Crystallization of soluble proteins in vapor diffusion for x-ray crystallography

Nature Protocols

Volumn 2, Issue 7, 2007, Pages 1633-1651

  Benvenuti, Manuela ^a   Mangani, Stefano ^a,b  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ARTICLE; CHEMISTRY; CRYSTALLIZATION; DIFFUSION; ISOLATION AND PURIFICATION; METHODOLOGY; PROTEIN DENATURATION; SOLUBILITY; X RAY CRYSTALLOGRAPHY;

CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIFFUSION; PROTEIN DENATURATION; PROTEINS; SOLUBILITY;

EID: 34548558727     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2007.198     Document Type: Article

References (121)

1. Berman, H., Henrick, K., Nakamura, H. and Markley, J.L. The worldwide Protein Data Bank (wwPDB): ensuring a single, uniform archive of PDB data. Nucleic Acids Res. 35, D301-D303 (2007).
2. Vainshtein, B.K.: Modern Crystallography I Symmetry of Crystals, Methods of Structural Crystallography (Springer-Verlag, Berlin, 1981).
3. Chayen, N.E.: Turning protein crystallisation from an art into a science. Curr. Opin. Struct. Biol. 14, 577-583 (2004).
4. McPherson, A. Introduction to protein crystallization. Methods 34, 254-265 (2004).
5. McPherson, A.: Crystallization of Biological Macromolecules (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1999).
6. Bergfors, T.M.: Protein Crystallization: Techniques, Strategies and Tips (International University Line, La Jolla, CA, 1999).
7. Ducruix, A. and Giege, R.: Crystallization of Nucleic Acids and Proteins, A Practical Approach. (IRL Press, Oxford, UK, NewYork, 1992).
8. Michel, H.: Crystallization of Membrane Proteins (CRC Press, Boca Raton, 1991).
9. Iwata, S.: Methods and Results in Crystallization of Membrane Proteins (IUL Biotechnology Series, La Jolla, CA, 2003).
10. Hunte, C., von Jagow, G. and Shagger, H.: Membrane Protein Purification and Crystallization: A Practical Guide (Academic Press, New York, 2002).
11. Caffrey, M.: Membrane protein crystallization. J. Struct. Biol. 142, 108-132 (2003).
12. Wiener, M.C.: A pedestrian guide to membrane protein crystallization. Methods 34, 364-372 (2004).
13. Lundstrom, K.: Structural genomics on membrane proteins: mini review. Comb. Chem. High Throughput Screen. 7, 431-439 (2004).
14. Asherie, N. Protein crystallization and phase diagrams. Methods 34, 266-272 (2004).
15. Chernov, A.A.: Crystal growth and crystallography. Acta Crystallogr. A 54, 859-872 (1998).
16. Chayen, N.E.: The role of oil in macromolecular crystallization. Structure 5, 1269-1274 (1997).
17. McPherson, A.: Protein crystallization in the structural genomics era. J. Struct. Funct. Genomics 5, 3-12 (2004).
18. Rupp, B. and Wang, J.: Predictive models for protein crystallization. Methods 34, 390-407 (2004).
19. Rupp, B.: High-throughput crystallography at an affordable cost: the TB structural genomics consortium crystallization facility. Acc. Chem. Res. 36, 173-181 (2003).
20. Sharff, A. and Jhoti, H.: High-throughput crystallography to enhance drug discovery. Curr. Opin. Chem. Biol. 7, 340-345 (2003).
21. Morissette, S.L.: High-throughput crystallization: polymorphs, salts, cocrystals and solvates ofpharmaceutical solids. Adv. Drug Deliv. Rev. 56, 275-300 (2004).
22. Stevens, R.C.: High-throughput protein crystallization. Curr. Opin. Struct. Biol. 10, 558-563 (2000).
23. Chayen, N.E.: Protein crystallization for genomics: throughput versus output. J. Struct. Funct. Genomics 4, 115-120 (2003).
24. Calderone, V.: The crystalstructure of yeast copper thione in: the solution of a long-lasting enigma. Proc. Natl. Acad. Sci. USA 102, 51-56 (2005).
25. Derewenda, Z.S. and Vekilov, P.G.: Entropy and surface engineering in protein crystallization. Acta Crystallogr. D Biol. Crystallogr. 62, 116-124 (2006).
26. Derewenda, Z.S.: The use of recombinant methods and molecular engineering in protein crystallization. Methods 34, 354-363 (2004).
27. Giege, R.: The role of purification in the crystallization of proteins and nucleic acids. J. Cryst. Growth 76, 554-561 (1986).
28. Zulauf, M. and D'Arcy, A.: Light scattering of proteins as a criterion for crystallization. J. Cryst. Growth 122, 102-106 (1992).
29. Thomas, B.R., Carter, D. and Rosenberger, F.: Effect of micro heterogeneity on horse spleen apoferritin crystallization. J. Cryst. Growth 187, 499-510 (1998).
30. Rosenberger, F.: Protein crystallization. J. Cryst. Growth 166, 40-54 (1996).
31. Pusey, M.L.: Life in the fast lane for protein crystallization and x-ray crystallography. Prog. Biophys. Mol. Biol. 88, 359-386 (2005).
32. Pikal-Cleland, K.A. and Carpenter, J.F.: Lyophilization-induced protein denaturation in phosphate buffer systems: monomeric and tetrameric beta-galactosidase. J. Pharm. Sci. 90, 1255-1268 (2001).
33. Carpenter, J.F., Chang, B.S., Garzon-Rodriguez, W. and Randolph, T.W.: Rational design of stable lyophilized protein formulations: theory and practice. Pharm. Biotechnol. 13, 109-133 (2002).
34. McPherson, A., Malkin, A.J., Kuznetsov, Y.G. and Koszelak, S.: Incorporation of impurities into macromolecular crystals. J. Cryst. Growth 168, 74-92 (1996).
35. Saridakis, E. and Chayen, N.E.: Systematic improvement of protein crystals by determining the supersolubility curves of phase diagrams. Biophys. J. 84, 1218-1222 (2003).
36. Saridakis, E. and Chayen, N.E.: Improving protein crystal quality by decoupling nucleation and growth in vapor diffusion. Protein Sci. 9, 755-757 (2000).
37. Nneji, G.A. and Chayen, N.E.: A crystallization plate for controlling evaporation in hanging drops. J. Appl. Crystallogr. 37, 502-503 (2004).
38. Chayen, N.E.: Methods for separating nucleation and growth in protein crystallisation. Prog. Biophys. Mol. Biol. 88, 329-337 (2005).
39. Talreja, S., Kim, D.Y., Mirarefi, A.Y., Zukoski, C.F. and Kenis, P.J.A.: Screening and optimization of protein crystallization conditions through gradual evaporation using a novel crystallization platform. J. Appl. Crystallogr. 38, 988-995 (2005).
40. D'Arcy, A., Sweeney, A.M. and Haber, A.: Practical aspects of using the microbatch method in screening conditions for protein crystallization. Methods 34, 323-328 (2004).
41. Landsberg, M.J., Bond, J., Gee, C.L., Martin, J.L. and Hankamer, B.: A method for screening the temperature dependence of three-dimensional crystal formation. Acta Crystallogr. D Biol. Crystallogr. 62, 559-562 (2006).
42. Przybylska, M. A double cell for controlling nucleation and growth of protein crystals. J. Appl. Crystallogr. 22, 115-118 (1989).
43. Saridakis, E.E., Stewart, P.D., Lloyd, L.F. and Blow, D.M.: Phase diagram and dilution experiments in the crystallization of car boxy peptidase G2. Acta Crystallogr. D Biol. Crystallogr. 50,293-297 (1994).
44. Stura, E.A. and Wilson, I.A.: Analytical and production seeding techniques. Methods 1, 38-49 (1990).
45. Bergfors, T.: Seeds to crystals. J. Struct. Biol. 142, 66-76 (2003).
46. Thaller, C.: Repeated seeding technique for growing large single crystals of proteins. J. Mol. Biol. 147, 465-469 (1981).
47. Stura, E.A. and Wilson, I.A.: Applications ofthe streak seeding technique in protein crystallization. J. Cryst. Growth 110, 270-282 (1991).
48. Chayen, N.E., Saridakis, E. andSear, R.P.: Experimentand theory for heterogeneous nucleation of protein crystals in a porous medium. Proc. Natl. Acad. Sci. USA 103, 597-601 (2006).
49. Chayen, N.E., Saridakis, E., El Bahar, R. and Nemirovsky, Y.: Porous silicon: an effective nucleation-inducing material for protein crystallization. J. Mol. Biol. 312, 591-595 (2001).
50. Fermani, S., Falini, G., Minnucci, M. and Ripamonti, A.: Protein crystallization on polymeric film surfaces. J. Cryst. Growth 224, 327-334 (2001).
51. Pechkova, E. and Nicolini, C.: Accelerated protein crystal growth by protein thin film template. J. Cryst. Growth 231, 599-602 (2001).
52. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
53. Spangler, B.D. and Westbrook, E.M.: Isolation of isoelectrically pure cholera toxin for crystallization. J. Cryst. Growth 110, 220-227 (1991).
54. Wilson, W.W.: Light scattering as a diagnostic for protein crystal growth—a practical approach. J. Struct. Biol. 142, 56-65 (2003).
55. Skouri, M., Delsanti, M., Munch, J.P., Lorber, B. and Giege, R.: Dynamic light scattering studies of the aggregation of lysozyme under crystallization conditions. FEBS Lett. 295, 84-88 (1991).
56. Mogridge, J.: Using light scattering to determine the stoichiometry of protein complexes. Methods Mol. Biol. 261,113-118 (2004).
57. Georgalis, Y. and Saenger, W.: Light scattering studies on supersaturated protein solutions. Sci. Prog. 82, 271-294 (1999).
58. Geerlof, A.: The impact of protein characterization in structural proteomics. Acta Crystallogr. D Biol. Crystallogr. 62, 1125-1136 (2006).
59. Ferre-D'Amare, A.R. and Burley, S.K.: Use of dynamic light scattering to assess crystallizability of macromolecules and macromolecular assemblies. Structure 2, 357-359 (1994).
60. Chayen, N.E.: Trends and challenges in experimental macromolecular crystallography. Q. Rev. Biophys. 29, 227-278 (1996).
61. Banci, L.: A prokaryotic superoxide dismutase paralog lacking two Cu ligands: from largely unstructured in solution to ordered in the crystal. Proc. Natl. Acad. Sci. USA 102, 7541-7546 (2005).
62. Banci, L.: Fully metallated S134N Cu, Zn-superoxide dismutase displays abnormal mobility and intermolecular contacts in solution. J. Biol. Chem. 280, 35815-35821 (2005).
63. Liou, Y.C.: Folding and structural characterization of highly disulfide-bonded beetle antifreeze protein produced in bacteria. Protein Expr. Purif. 19, 148-157 (2000).
64. Mao, H., Gunasekera, A.H. and Fesik, S.W.: Expression, refolding, and isotopic labeling of human serum albumin domains for NMR spectroscopy. Protein Expr. Purif. 20, 492-499 (2000).
65. Jancarik, J., Pufan, R., Hong, C., Kim, S.H. and Kim, R.: Optimum solubility (OS) screening: an efficient method to optimize buffer conditions for homogeneity and crystallization of proteins. Acta Crystallogr. D Biol. Crystallogr. 60, 1670-1673 (2004).
66. Liljas, A.: Crystal structure of human carbonic anhydrase C. Nat. New Biol. 235, 131-137 (1972).
67. Arnesano, F.: The evolutionarily conserved trimeric structure of CutA1 proteins suggests a role in signal transduction. J. Biol. Chem. 278, 45999-46006 (2003).
68. Lepre, C.A. and Moore, J.M.: Microdrop screening: a rapid method to optimize solvent conditions for NMR spectroscopy of proteins. J. Biomol. NMR 12, 493-499 (1998).
69. Izaac, A., Schall, C.A. and Mueser, T.C.: Assessment of a preliminary solubility screen to improve crystallization trials: uncoupling crystal condition searches. Acta Crystallogr. D Biol. Crystallogr. 62, 833-842 (2006).
70. Collins, B.K., Tomanicek, S.J., Lyamicheva, N., Kaiser, M.W. and Mueser, T.C.: A preliminary solubility screen used to improve crystallization trials: crystallization and preliminary x-ray structure determination of Aeropyrum pernix flap endonuclease-1. Acta Crystallogr. D. Biol. Crystallogr. 60, 1674-1678 (2004).
71. Sazaki, G., Kurihara, K., Nakada, T., Miyashita, S. and Komatsu, H.: A novel approach to the solubility measurement of protein crystals by two-beam interferometry. J. Cryst. Growth 169, 355-360 (1996).
72. Nakazato, K., Homma, T. and Tomo, T.: Rapid solubility measurement of protein crystals as a function of precipitant concentration with micro-dialysis cell and two-beam interferometer. J. Synchrotron Rad. 11, 34-37 (2004).
73. Jancarik, J. and Kim, S.H.: Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr. 24, 409-411 (1991).
74. Cudney, R., Patel, S., Weisgraber, K., Newhouse, Y. and McPherson, A.: Screening and optimization strategies for macromolecular crystal growth. Acta Crystallogr. D. Biol. Crystallogr. 50, 414-423 (1994).
75. Tran, T.T., Sorel, I. and Lewit-Bentley, A.: Statistical experimental design of protein crystallization screening revisited. Acta Crystallogr. D Biol. Crystallogr. 60, 1562-1568 (2004).
76. Boistelle, R. and Astier, J.P.: Crystallization mechanism in solution. J. Cryst. Growth 90, 14-30 (1988).
77. Ng, J.D.: The crystallization of biological macromolecules from precipitates: evidence for Ostwald ripening. J. Cryst. Growth 168, 50-62 (1996).
78. Vedadi, M.: Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination. Proc. Natl. Acad. Sci. USA 103, 15835-15840 (2006).
79. McPherson, A.: The effects of neutral detergents on the crystallization of soluble proteins. J. Cryst. Growth 76, 547-553 (1986).
80. Hayes, M.E.: Assembly of nucleic acid-lipid nanoparticles from aqueous-organic monophases. Biochim. Biophys. Acta 1758, 429-442 (2006).
81. Guan, R.J., Wang, M., Liu, X.Q. and Wang, D.C.: Optimization of soluble protein crystallization with detergents. J. Cryst. Growth 231, 273-279 (2001).
82. Shulgin, I.L. and Ruckenstein, E.: Relationship between preferential interaction of a protein in an aqueous mixed solvent and its solubility. Biophys. Chem. 118, 128-134 (2005).
83. Tarentino, A.L., Gomez, C.M. and Plummer, T.H.: Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase. Biochemistry 24, 4665-4671 (1985).
84. Grueninger-Leitch, F., D'Arcy, A., D'Arcy, B. and Chene, C.: Deglycosylation of proteins for crystallization using recombinant fusion protein glycosidases. Protein Sci. 5, 2617-2622 (1996).
85. Prota, A.E., Sage, D.R., Stehle, T. and Fingeroth, J.D.: The crystal structure of human CD21: Implications for Epstein-Barr virus and C3d binding. Proc. Natl. Acad. Sci. USA 99, 10641-10646 (2002).
86. Carafoli, F., Chirgadze, D.Y., Blundell, T.L. and Gherardi, E.: Crystal structure ofthe beta-chain of human hepatocyte growth factor-like/macrophage stimulating protein. FEBS J. 272, 5799-5807 (2005).
87. Nasreen, A., Vogt, M., Kim, H.J., Eichinger, A. and Skerra, A.: Solubility engineering and crystallization of human apolipoprotein D. Protein Sci. 15, 190-199 (2006).
88. Roe, S.: Protein Purification Applications: a Practical Approach (Oxford University Press, Oxford, UK, New York, 2001).
89. Liu, J.-W., Boucher, Y., Stokes, H.W. and Ollis, D.L.: Improving protein solubility: the use of the Escherichia coli dihydrofolate reductase gene as a fusion reporter. Protein Expr. Purif. 47, 258-263 (2006).
90. Chernov, A.A.: Protein crystals and their growth. J. Struct. Biol. 142, 3-21 (2003).
91. Chayen, N.E.: Comparative studies of protein crystallization by vapour-diffusion and microbatch techniques. Acta Crystallogr. D. Biol. Crystallogr. 54, 8-15 (1998).
92. McPherson, A. Jr.: The growth and preliminary investigation of protein and nucleic acid crystals for x-ray diffraction analysis. Methods Biochem. Anal. 23, 249-345 (1976).
93. Cudney, R., Patel, S. and McPherson, A.: Crystallization of macromolecules in silica gels. Acta Crystallogr. D. Biol. Crystallogr. 50, 479-483 (1994).
94. Garcia-Ruiz, J.M.: Counterdiffusion methods for macromolecular crystallization. Methods Enzymol. 368, 130-154 (2003).
95. Garcia-Ruiz, J.M., Gonzalez-Ramirez, L.A., Gavira, J.A. and Otalora, F.: Granada crystallisation box: a new device for protein crystallisation by counter-diffusion techniques. Acta Crystallogr. D. Biol. Crystallogr. 58, 1638-1642 (2002).
96. Papanikolau, Y.: Ionic strength reducers: an efficient approach to protein purification and crystallization. Application to two Rop variants. Acta Crystallogr. D Biol. Crystallogr. 60, 1334-1337 (2004).
97. Anand, K., Pal, D. and Hilgenfeld, R.: An overview on 2-methyl-2,4-pentanediol in crystallization and in crystals of biological macromolecules. Acta Crystallogr. D Biol. Crystallogr. 58, 1722-1728 (2002).
98. Berger, B.W., Blamey, C.J., Naik, U.P., Bahnson, B.J. and Lenhoff, A.M.: Roles of additives and precipitants in crystallization of calcium- and integrin-binding protein. Cryst. Growth Des. 5, 1499-1507 (2005).
99. Wiencek, J.M.: New strategies for protein crystal growth. Annu. Rev. Biomed. Eng I,505-534(1999).
100. Forsythe, E.L., Maxwell, D.L. and Pusey, M.: Vapor diffusion, nucleation rates and the reservoir to crystallization volume ratio. Acta Crystallogr. D Biol. Crystallogr. 58, 1601-1605 (2002).
101. Walter, T.S.: A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D Biol. Crystallogr. 61,651-657 (2005).
102. Wolfova, J., Grandori, L., Chatterjee, N., Carey, J. and Smatanova, I.K.: Crystallization of the flavoprotein WrbA optimized by using additives and gels. J. Cryst. Growth 284, 502-505 (2005).
103. Moreno, A., Theobald-Dietrich, A., Lorber, B., Sauter, C. and Giege, R.: Effects of macromolecular impurities and of crystallization method on the quality of eubacterial aspartyl-tRNA synthetase crystals. Acta Crystallogr. D Biol. Crystallogr. 61,789-792 (2005).
104. Kinoshita, T., Ataka, M., Warizaya, M., Neya, M. and Fujii, T. Improving quality and harvest period of protein crystals forstructure-based drug design: effects ofa gel and a magnetic field on bovine adenosine deaminase crystals. Acta Crystallogr. D Biol. Crystallogr. 59,1333-1335 (2003).
105. Sica, F.: Elimination oftwinning in crystals of Sulfolobussolfataricus alcohol dehydrogenase holo-enzyme by growth in agarose gels. Acta Crystallogr. D Biol. Crystallogr. 50, 508-511 (1994).
106. McPherson, A. and Schlichta, P.: The use of heterogeneous and epitaxial nucleants to promote the growth of protein crystals. J. Cryst. Growth 90, 47-50 (1988).
107. Banci, L.: From an inactive prokaryotic SOD homologue to an active protein through site-directed mutagenesis. J. Am. Chem. Soc. 127, 13287-13292 (2005).
108. Prinz, R. and Weser, U.: A naturally occurring Cu-thionein in Saccharomyces cerevisiae. Hoppe Seylers. Z. Physiol Chem. 356, 767-776 (1975).
109. Luchinat, C.: The Cu(I)(7) cluster in yeast copper thionein survives major shortening of the polypeptide backbone as deduced from electronic absorption, circular dichroism, luminescence and (1)H NMR. J. Biol. Inorg. Chem. 8, 353-359 (2003).
110. Sousa, R.: Use of glycerol, polyols and other protein structure stabilizing agents in protein crystallization. Acta Crystallogr. D. Biol. Crystallogr. 51, 271-277 (1995).
111. Farnum, M. and Zukoski, C.: Effect of glycerol on the interactions and solubility of bovine pancreatic trypsin inhibitor. Biophys. J. 76, 2716-2726 (1999).
112. Charron, C., Kadri, A., Robert, M.C., Giege, R. and Lorber, B.: Crystallization in the presence of glycerol displaces water molecules in the structure of thaumatin. Acta Crystallogr. D. Biol. Crystallogr. 58, 2060-2065 (2002).
113. Trakhanov, S. and Quiocho, S.A.: Influence of divalent cations in protein crystallization. Protein Sci. 4, 1914-1919 (1995).
114. Carbonnaux, C., Ries-Kautt, M. and Ducruix, A.: Relative effectiveness of various anions on the solubility of acidic Hypoderma lineatum collagenase at pH 7.2. Protein Sci. 4, 2123-2128 (1995).
115. Vaney, M.C.: Structural effects of monovalent anions on polymorphic lysozyme crystals. Acta Crystallogr. D. Biol. Crystallogr. 57, 929-940 (2001).
116. Ries-Kautt, M.M. and Ducruix, A.F.: Relative effectiveness of various ions on the solubility and crystal growth of lysozyme. J. Biol. Chem. 264, 745-748 (1989).
117. Dauter, Z. and Dauter, M.: Entering a new phase. Using solvent halide ions in protein structure determination. Structure 9, R21-R26 (2001).
118. Dauter, Z., Dauter, M. and Rajashankar, K.R.: Novel approach to phasing proteins: derivatization by short cryo-soaking with halides. Acta Crystallogr. D. Biol. Crystallogr. 56, 232-237 (2000).
119. Dauter, Z.: New approaches to high-throughput phasing. Curr. Opin. Struct. Biol. 12, 674-678 (2002).
120. Lorber, B., Delucas, L.J. and Bishop, J.B.: Changes in the physico-chemical properties of the detergent octyl glucoside during membrane protein crystallization using salts as the precipitant. J. Cryst. Growth 110, 103-113 (1991).
121. Gebicka, L. and Gebicki, J.L.: Kinetic studies on the interaction of ferricytochrome c with anionic surfactants. J. Protein Chem. 18, 165-172 (1999).