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat Struct Mol Biol 14, 727-732.
179. Selmer M, Dunham CM, Murphy FV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, &, Ramakrishnan V, (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935-1942.
180. Ben-Shem A, de Garreau LN, Melnikov S, Jenner L, Yusupova G, &, Yusupov M, (2011) The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334, 1524-1529.
181. 2 adrenergic G-protein-coupled receptor. Nature 450, 383-387.
182. 2 adrenergic receptor function. Science 318, 1266-1273.
183. 2 adrenergic G protein-coupled receptor. Science 318, 1258-1265.
184. 2 adrenoceptor. Nature 469, 175-180.
185. 2 adrenergic receptor-Gs protein complex. Nature 477, 549-555.
186. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong T, Teller DC, Okada T, Stenkamp RE, et al,. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739-745.
187. Perutz MF, Rosa J, &, Schechter A, (1978) Therapeutic agents for sickle cell disease. Nature 275, 369-370.
188. Beddell CR, Goodford PJ, Norrington FE, Wilkinson S, &, Wootton R, (1976) Compounds designed to fit a site of known structure in human haemoglobin. Br J Pharmacol 57, 201-209.
189. Pullen RA, Lindsay DG, Wood SP, Tickle IJ, Blundell TL, Wollmer A, Krail G, Brandenburg D, Zahn H, Gliemann J, et al,. (1976) Receptor-binding region of insulin. Nature 259, 369-373.
190. Abelson J, (2009) From molecular biology to geology: a surprising trajectory. J Biol Chem 284, 35997-36006.
191. Goodford PJ, (1985) A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J Med Chem 28, 849-857.
192. Kuntz ID, Blaney JM, Oatley SJ, Langridge R, &, Ferrin TE, (1982) A geometric approach to macromolecule-ligand interactions. J Mol Biol 161, 269-288.
193. Ondetti MA, Rubin B, &, Cushman DW, (1977) Design of specific inhibitors of angiotensin-converting enzyme: new class of orally active antihypertensive agents. Science 196, 441-444.
194. Blundell T, Sibanda BL, &, Pearl L, (1983) Three-dimensional structure, specificity and catalytic mechanism of renin. Nature 304, 273-275.
195. Wlodawer A, Miller M, Jaskõlski M, Sathyanarayana BK, Baldwin E, Weber IT, Selk LM, Clawson L, Schneider J, &, Kent SBH, (1989) Conserved folding in retroviral proteases: crystal structure of a synthetic HIV-1 protease. Science 245, 616-621.
196. Miller M, Schneider J, Sathyanarayana BK, Toth MV, Marshall GR, Clawson L, Selk L, Kent SBH, &, Wlodawer A, (1989) Structure of complex of synthetic HIV-1 protease with a substrate-based inhibitor at 2.3 Å resolution. Science 246, 1149-1152.
197. Wlodawer A, &, Erickson JW, (1993) Structure-based inhibitors of HIV-1 protease. Annu Rev Biochem 62, 543-585.
198. Miller M, Jaskõlski M, Rao JKM, Leis J, &, Wlodawer A, (1989) Crystal structure of a retroviral protease proves relationship to aspartic protease family. Nature 337, 576-579.
199. Weber IT, Miller M, Jaskõlski M, Leis J, Skalka AM, &, Wlodawer A, (1989) Molecular modeling of the HIV-1 protease and its substrate binding site. Science 243, 928-931.
200. Tickle IJ, Sibanda BL, Pearl LH, Hemmings AM, &, Blundell TL, (1984) Protein crystallography, interactive computer graphics, and drug design. In X-ray Crystallography and Drug Action (, Hirn AS, ed.), pp. 427-440. Clarendon Press, Oxford, UK.
201. Navia MA, &, Murcko MA, (1992) Use of structural information in drug design. Curr Opin Struct Biol 2, 202-210.
202. Colman PM, (1994) Structure-based drug design. Curr Opin Struct Biol 4, 868-874.
203. Gaasterland T, (1998) Structural genomics taking shape. Trends Genet 14, 135.
204. Terwilliger TC, Waldo G, Peat TS, Newman JM, Chu K, &, Berendzen J, (1998) Class-directed structure determination: foundation for a protein structure initiative. Protein Sci 7, 1851-1856.
205. Kim SH, (1998) Shining a light on structural genomics. Nat Struct Biol 5, 643-645.
206. Burley SK, Almo SC, Bonanno JB, Capel M, Chance MR, Gaasterland T, Lin D, Sali A, Studier FW, &, Swaminathan S, (1999) Structural genomics: beyond the human genome project. Nat Genet 23, 151-157.
207. Montelione GT, &, Anderson S, (1999) Structural genomics: keystone for a Human Proteome Project. Nat Struct Biol 6, 11-12.
208. Heinemann U, Frevert J, Hofmann K, Illing G, Maurer C, Oschkinat H, &, Saenger W, (2000) An integrated approach to structural genomics. Prog Biophys Mol Biol 73, 347-362.
209. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al,. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
210. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, et al,. (2001) The sequence of the human genome. Science 291, 1304-1351.
211. Boutet S, Lomb L, Williams GJ, Barends TR, Aquila A, Doak RB, Weierstall U, DePonte DP, Steinbrener J, Shoeman RL, et al,. (2012) High-resolution protein structure determination by serial femtosecond crystallography. Science 337, 362-364.
212. Redecke L, Nass K, DePonte DP, White TA, Rehders D, Barty A, Stellato F, Liang M, Barends TR, Boutet S, et al,. (2013) Natively inhibited Trypanosoma brucei cathepsin B structure determined by using an X-ray laser. Science 339, 227-230.
213. Neutze R, Wouts R, van der SD, Weckert E, &, Hajdu J, (2000) Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406, 752-757.
214. Bergh M, Huldt G, Timneanu N, Maia FR, &, Hajdu J, (2008) Feasibility of imaging living cells at subnanometer resolutions by ultrafast X-ray diffraction. Q Rev Biophys 41, 181-204.
215. Sayre D, (2008) Report on a project on three-dimensional imaging of the biological cell by single-particle X-ray diffraction. Acta Crystallogr A64, 33-35.