Introduction to protein crystallization.

Biological macromolecules can be crystallized by a variety of techniques, and using a wide range of reagents which produce supersaturated mother liquors. These may, in turn, be applied under different physical conditions such as temperature. The fundamental approaches to devising successful crystallization conditions and the factors that influence them are summarized here. For the Novice, it is hoped that this brief review might serve as a useful introduction and a stepping-stone to a successful X-ray structure determination. In addition, it may provide a framework in which to place the articles that follow.

[1]  J. García-Ruiz,et al.  Counterdiffusion methods for macromolecular crystallization. , 2003, Methods in enzymology.

[2]  A. McPherson,et al.  Searching for silver bullets: an alternative strategy for crystallizing macromolecules. , 2006, Journal of structural biology.

[3]  N. Madsen,et al.  Improvement of limit of diffraction and useful X-ray lifetime of crystals of glycogen debranching enzyme , 1986 .

[4]  Daniel Scheibe,et al.  A fully integrated protein crystallization platform for small-molecule drug discovery. , 2003, Journal of structural biology.

[5]  K. D. Collins,et al.  The Hofmeister effect and the behaviour of water at interfaces , 1985, Quarterly Reviews of Biophysics.

[6]  Carola Hunte,et al.  Membrane protein purification and crystallization : a practical guide , 2003 .

[7]  C. R. Middaugh,et al.  Stabilization of proteins by low molecular weight multi-ions. , 2002, Journal of pharmaceutical sciences.

[8]  W. Somers,et al.  Automated systems for protein crystallization. , 2004, Methods.

[9]  D. Myles,et al.  Neutron protein crystallography: current status and a brighter future. , 2006, Current opinion in structural biology.

[10]  J. Sedzik Regression analysis of factorially designed trials--a logical approach to protein crystallization. , 1995, Biochimica et biophysica acta.

[11]  A. McPherson In situ X‐ray crystallography , 2000 .

[12]  A. McPherson,et al.  Chimeric human-simian anti-CD4 antibodies form crystalline high symmetry particles. , 2000, Journal of structural biology.

[13]  EDWIN C. Webb The Enzymes , 1961, Nature.

[14]  Katherine A. Kantardjieff,et al.  Protein isoelectric point as a predictor for increased crystallization screening efficiency , 2004, Bioinform..

[15]  A. McPherson,et al.  ATOMIC-FORCE-MICROSCOPY STUDIES OF PHASE SEPARATIONS IN MACROMOLECULAR SYSTEMS , 1998 .

[16]  R. Wolfenden,et al.  Incomplete factorial search for conditions leading to high quality crystals of Escherichia coli cytidine deaminase complexed to a transition state analog inhibitor. , 1989, The Journal of biological chemistry.

[17]  J. Pflugrath,et al.  Developments in X-ray detectors , 1992, Current Biology.

[18]  P. Loll Membrane protein structural biology: the high throughput challenge. , 2003, Journal of structural biology.

[19]  A. D'arcy,et al.  The protein as a variable in protein crystallization. , 2003, Journal of structural biology.

[20]  R. Garavito,et al.  Detergents as Tools in Membrane Biochemistry* , 2001, The Journal of Biological Chemistry.

[21]  B. Segelke,et al.  Efficiency analysis of sampling protocols used in protein crystallization screening , 2001 .

[22]  J Sedzik DESIGN: a guide to protein crystallization experiments. , 1994, Archives of biochemistry and biophysics.

[23]  D. Frenkel,et al.  Enhancement of protein crystal nucleation by critical density fluctuations. , 1997, Science.

[24]  M. Caffrey,et al.  Membrane protein crystallization in lipidic mesophases: detergent effects. , 2000, Biophysical journal.

[25]  I. Wilson,et al.  Applications of the streak seeding technique in protein crystallization , 1991 .

[26]  J. J. Abel,et al.  Crystalline Insulin. , 1926, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A McPherson,et al.  The science of macromolecular crystallization. , 1995, Structure.

[28]  A. McPherson,et al.  Atomic force microscopy in the study of macromolecular crystal growth. , 2000, Annual review of biophysics and biomolecular structure.

[29]  K. D. Collins,et al.  Ions from the Hofmeister series and osmolytes: effects on proteins in solution and in the crystallization process. , 2004, Methods.

[30]  W. Denny,et al.  CRYSTALLOGRAPHY OF BIOLOGICAL MACROMOLECULES , 2005 .

[31]  C. Bracker,et al.  Polyethylene glycol: Catalytic effect on the crystallization of phosphoglucomutase at high salt concentration☆ , 1986 .

[32]  A. McPherson,et al.  Crystallization of proteins from polyethylene glycol. , 1976, The Journal of biological chemistry.

[33]  A. McPherson,et al.  Interferometric Studies of Growth Kinetics and Surface Morphology in Macromolecular Crystal Growth: Canavalin, Thaumatin, and Turnip Yellow Mosaic Virus , 1995 .

[34]  F. Franceschi,et al.  Crystallization of Biological Macromolecules , 1997 .

[35]  G. Nemerow,et al.  Strategies in the crystallization of glycoproteins and protein complexes , 1992 .

[36]  B. Warren,et al.  X-Ray Diffraction , 2014 .

[37]  W. Hughes,et al.  Preparation and Properties of Serum and Plasma Proteins. XIII. Crystallization of Serum Albumins from Ethanol-Water Mixtures1a,b , 1947 .

[38]  G. Eichele,et al.  Diffraction methods for biological macromolecules. Seed enlargement and repeated seeding. , 1985, Methods in enzymology.

[39]  David Glick,et al.  Methods of Biochemical Analysis , 1956 .

[40]  R Giegé,et al.  Crystallogenesis of biological macromolecules: facts and perspectives. , 1994, Acta crystallographica. Section D, Biological crystallography.

[41]  W. Comper,et al.  Thermodynamic nonideality in macromolecular solutions: interpretation of virial coefficients. , 1993, Archives of biochemistry and biophysics.

[42]  Sung-Hou Kim,et al.  Sparse matrix sampling: a screening method for crystallization of proteins , 1991 .

[43]  Alexander McPherson,et al.  Two approaches to the rapid screening of crystallization conditions , 1992 .

[44]  Charles W. Carter,et al.  Statistical design of experiments for protein crystal growth and the use of a precrystallization assay , 1988 .

[45]  Jan Drenth,et al.  Understanding protein crystallization on the basis of the phase diagram , 1999 .

[46]  C. Carter [5] Response surface methods for optimizing and improving reproducibility of crystal growth. , 1997, Methods in enzymology.

[47]  J. Neugebauer Detergents: an overview. , 1990, Methods in enzymology.

[48]  Martin Caffrey,et al.  Membrane protein crystallization. , 2003, Journal of structural biology.

[49]  A. McPherson,et al.  Atomic Force Microscopy Studies of Surface Morphology and Growth Kinetics in Thaumatin Crystallization , 1996 .

[50]  H. Komatsu,et al.  Principles of Crystal Growth in Protein Crystallization , 1995 .

[51]  M. J. Adams Preparation and Analysis of Protein Crystals , 1983 .

[52]  C. Carter Protein crystallization using incomplete factorial experiments. , 1979, The Journal of biological chemistry.

[53]  John R. Helliwell,et al.  Macromolecular Crystallography with Synchrotron Radiation , 1992 .

[54]  R. Piazza Interactions in protein solutions near crystallisation: a colloid physics approach 1 This work is de , 1999 .

[55]  A George,et al.  Predicting protein crystallization from a dilute solution property. , 1994, Acta crystallographica. Section D, Biological crystallography.

[56]  Joseph D Ng,et al.  Protein crystallization by capillary counterdiffusion for applied crystallographic structure determination. , 2003, Journal of structural biology.

[57]  J. Davenport Editor , 1960 .

[58]  W. Ray,et al.  The effect of polyethylene glycol on the growth and dissolution rates of a crystalline protein at high salt concentration. Phosphoglucomutase. , 1986, The Journal of biological chemistry.

[59]  Marc L Pusey,et al.  Trace fluorescent labeling for high-throughput crystallography. , 2006, Acta crystallographica. Section D, Biological crystallography.

[60]  Terese Bergfors,et al.  Seeds to crystals. , 2003, Journal of structural biology.

[61]  A. McPherson,et al.  Crystallization of Proteins, Nucleic Acids, and Viruses for X‐ray Diffraction Analysis , 2003 .

[62]  N. Chayen A novel technique to control the rate of vapour diffusion, giving larger protein crystals , 1997 .

[63]  Joseph R Luft,et al.  A deliberate approach to screening for initial crystallization conditions of biological macromolecules. , 2003, Journal of structural biology.

[64]  D. Crowfoot Crystalline Enzymes , 1940, Nature.

[65]  A. McPherson,et al.  Mechanisms of growth for protein and virus crystals , 1995, Nature Structural Biology.

[66]  D. Weiner,et al.  CHEMICAL and STRUCTURAL APPROACHES to RATIONAL DRUG DESIGN , 2020 .

[67]  K. Ingham Precipitation of proteins with polyethylene glycol. , 1990, Methods in enzymology.

[68]  J C Fontecilla-Camps,et al.  Systematic use of the incomplete factorial approach in the design of protein crystallization experiments. , 1991, The Journal of biological chemistry.

[69]  Terese Bergfors,et al.  Protein Crystallization: Techniques, Strategies, and Tips. , 1999 .

[70]  J. García‐Ruiz The Uses of Crystal Growth in Gels and other Diffusing-Reacting Systems , 1991 .

[71]  Arnaud Ducruix,et al.  Crystallization of Nucleic Acids and Proteins: A practical Approach , 1998 .

[72]  M. Wiener,et al.  A pedestrian guide to membrane protein crystallization. , 2004, Methods.

[73]  G. Gilliland A biological macromolecule crystallization database: A basis for a crystallization strategy , 1988 .

[74]  Arnon Chait,et al.  Efficient protein crystallization. , 2003, Journal of structural biology.

[75]  A. McPherson A brief history of protein crystal growth , 1991 .

[76]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[77]  E. Pebay-Peyroula,et al.  X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. , 1997, Science.

[78]  G. Langlet,et al.  International Tables for Crystallography , 2002 .

[79]  D. Winzor,et al.  Analysis of sedimentation equilibrium distributions reflecting nonideal macromolecular associations. , 2000, Biophysical Journal.

[80]  T. B. Osborne THE PROTEIDS OF THE KIDNEY BEAN. , 1894 .

[81]  P. Shlichta,et al.  Heterogeneous and Epitaxial Nucleation of Protein Crystals on Mineral Surfaces , 1988, Science.

[82]  A. McPherson Macromolecular crystals. , 1989, Scientific American.

[83]  P. Nollert,et al.  Lipidic cubic phases as matrices for membrane protein crystallization. , 2004, Methods.

[84]  A. McPherson,et al.  The influence of precipitant concentration on macromolecular crystal growth mechanisms , 2001 .

[85]  Goldberg,et al.  Non-detergent sulphobetaines: a new class of molecules that facilitate in vitro protein renaturation. , 1995, Folding & design.

[86]  H. Michel,et al.  Crystallization of membrane proteins. , 1983, Current opinion in structural biology.

[87]  I. Sorel,et al.  Statistical experimental design of protein crystallization screening revisited. , 2004, Acta crystallographica. Section D, Biological crystallography.

[88]  D. W. Bolen Effects of naturally occurring osmolytes on protein stability and solubility: issues important in protein crystallization. , 2004, Methods.

[89]  Alexander McPherson,et al.  Science in Pictures: Macromolecular Crystals , 1989 .

[90]  R. M. Herriott Solubility Methods in the Study of Proteins. , 1942 .

[91]  R. Feigelson The relevance of small molecule crystal growth theories and techniques to the growth of biological macromolecules , 1988 .

[92]  Richard Earl Dickerson Present at the Flood: How Structural Molecular Biology Came About , 2005 .

[93]  J. Sumner THE ISOLATION AND CRYSTALLIZATION OF THE ENZYME UREASE PRELIMINARY PAPER , 1926 .

[94]  A. McPherson,et al.  An in situ AFM investigation of catalase crystallization , 1997 .

[95]  J. García‐Ruiz,et al.  Ab initio crystallographic structure determination of insulin from protein to electron density without crystal handling. , 2002, Acta crystallographica. Section D, Biological crystallography.

[96]  Takao Sato,et al.  Precipitation diagram and optimization of crystallization conditions at low ionic strength for deglycosylated dye-decolorizing peroxidase from a basidiomycete. , 2005, Acta crystallographica. Section F, Structural biology and crystallization communications.

[97]  E. T. White,et al.  Protein purification by bulk crystallization: the recovery of ovalbumin. , 1995, Biotechnology and bioengineering.

[98]  Alexander McPherson,et al.  Preparation and analysis of protein crystals , 1982 .

[99]  N. Chayen,et al.  Experiment and theory for heterogeneous nucleation of protein crystals in a porous medium. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[100]  T. L. Hill Theory of Solutions. II. Osmotic Pressure Virial Expansion and Light Scattering in Two Component Solutions , 1959 .

[101]  M. Perutz THE HEMOGLOBIN MOLECULE. , 1964, Scientific American.

[102]  G L Gilliland,et al.  Biological Macromolecule Crystallization Database, Version 3.0: new features, data and the NASA archive for protein crystal growth data. , 1994, Acta crystallographica. Section D, Biological crystallography.

[103]  A. Chernov,et al.  Protein crystals and their growth. , 2003, Journal of structural biology.

[104]  S. Seifter,et al.  Precipitation techniques. , 1990, Methods in enzymology.

[105]  Anil Verma,et al.  Lysine Methylation as a Routine Rescue Strategy for Protein Crystallization , 2006, Structure.

[106]  J. D. Bernal,et al.  X-Ray Photographs of Crystalline Pepsin , 1934, Nature.

[107]  M. Wiener Existing and emergent roles for surfactants in the three-dimensional crystallization of integral membrane proteins , 2001 .

[108]  T. Hahn International tables for crystallography , 2002 .

[109]  R. Judge,et al.  An ultraviolet fluorescence-based method for identifying and distinguishing protein crystals. , 2005, Acta crystallographica. Section D, Biological crystallography.

[110]  A. McPherson,et al.  Polymeric precipitants for the crystallization of macromolecules. , 1995, Biochemical and biophysical research communications.

[111]  J. Kirkwood,et al.  Proteins, amino acids and peptides as ions and dipolar ions , 1943 .

[112]  S. Seifter,et al.  [22] Precipitation techniques , 1990 .

[113]  Crystallization of yeast orotidine 5′‐monophosphate decarboxylase complexed with 1‐(5′‐phospho‐β‐D‐ribofuranosyl) barbituric acid , 1991, Proteins.

[114]  P. Vekilov,et al.  Entropy and surface engineering in protein crystallization. , 2006, Acta crystallographica. Section D, Biological crystallography.

[115]  Arnaud Ducruix,et al.  Crystallization of nucleic acids and proteins , 1992 .

[116]  P. Vekilov,et al.  The Physics of Protein Crystallization , 2002 .

[117]  Miss A.O. Penney (b) , 1974, The New Yale Book of Quotations.