Large-volume protein crystal growth for neutron macromolecular crystallography

Acta Crystallographica Section F: Structural Biology Communications

Volumn 71, Issue , 2015, Pages 358-370

  Ng, Joseph D ^a,b   Baird, James K ^c   Coates, Leighton ^d   Garcia Ruiz, Juan M ^e   Hodge, Teresa A ^c   Huang, Sijay ^c  

^a University of Alabama in Huntsville   (United States)

^b HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^c University of Alabama in Huntsville   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e CSIC   (Spain)

Author keywords

large volume crystals; neutron macromolecular crystallography

Indexed keywords

MACROMOLECULE; PROTEIN;

CHEMISTRY; CRYSTALLIZATION; CRYSTALLOGRAPHY; MACROMOLECULE; NEUTRON DIFFRACTION; PROCEDURES;

CRYSTALLIZATION; CRYSTALLOGRAPHY; MACROMOLECULAR SUBSTANCES; NEUTRON DIFFRACTION; PROTEINS;

EID: 84927642655     PISSN: None     EISSN: 2053230X     Source Type: Journal    
DOI: 10.1107/S2053230X15005348     Document Type: Article

References (82)

1. Anand, K., Pal, D., Hilgenfeld, R. (2002). An overview on 2-methyl-2, 4-pentanediol in crystallization and in crystals of biological macromolecules. Acta Cryst. D58, 1722-1728.
2. Asherie, N. (2004). Protein crystallization and phase diagrams. Methods, 34, 266-272.
3. Baird, J. K., Kim, Y. W. (2002). Theory of the nucleation of protein macromolecular ions. Mol. Phys. 100, 1855-1866.
4. Benvenuti, M., Mangani, S. (2007). Crystallization of soluble proteins in vapor diffusion for X-ray crystallography. Nature Protoc. 2, 1633-1651.
5. Bergfors, T. (2007). Screening and optimization methods for nonautomated crystallization laboratories. Methods Mol. Biol. 363, 131-151.
6. Blakeley, M. P., Kalb, A. J., Helliwell, J. R., Myles, D. A. (2004). The 15 K neutron structure of saccharide-free concanavalin A. Proc. Natl Acad. Sci. USA, 101, 16405-16410.
7. Blakeley, M. P., Langan, P., Niimura, N., Podjarny, A. (2008). Neutron crystallography: opportunities, challenges, and limitations. Curr. Opin. Struct. Biol. 18, 593-600.
8. Blakeley, M. P., Teixeira, S. C. M., Petit-Haertlein, I., Hazemann, I., Mitschler, A., Haertlein, M., Howard, E., Podjarny, A. D. (2010). Neutron macromolecular crystallography with LADI-III. Acta Cryst. D66, 1198-1205.
9. Borgstahl, G. E., Pokross, M., Chehab, R., Sekher, A., Snell, E. H. (2000). Cryo-trapping the six-coordinate, distorted-octahedral active site of manganese superoxide dismutase. J. Mol. Biol. 296, 951-959.
10. Budayova-Spano, M., Dauvergne, F., Audiffren, M., Bactivelane, T., Cusack, S. (2007). A methodology and an instrument for the temperature-controlled optimization of crystal growth. Acta Cryst. D63, 339-347.
11. Cacioppo, E., Pusey, M. L. (1991). The solubility of the tetragonal form of hen egg white lysozyme from pH 4.0 to 5.4. J. Cryst. Growth, 114, 286-292.
12. Carotenuto, L., Piccolo, C., Castagnolo, D., Lappa, M., Tortora, A., Garc?à-Ruiz, J. M. (2002). Experimental observations and numerical modelling of diffusion-driven crystallisation processes. Acta Cryst. D58, 1628-1632.
13. Casadei, C. M., Gumiero, A., Metcalfe, C. L., Murphy, E. J., Basran, J., Concilio, M. G., Teixeira, S. C. M., Schrader, T. E., Fielding, A. J., Ostermann, A., Blakeley, M. P., Raven, E. L., Moody, P. C. E. (2014). Neutron cryo-crystallography captures the protonation state of ferryl heme in a peroxidase. Science, 345, 193-197.
14. Chayen, N. E., Shaw Stewart, P. D., Maeder, D. L., Blow, D. M. (1990). An automated system for micro-batch protein crystallization and screening. J. Appl. Cryst. 23, 297-302.
15. Coates, L., Erskine, P. T., Wood, S. P., Myles, D. A. A., Cooper, J. B. (2001). A neutron Laue diffraction study of endothiapepsin: implications for the aspartic proteinase mechanism. Biochemistry, 40, 13149-13157.
16. Coates, L., Stoica, A. D., Hoffmann, C., Richards, J., Cooper, R. (2010). The macromolecular neutron diffractometer (MaNDi) at the Spallation Neutron Source, Oak Ridge: enhanced optics design, high-resolution neutron detectors and simulated diffraction. J. Appl. Cryst. 43, 570-577.
17. Coates, L., Tomanicek, S., Schrader, T. E., Weiss, K. L., Ng, J. D., Jü ttner, P., Ostermann, A. (2014). Cryogenic neutron protein crystallography: routine methods and potential benefits. J. Appl. Cryst. 47, 1431-1434.
18. Cudney, B., Patel, S. (1994). Crystallization as a tool for bioseparation. Am. Biotechnol. Lab. 12(7), 42.
19. Day, J., McPherson, A. (1992). Macromolecular crystal growth experiments on International Microgravity Laboratory-1. Protein Sci. 1, 1254-1268.
20. DeLucas, L. J., Moore, K. M., Long, M. M. (1999). Protein crystal growth and the International Space Station. Gravit. Space Biol. Bull. 12, 39-45.
21. Ducruix, A., Giegé, R. (1999). Crystallization of Nucleic Acids and Proteins: A Practical Approach. Oxford University Press.
22. Dunuwila, D. D., Berglund, K. A. (1997). ATR FTIR spectroscopy for in situ measurement of supersaturation. J. Cryst. Growth, 179, 185-193.
23. Ewing, F., Forsythe, E., Pusey, M. (1994). Orthorhombic lysozyme solubility. Acta Cryst. D50, 424-428.
24. Feigelson, R. S. (1988). The relevance of small molecule crystal growth theories and techniques to the growth of biological macromolecules. J. Cryst. Growth, 90, 1-13
25. Garc?á-Ruiz, J. M. (2003). Counterdiffusion methods for macromolecular crystallization. Methods Enzymol. 368, 130-154
26. Garc?á-Ruiz, J. M., Ng, J. D. (2006). Protein Crystallization Strategies for Structural Genomics, edited by N. E. Chayen, ch. 5. La Jolla: International University Line
27. Garcá-Ruiz J M. Otá lora F., 1997, Crystal growth studies in microgravity with the APCF II. Image analysis studies, J. Cryst. Growth, 182, 155-167
28. Garc?á-Ruiz, J. M., Otá lora, F., Novella, M. L., Gavira, J. A., Sauter, C., Vidal, O. (2001). A supersaturation wave of protein crystallization. J. Cryst. Growth, 232, 149-155.
29. Garman, E. F., Doublié, S. (2003). Cryocooling of macromolecular crystals: optimization methods. Methods Enzymol. 368, 188-216.
30. Garman, E. F., McSweeney, S. M. (2007). Progress in research into radiation damage in cryo-cooled macromolecular crystals. J. Synchrotron Rad. 14, 1-3.
31. Garman, E., Owen, R. L. (2007). Cryocrystallography of macromolecules: practice and optimization. Methods Mol. Biol. 364, 1-18.
32. Gavira, J. A., Toh, D., Lopé z-Jaramillo, J., Garc?á-Ruéz, J. M., Ng, J. D. (2002). Ab initio crystallographic structure determination of insulin from protein to electron density without crystal handling. Acta Cryst. D58, 1147-1154.
33. Gray, R. J., Hou, W. B., Kudryavtsev, A. B., DeLucas, L. J. (2001). A new approach to the measurement of protein solubility by Michaelson interferometry. J. Cryst. Growth, 232, 10-16.
34. Haire, L. F., Blow, D. M. (2001). A novel spin filter method for the measurement of solubility. J. Cryst. Growth, 232, 17-20.
35. Hodge, T. A. (2014). A Size Limit for Protein Crystals, Chemistry. MS thesis, University of Alabama in Huntsville, Huntsville, Alabama, USA.
36. Hope, H. (1988). Cryocrystallography of biological macromolecules: a generally applicable method. Acta Cryst. B44, 22-26.
37. Howard, E. I., Blakeley, M. P., Haertlein, M., Petit-Haertlein, I., Mitschler, A., Fisher, S. J., Cousido-Siah, A., Salvay, A. G., Popov, A., Muller-Dieckmann, C., Petrova, T., Podjarny, A. (2011). Neutron structure of type-III antifreeze protein allows the reconstruction of AFP-ice interface. J. Mol. Recognit. 24, 724-732.
38. Hughes, R. C., Coates, L., Blakeley, M. P., Tomanicek, S. J., Langan, P., Kovalevsky, A. Y., Garc?á-Ruiz, J. M., Ng, J. D. (2012). Inorganic pyrophosphatase crystals from Thermococcus thioreducens for X-ray and neutron diffraction. Acta Cryst. F68, 1482-1487.
39. Iwai, W., Yagi, D., Ishikawa, T., Ohnishi, Y., Tanaka, I., Niimura, N. (2008). Crystallization and evaluation of hen egg-white lysozyme crystals for protein pH titration in the crystalline state. J. Synchrotron Rad. 15, 312-315.
40. Juers, D. H., Matthews, B. W. (2004a). The role of solvent transport in cryo-annealing of macromolecular crystals. Acta Cryst. D60, 412-421.
41. Juers, D. H., Matthews, B. W. (2004b). Cryo-cooling in macromolecular crystallography: advantages, disadvantages and optimization. Q. Rev. Biophys. 37, 105-119.
42. Juers, D. H., Weik, M. (2011). Similarities and differences in radiation damage at 100 K versus 160 K in a crystal of thermolysin. J. Synchrotron Rad. 18, 329-337.
43. Kim, Y. W., Barlow, D. A., Caraballo, K. G., Baird, J. K. (2003). Kinetics of supersaturation decay in the crystallization of lysozyme. Mol. Phys. 101, 2677-2686.
44. Kitago, Y., Watanabe, N., Tanaka, I. (2005). Structure determination of a novel protein by sulfur SAD using chromium radiation in combination with a new crystal-mounting method. Acta Cryst. D61, 1013-1021.
45. Lee, H.-M., Kim, Y. W., Baird, J. K. (2001). Electrophoretic mobility and zeta-potential of lysozyme crystals in aqueous solutions of some 1:1 electrolytes. J. Cryst. Growth, 232, 294-300.
46. Loll, P. J. (2014). Membrane proteins, detergents and crystals: what is the state of the art? Acta Cryst. F70, 1576-1583.
47. Lorber, B., Thé obald-Dietrich, A., Charron, C., Sauter, C., Ng, J. D., Zhu, D.-W., Giegé, R. (2002). From conventional crystallization to better crystals from space: a review on pilot crystallogenesis studies with aspartyl-tRNA synthetases. Acta Cryst. D58, 1674-1680.
48. Malkin, A. J., Kuznetsov, Y. G., Lucas, R.W., McPherson, A. (1999). Surface processes in the crystallization of turnip yellow mosaic virus visualized by atomic force microscopy. J. Struct. Biol. 127, 35-43.
49. Malkin, A. J., Thorne, R. E. (2004). Growth and disorder of macromolecular crystals: insights from atomic force microscopy and X-ray diffraction studies. Methods, 34, 273-299.
50. McPherson, A. (1999). Crystallization of Biological Macromolecules. Cold Spring Harbor Laboratory Press.
51. McPherson, A., Cudney, B. (2014). Optimization of crystallization conditions for biological macromolecules. Acta Cryst. F70, 1445-1467.
52. Meilleur, F., Munshi, P., Robertson, L., Stoica, A. D., Crow, L., Kovalevsky, A., Koritsanszky, T., Chakoumakos, B. C., Blessing, R. & Myles, D. A. A. (2013). The IMAGINE instrument: first neutron protein structure and new capabilities for neutron macromolecular crystallography. Acta Cryst. D69, 2157-2160.
53. Miers, H. A., Isaac, F. (1907). The spontaneous crystallisation of binary mixtures. Experiments on salol and betol. Proc. R. Soc. Lond. Ser. A, 79, 322-351.
54. Mullin, J. W. (1993). Crystallization, 3rd ed. Oxford: Butterworth-Heinemann.
55. Nakazato, K. (2008). Method of measuring protein solubility, process for producing crystal and apparatus therefore. US Patent No. 7416708 B2.
56. Ng, J. D., Clark, P. J., Stevens, R. C., Kuhn, P. (2008). In situ X-ray analysis of protein crystals in low-birefringent and X-ray transmissive plastic microchannels. Acta Cryst. D64, 189-197.
57. Ng, J. D., Garc?á-Ruiz, J. M. (2006). Counter-diffusion capillary crystallization for structural genomics. Trends Drug Discov. 3, 36.
58. Ng, J. D., Gavira, J. A., Garc?á-Ruiz, J. M. (2003). Protein crystallization by capillary counterdiffusion for applied crystallographic structure determination. J. Struct. Biol. 142, 218-231.
59. Ng, J. D., Kuznetsov, Y. G., Malkin, A. J., Keith, G., Giegé, R., McPherson, A. (1997). Visualization of RNA crystal growth by atomic force microscopy. Nucleic Acids Res. 25, 2582-2588.
60. Ng, J. D., Lorber, B., Giegé, R., Koszelak, S., Day, J., Greenwood, A. & McPherson, A. (1997). Comparative analysis of thaumatin crystals grown on earth and in microgravity. Acta Cryst. D53, 724-733.
61. Ng, J. D., Lorber, B., Witz, J., Thé obald-Dietrich, A., Kern, D., Giegé, R. (1996). The crystallization of biological macromolecules from precipitates: evidence for Ostwald ripening. J. Cryst. Growth, 168, 50-62.
62. Ng, J. D. (2002). Space-grown protein crystals are more useful for structure determination. Ann. N. Y. Acad. Sci. 974, 598-609.
63. Ng, J. D., Sauter, C., Lorber, B., Kirkland, N., Arnez, J., Giegé, R. (2002). Comparative analysis of space-grown and earth-grown crystals of an aminoacyl-tRNA synthetase: space-grown crystals are more useful for structural determination. Acta Cryst. D58, 645-652.
64. Ng, J. D., Stevens, R. C., Kuhn, P. (2008). Protein crystallization in restricted geometry: advancing old ideas for modern times in structural proteomics. Methods Mol. Biol. 426, 363-376.
65. Niimura, N. (2010). Neutron Scattering in Biology: Techniques and Applications, edited by J. Fitter, T. Gutberlet, J. Katsaras, pp. 43-62, Dordrecht: Springer.
66. Niimura, N., Bau, R. (2008). Neutron protein crystallography: beyond the folding structure of biological macromolecules. Acta Cryst. A64, 12-22.
67. Oksanen, E., Blakeley, M. P., Bonneté, F., Dauvergne, M. T., Dauvergne, F., Budayova-Spano, M. (2009). Large crystal growth by thermal control allows combined X-ray and neutron crystallographic studies to elucidate the protonation states in Aspergillus flavus urate oxidase. J. R. Soc. Interface, 6, S599-S610.
68. Ostwald, W. (1897). Studien über die Bildung und Umwandlung fester Kö rper. Z. Phys. Chem. 22, 289-330.
69. Otá lora, F., Garc?á-Ruiz, J. M. (1997). Crystal growth studies in microgravity with the APCF. I. Computer simulation of transport dynamics. J. Cryst. Growth, 182, 141-154
70. Otá lora, F., Gavira, J. A., Ng, J. D., Garc?á-Ruiz, J. M. (2009). Counterdiffusion methods applied to protein crystallization. Prog. Biophys. Mol. Biol. 101, 26-37.
71. Rakel, N., Baum, M., Hubbuch, J. (2014). Moving through threedimensional phase diagrams of monoclonal antibodies. Biotechnol. Prog. 30, 1103-1113.
72. Rayment, I. (2002). Small-scale batch crystallization of proteins revisited. Structure, 10, 147-151.
73. Rowe, J. D., Baird, J. K. (2007). Reduced capillary length scale in the application of Ostwald ripening theory to the coarsening of charged colloidal crystals in electrolyte solutions. Int. J. Thermophys. 28, 855-864.
74. Rupp, B. (2015). Origin and use of crystallization phase diagrams. Acta Cryst. F71, 247-260.
75. Sauter, C., Lorber, B., Kern, D., Cavarelli, J., Moras, D., Giegé, R. (1999). Crystallogenesis studies on yeast aspartyl-tRNA synthetase: use of phase diagram to improve crystal quality. Acta Cryst. D55, 149-156.
76. Sazaki, G., Kurihara, K., Nakada, T., Miyashita, S., Komatsu, H. (1996). A novel approach to the solubility measurement of protein crystals by two-beam interferometry. J. Cryst. Growth, 169, 355-360.
77. Shu, F., Ramakrishnan, V., Schoenborn, B. P. (2000). Enhanced visibility of hydrogen atoms by neutron crystallography on fully deuterated myoglobin. Proc. Natl Acad. Sci. USA, 97, 3872-3877.
78. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N.M., Olson, B. J. & Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
79. Streets, A. M., Quake, S. R. (2010). Ostwald ripening of clusters during protein crystallization. Phys. Rev. Lett. 104, 178102.
80. Teixeira, S. C. et al. (2008). New sources and instrumentation for neutrons in biology. Chem. Phys. 345, 133-151.
81. Veesler, S., Marcq, S., Lafont, S., Astier, J. P., Boistelle, R. (1994). Influence of polydispersity on protein crystallization: a quasi-elastic light-scattering study applied to-amylase. Acta Cryst. D50, 355-360.
82. Weber, I. T., Waltman, M. J., Mustyakimov, M., Blakeley, M. P., Keen, D. A., Ghosh, A. K., Langan, P., Kovalevsky, A. Y. (2013). Joint X-ray/neutron crystallographic study of HIV-1 protease with clinical inhibitor amprenavir: insights for drug design. J. Med. Chem. 56, 5631-5635.