Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-19T21:52:43.609Z Has data issue: false hasContentIssue false
  • English
  • Français

Shape change in crystallization of biological macromolecules

Published online by Cambridge University Press:  04 May 2016

Peter G. Vekilov ,
Sungwook Chung  and
Katy N. Olafson
Peter G. Vekilov
Affiliation:
Department of Chemical and Biomolecular Engineering, University of Houston, USA; [email protected]
Sungwook Chung
Affiliation:
School of Chemical and Biomolecular Engineering, Pusan National University, South Korea; [email protected]
Katy N. Olafson
Affiliation:
University of Houston, USA; [email protected]
Get access

Abstract

Conformational changes, and the formation of densely packed ordered aggregates or crystals, are behaviors that profoundly affect the properties of a molecule. Using the example of biological macromolecules, we discuss two types of interactions between these two behaviors. First, we demonstrate that shape change may be driven by crystallization if the gain in crystallization free energy is sufficient to overcome the transition to an unfavorable molecular conformation. Hence, the crystal structures of flexible molecules may be a poor representation of their free-phase atomic arrangements. Second, molecules with conformational variability, such as proteins, may facilitate the nucleation of their crystals by forming dense liquid clusters enriched in domain-swapped or misassembled oligomers. In the clusters, the nucleation barrier is reduced due to the lower surface free energy of the crystal/dense liquid interface, and nucleation is significantly faster.

Keywords

crystalnucleation & growthcrystallographic structure
Type
Research Article
Information
MRS Bulletin , Volume 41 , Issue 5: Nucleation in Atomic, Molecular, and Colloidal Systems , May 2016 , pp. 375 - 380
Copyright
Copyright © Materials Research Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Trotter, J., Acta Crystallogr. 14, 1135 (1961).Google Scholar
Almenningen, A., Bastiansen, O., Fernholt, L., Cyvin, B.N., Cyvin, S.J., Samdal, S., J. Mol. Struct. 128, 59 (1985).Google Scholar
Chayen, N.E., Helliwell, J.R., Snell, E.H., “Macromolecular Crystallization and Crystal Perfection,”IUCr Monographs on Crystallography, 24 (Oxford University Press, Oxford, New York, 2010).Google Scholar
Bergfors, T., Ed., Protein Crystallization, 2nd ed. (International University Line, La Jolla, CA, 2009).Google Scholar
Ng, J.D., Kuznetsov, Y.G., Malkin, A.J., Keith, G., Giege, R., McPherson, A., Nucleic Acids Res. 25, 2582 (1997).CrossRefGoogle Scholar
McPherson, A., Crystallization of Biological Macromolecules (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1999).Google Scholar
Malkin, A.J., Thorne, R.E., Methods 34, 273 (2004).CrossRefGoogle Scholar
Vekilov, P., “Nucleation and Growth Mechanisms of Protein Crystals,” in Handbook of Crystal Growth, Nishinaga, T., Ed. (Elsevier, Amsterdam, 2015), vol. 1, p. 795.Google Scholar
Nelson, D.L., Cox, M.M., Lehninger’s Principles of Biochemistry, 3rd ed. (W.H. Freeman, New York, 2000).Google Scholar
Ducruix, A., Giege, R., Eds., Crystallization of Nucleic Acids and Proteins: A Practical Approach (IRL Press, Oxford, 1992).Google Scholar
Devedjiev, Y., Acta Crystallogr. F Struct. Biol. Cryst. Commun. 71, 157 (2015).Google Scholar
Wütrich, K., Acta Crystallogr. D Biol. Crystallogr. 51, 249 (1995).CrossRefGoogle Scholar
Yee, A.A., Savchenko, A., Ignachenko, A., Lukin, J., Xu, X., Skarina, T., Evdokimova, E., Liu, C.S., Semesi, A., Guido, V., Edwards, A.M., Arrowsmith, C.H., J. Am. Chem. Soc. 127, 16512 (2005).Google Scholar
Grace, C.R.R., Perrin, M.H., Gulyas, J., DiGruccio, M.R., Cantle, J.P., Rivier, J.E., Vale, W.W., Riek, R., Proc. Natl. Acad. Sci. U.S.A. 104, 4858 (2007).Google Scholar
Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., Nucleic Acids Res. 28, 235 (2000).Google Scholar
Fisher, C.K., Stultz, C.M., Curr. Opin. Struct. Biol. 21, 426 (2011).CrossRefGoogle Scholar
Garbuzynskiy, S.O., Melnik, B.S., Lobanov, M.Y., Finkelstein, A.V., Galzitskaya, O.V., Proteins Struct. Funct. Bioinform. 60, 139 (2005).Google Scholar
Bissantz, C., Bernard, P., Hibert, M., Rognan, D., Proteins Struct. Funct. Bioinform. 50, 5 (2003).CrossRefGoogle Scholar
Kontoyianni, M., McClellan, L.M., Sokol, G.S., J. Med. Chem. 47, 558 (2004).Google Scholar
Meagher, K.L., Carlson, H.A., J. Am. Chem. Soc. 126, 13276 (2004).CrossRefGoogle Scholar
Cerqueira, N.M.F.S.A., Bras, N.F., Fernandes, P.A., Ramos, M.J., Proteins Struct. Funct. Bioinform. 74, 192 (2009).Google Scholar
Schlunegger, M.P., Bennett, M.J., Eisenberg, D., Adv. Protein Chem. 50, 61 (1997).Google Scholar
Bennett, M.J., Schlunegger, M.P., Eisenberg, D., Protein Sci. 4, 2455 (1995).Google Scholar
Zegers, I., Deswarte, J., Wyns, L., Proc. Natl. Acad. Sci. U.S.A. 96, 818 (1999).CrossRefGoogle Scholar
Liu, Y., Hart, P.J., Schlunegger, M.P., Eisenberg, D., Proc. Natl. Acad. Sci. U.S.A. 95, 3437 (1998).CrossRefGoogle Scholar
Hirota, S., Hattori, Y., Nagao, S., Taketa, M., Komori, H., Kamikubo, H., Wang, Z., Takahashi, I., Negi, S., Sugiura, Y., Kataoka, M., Higuchi, Y., Proc. Natl. Acad. Sci. U.S.A. 107, 12854 (2010).Google Scholar
McPherson, A., Introduction to Macromolecular Crystallography (Wiley, Hoboken, NJ, 2009).Google Scholar
Chernov, A.A., Komatsu, H., “Principles of Crystal Growth in Protein Crystallization,” in Science and Technology of Crystal Growth, van der Eerden, J.P., Bruinsma, O.S.L., Eds. (Kluwer Academic, Dordrecht, The Netherlands, 1995), p. 329.Google Scholar
Vekilov, P.G., Cryst. Growth Des. 7, 2796 (2007).CrossRefGoogle Scholar
Petsev, D.N., Chen, K., Gliko, O., Vekilov, P.G., Proc. Natl. Acad. Sci. U.S.A. 100, 792 (2003).Google Scholar
Yau, S.-T., Thomas, B.R., Vekilov, P.G., Phys. Rev. Lett. 85, 353 (2000).CrossRefGoogle Scholar
Yau, S.-T., Petsev, D.N., Thomas, B.R., Vekilov, P.G., J. Mol. Biol. 303, 667 (2000).Google Scholar
Derewenda, Z., Structure 12, 529 (2004).Google Scholar
Derewenda, Z.S., Acta Crystallogr. D Biol. Crystallogr. 66, 604 (2010).CrossRefGoogle Scholar
Derewenda, Z.S., Vekilov, P.G., Acta Crystallogr. D Biol. Crystallogr. 62, 116 (2006).Google Scholar
Malkin, A.J., Kuznetsov, Y.G., Glanz, W., McPherson, A., J. Phys. Chem. 100, 11736 (1996).CrossRefGoogle Scholar
Reviakine, I., Georgiou, D.K., Vekilov, P.G., J. Am. Chem. Soc. 125, 11684 (2003).CrossRefGoogle Scholar
Yau, S.-T., Vekilov, P.G., Nature 406, 494 (2000).Google Scholar
Gibbs, J.W., Trans. Connect. Acad. Sci. 3, 108 (1876).Google Scholar
Gibbs, J.W., Trans. Connect. Acad. Sci. 3, 343 (1878).Google Scholar
Galkin, O., Vekilov, P.G., Proc. Natl. Acad. Sci. U.S.A. 97, 6277 (2000).Google Scholar
Vekilov, P.G., Cryst. Growth Des. 4, 671 (2004).CrossRefGoogle Scholar
Pan, W., Kolomeisky, A.B., Vekilov, P.G., J. Chem. Phys. 122, 174905 (2005).CrossRefGoogle Scholar
Vekilov, P.G., Cryst. Growth Des. 10, 5007 (2010).Google Scholar
Malkin, A.J., McPherson, A., J. Cryst. Growth 128, 1232 (1993).CrossRefGoogle Scholar
Malkin, A.J., McPherson, A., Acta Crystallogr. D Biol. Crystallogr. 50, 385 (1994).Google Scholar
Vekilov, P.G., Nat. Nanotechnol. 6, 82 (2011).CrossRefGoogle Scholar
Yau, S.-T., Vekilov, P.G., J. Am. Chem. Soc. 123, 1080 (2001).Google Scholar
Galkin, O., Vekilov, P.G., J. Am. Chem. Soc. 122, 156 (2000).Google Scholar
Gibbs, J.W., The Scientific Papers of J. Willard Gibbs, Vol. One: Thermodynamics (Oxbow Press, Woodbridge, CT, 1993).Google Scholar
Li, Y., Lubchenko, V., Vorontsova, M.A., Filobelo, L., Vekilov, P.G., J. Phys. Chem. B 116, 10657 (2012).Google Scholar
Gliko, O., Pan, W., Katsonis, P., Neumaier, N., Galkin, O., Weinkauf, S., Vekilov, P.G., J. Phys. Chem. B 111, 3106 (2007).CrossRefGoogle Scholar
Sleutel, M., Van Driessche, A.E., Proc. Natl. Acad. Sci. U.S.A. 111, E546 (2014).Google Scholar
Maes, D., Vorontsova, M.A., Potenza, M.A.C., Sanvito, T., Sleutel, M., Giglio, M., Vekilov, P.G., Acta Crystallogr. F Struct. Biol. Cryst. Commun. 71, 815 (2015).Google Scholar
Gliko, O., Neumaier, N., Pan, W., Haase, I., Fischer, M., Bacher, A., Weinkauf, S., Vekilov, P.G., J. Am. Chem. Soc. 127, 3433 (2005).Google Scholar
Pan, W., Galkin, O., Filobelo, L., Nagel, R.L., Vekilov, P.G., Biophys. J. 92, 267 (2007).CrossRefGoogle Scholar
Pan, W., Vekilov, P.G., Lubchenko, V., J. Phys. Chem. B 114, 7620 (2010).Google Scholar
Bennett, M.J., Sawaya, M.R., Eisenberg, D., Structure 14, 811 (2006).CrossRefGoogle Scholar
Royer, W. Jr., “Structures of Red Blood Cell Hemoglobins,” in Blood and Tissue Oxygen Carriers, Mangum, Ch.P., Ed. (Springer, Berlin, 1992), p. 87.CrossRefGoogle Scholar
Bhosale, S.H., Rao, M.B., Deshpande, V.V., Microbiol. Rev. 60, 280 (1996).Google Scholar
Srivastava, P., Shukla, S., Choubey, S.K., Gomase, V.S., J. Enzyme Res. 1, 1 (2010).Google Scholar
Vorontsova, M.A., Maes, D., Vekilov, P.G., Faraday Discuss. 179, 27 (2015).Google Scholar
Vekilov, P.G., Vorontsova, M.A., Acta Crystallogr. F Struct. Biol. Cryst. Commun. 70, 271 (2014).Google Scholar
Albers, S.V., Meyer, B.H., Nat. Rev. Microbiol. 9, 414 (2011).Google Scholar
Sleytr, U.B., Messner, P., Pum, D., Sara, M., Angew. Chem. Int. Ed. 38, 1035 (1999).Google Scholar
Stewart, M., Beveridge, T.J., Trust, T.J., J. Bacteriol. 166, 120 (1986).Google Scholar
Chung, S., Shin, S.H., Bertozzi, C.R., De Yoreo, J.J., Proc. Natl. Acad. Sci. U.S.A. 107, 16536 (2010).Google Scholar
Shin, S.H., Chung, S., Sanii, B., Comolli, L.R., Bertozzi, C.R., De Yoreo, J.J., Proc. Natl. Acad. Sci. U.S.A. 109, 12968 (2012).Google Scholar
Kim, S.-H., Shin, D.H., Liu, J., Oganesyan, V., Chen, S., Xu, Q.S., Kim, J.-S., Das, D., Schulze-Gahmen, U., Holbrook, S.R., Holbrook, E.L., Martinez, B.A., Oganesyan, N., DeGiovanni, A., Lou, Y., Henriquez, M., Huang, C., Jancarik, J., Pufan, R., Choi, N.-G., Chandonia, J.-M., Hou, J., Gold, B., Yokota, H., Brenner, S.E., Adams, P.D., Kim, R., J. Struct. Funct. Genomics 6, 63 (2005).Google Scholar
Naganathan, A.N., Munoz, V., J. Am. Chem. Soc. 127, 480 (2005).Google Scholar