2D crystallization: from art to science.

The techniques as well as the principles of the 2D crystallization of membrane and water-soluble proteins for electron crystallography are reviewed. First, the biophysics of the interactions between proteins, lipids and detergents is surveyed. Second, crystallization of membrane proteins in situ and by reconstitution methods is discussed, and the various factors involved are addressed. Third, we elaborate on the 2D crystallization of water-soluble proteins, both in solution and at interfaces, such as lipid monolayers, mica, carbon film or mercury surfaces. Finally, techniques and instrumentations that are required for 2D crystallization are described.

[1]  W. Baumeister,et al.  Interfacial energies and surface‐tension forces involved in the preparation of thin, flat crystals of biological macromolecules for high‐resolution electron microscopy , 1991, Journal of microscopy.

[2]  W. Kühlbrandt.  Three-dimensional structure of the light-harvesting chlorophyll a/b–protein complex , 1984, Nature.

[3]  T. Ceska,et al.  Three-dimensional reconstruction of tubulin in zinc-induced sheets. II. Consequences of removal of microtubule associated proteins. , 1984, Journal of molecular biology.

[4]  W. Baumeister,et al.  The molecular architecture of extracellular hemoglobin of Eophila tellinii , 1989 .

[5]  J. Dubochet,et al.  Nucleosome arcs and helices. , 1978, Science.

[6]  J Frank,et al.  The structure of the stalk surface layer of a brine pond microorganism: correlation averaging applied to a double layered lattice structure , 1985, Journal of microscopy.

[7]  H. Fujisawa,et al.  Purification of characterization of gene 8 product of bacteriophage T3. , 1985, Virology.

[8]  R. Kornberg,et al.  Improved transfer of two-dimensional crystals from the air/water interface to specimen support grids for high-resolution analysis by electron microscopy. , 1991, Ultramicroscopy.

[9]  R. Josephs.  An analysis of the mechanism of crystallization of glutamic dehydrogenase. , 1975, Journal of Molecular Biology.

[10]  B. Jap.  High-resolution electron diffraction of reconstituted PhoE porin. , 1988, Journal of molecular biology.

[11]  G. Gaines,et al.  Insoluble Monolayers at Liquid-gas Interfaces , 1966 .

[12]  A. Klug,et al.  States of aggregation of tobacco mosaic virus protein. , 1971, Nature: New biology.

[13]  Two-dimensional crystalline arrays of Na,K-ATPase with new subunit interactions induced by cobalt-tetrammine-ATP. , 1989, Journal of ultrastructure and molecular structure research.

[14]  M. Mohraz,et al.  Structure of (Na+,K+)-ATPase as revealed by electron microscopy and image processing , 1984, The Journal of cell biology.

[15]  G. Mosser,et al.  Sub-domain structure of lipid-bound annexin-V resolved by electron image analysis. , 1991, Journal of molecular biology.

[16]  P. Yeagle.  Cholesterol and the cell membrane. , 1985, Biochimica et biophysica acta.

[17]  D. DeRosier,et al.  F-actin is a helix with a random variable twist , 1982, Nature.

[18]  R. Horne,et al.  A negative staining—carbon film technique for studying viruses in the electron microscope , 1975 .

[19]  J. Dubochet,et al.  Crystalline aggregation of a proteolytic fragment of the major head protein of bacteriophage T4. , 1979, Journal of molecular biology.

[20]  C. Remedios,et al.  Actin microcrystals and tubes formed in the presence of gadolinium ions , 1978, Nature.

[21]  R. Kornberg,et al.  Two-dimensional crystals of Escherichia coli RNA polymerase holoenzyme on positively charged lipid layers. , 1988, Journal of molecular biology.

[22]  F. Jurnak,et al.  Preliminary x-ray diffraction data for tetragonal crystals of trypsinized Escherichia coli elongation factor. , 1977, Journal of molecular biology.

[23]  R A Crowther,et al.  Visualization of alpha-helices in tobacco mosaic virus by cryo-electron microscopy. , 1989, Journal of molecular biology.

[24]  L. E. Donate,et al.  Bacteriophage T3 connector: three-dimensional structure and comparison with other viral head-tail connecting regions. , 1988, Journal of molecular biology.

[25]  R. Milligan,et al.  In vitro crystallization of ribosomes from chick embryos , 1982, The Journal of cell biology.

[26]  O. H. Griffith,et al.  THE LIPID‐PROTEIN INTERFACE IN BIOLOGICAL MEMBRANES * , 1980, Annals of the New York Academy of Sciences.

[27]  W. Chiu,et al.  Three-dimensional structural analysis of tetanus toxin by electron crystallography. , 1988, Journal of molecular biology.

[28]  J. N. Varghese,et al.  Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution , 1983, Nature.

[29]  N. Unwin,et al.  Ion channel of acetylcholine receptor reconstructed from images of postsynaptic membranes , 1988, Nature.

[30]  T. Arad,et al.  Membrane crystals of ubiquinone:cytochrome c reductase from Neurospora mitochondria , 1979, Nature.

[31]  D. Stokes,et al.  Structure of CaATPase: electron microscopy of frozen-hydrated crystals at 6 A resolution in projection. , 1990, Journal of molecular biology.

[32]  U. Sleytr.  Self-assembly of the hexagonally and tetragonally arranged subunits of bacterial surface layers and their reattachment to cell walls. , 1976, Journal of ultrastructure research.

[33]  W. Chiu,et al.  Crystallization of preliminary electron diffraction study to 3.7 A of DNA helix-destabilizing protein gp32*I. , 1978, Journal of molecular biology.

[34]  J. Lake,et al.  Ribosomal crystalline arrays of large subunits from Escherichia coli. , 1982, Science.

[35]  P. Argos,et al.  The Structure of Cytochrome b5 at 2.0 Å Resolution , 1972 .

[36]  T. Pollard,et al.  The structural basis for the intrinsic disorder of the actin filament: the "lateral slipping" model , 1991, The Journal of cell biology.

[37]  R. Huber,et al.  A porin‐type protein is the main constituent of the cell envelope of the ancestral eubacterium Thermotoga maritima , 1990 .

[38]  J. Rosenbusch,et al.  Paracrystalline arrays of protein-synthesis elongation factor Tu. Comparison with polymerized actin. , 1978, European journal of biochemistry.

[39]  W. Welte,et al.  The influence of heptane‐1,2,3‐triol on the size and shape of LDAO micelles Implications for the crystallisation of membrane proteins , 1991, FEBS letters.

[40]  K. Taylor,et al.  Three-dimensional reconstruction of negatively stained crystals of the Ca2+-ATPase from muscle sarcoplasmic reticulum. , 1986, Journal of molecular biology.

[41]  C. Taddei.  Ribosome arrangement during oogenesis of Lacerta sicula Raf. , 1972, Experimental cell research.

[42]  Kenneth A. Taylor,et al.  Structure of the S-layer of Sulfolobus acidocaldarius , 1982, Nature.

[43]  J. R. Harris.  The production of paracrystalline two-dimensional monolayers of purified protein molecules , 1982 .

[44]  C. Pabo,et al.  The operator-binding domain of λ repressor: structure and DNA recognition , 1982, Nature.

[45]  A. Kuzin,et al.  Two‐dimensional crystallization of reaction centers from Chloroflexus aurantiacus , 1990, FEBS letters.

[46]  A. Plückthun,et al.  Miniantibodies: use of amphipathic helices to produce functional, flexibly linked dimeric FV fragments with high avidity in Escherichia coli. , 1992, Biochemistry.

[47]  Two-dimensional and epitaxial crystallization of a mutant form of yeast RNA polymerase II. , 1991, Journal of molecular biology.

[48]  M. Yeager,et al.  Membrane topology and quaternary structure of cardiac gap junction ion channels. , 1992, Journal of molecular biology.

[49]  P. Shaw,et al.  The formation of two-dimensional arrays of isometric plant viruses in the presence of polyethylene glycol , 1980 .

[50]  H. Gaub,et al.  Synthetic lipid-anchored receptors based on the binding site of a monoclonal antibody. , 1992, Biochimica et biophysica acta.

[51]  S. Marčelja,et al.  Physical principles of membrane organization , 1980, Quarterly Reviews of Biophysics.

[52]  G. Mosser,et al.  Conditions of two-dimensional crystallization of cholera toxin B-subunit on lipid films containing ganglioside GM1 , 1991 .

[53]  P. Unwin,et al.  Electron microscopy of the stacked disk aggregate of tobacco mosaic virus protein. II. The influence of electron irradiation of the stain distribution. , 1974, Journal of molecular biology.

[54]  R. Horne.  The formation of virus crystalline and paracrystalline arrays for electron microscopy and image analysis. , 1979, Advances in virus research.

[55]  S. Hovmöller,et al.  Structural studies of cytochrome reductase. Improved membrane crystals of the enzyme complex and crystallization of a subcomplex. , 1983, Journal of molecular biology.

[56]  K. B. Blodgett.  Films Built by Depositing Successive Monomolecular Layers on a Solid Surface , 1935 .

[57]  J. Harris.  The negative staining-carbon film procedure : technical considerations and a survey of macromolecular applications , 1991 .

[58]  E. Boekema,et al.  Characterization by electron microscopy of isolated particles and two-dimensional crystals of the CP47-D1-D2-cytochrome b-559 complex of photosystem II. , 1990, Biochemistry.

[59]  R. Garavito,et al.  Intranuclear crystalloids in leaves and styles of Linaria vulgaris Mill. , 1980, Journal of ultrastructure research.

[60]  Y. Kagawa,et al.  Structure of ATPase (coupling factor TF1) from a thermophilic bacterium. , 1977, Journal of molecular biology.

[61]  G. Zampighi,et al.  Two forms of isolated gap junctions. , 1979, Journal of molecular biology.

[62]  Seth A. Darst,et al.  Three-dimensional structure of yeast RNA polymerase II at 16 Å resolution , 1991, Cell.

[63]  A. Hoenger,et al.  Two-dimensional crystals of Escherichia coli maltoporin and their interaction with the maltose-binding protein. , 1992, Journal of molecular biology.

[64]  J. Meunier,et al.  Microscope at the Brewster angle: Direct observation of first‐order phase transitions in monolayers , 1991 .

[65]  S. Edelstein,et al.  Structural studies on porcine brain tubulin in extended sheets. , 1977, Journal of molecular biology.

[66]  G. Shipley,et al.  Interaction of cholera toxin with ganglioside GM1 receptors in supported lipid monolayers. , 1987, Biochemistry.

[67]  J. Lake,et al.  Helical arrays of Escherichia coli small ribosomal subunits produced in vitro. , 1979, Journal of molecular biology.

[68]  U. Aebi,et al.  Probing actin polymerization by intermolecular cross-linking , 1988, The Journal of cell biology.

[69]  T. Pollard,et al.  Structure of crystalline actin sheets , 1980, Nature.

[70]  W. Baumeister,et al.  Principles of organization in eubacterial and archaebacterial surface proteins. , 1989, Canadian journal of microbiology.

[71]  J. Kistler,et al.  Lens gap junctions and orthogonal arrays are unrelated , 1980, FEBS letters.

[72]  J. Haselgrove,et al.  Structure of the cytochrome c oxidase dimer. Electron microscopy of two-dimensional crystals. , 1982, Journal of molecular biology.

[73]  J. W. Greenawalt,et al.  Ultrastructure of striated inclusions in Neurospora. , 1970, Journal of ultrastructure research.

[74]  D. Engelman,et al.  Refolding of bacteriorhodopsin in lipid bilayers. A thermodynamically controlled two-stage process. , 1987, Journal of molecular biology.

[75]  A Yonath,et al.  A tunnel in the large ribosomal subunit revealed by three-dimensional image reconstruction. , 1987, Science.

[76]  S. Singer,et al.  The Fluid Mosaic Model of the Structure of Cell Membranes , 1972, Science.

[77]  R. Kornberg,et al.  Two-dimensional crystallization technique for imaging macromolecules, with application to antigen–antibody–complement complexes , 1983, Nature.

[78]  H. Taguchi,et al.  Image analysis by electron microscopy of two-dimensional crystals developed on a mercury surface of chaperonin from Thermus thermophilus. , 1991, Journal of biochemistry.

[79]  R. Henderson,et al.  Three-dimensional model of purple membrane obtained by electron microscopy , 1975, Nature.

[80]  A. Sentenac,et al.  Structural study of the yeast RNA polymerase A. Electron microscopy of lipid-bound molecules and two-dimensional crystals. , 1990, Journal of molecular biology.

[81]  S. Müller,et al.  In vitro assembly of gap junctions. , 1991, Journal of structural biology.

[82]  J M Carazo,et al.  Three-dimensional reconstruction of the connector of bacteriophage phi 29 at 1.8 nm resolution. , 1986, Journal of molecular biology.

[83]  R. Newman,et al.  Crystallization of p68 on lipid monolayers and as three-dimensional single crystals. , 1989, Journal of molecular biology.

[84]  N. M. Tooney,et al.  Crystalline states of a modified fibrinogen. , 1977, Journal of molecular biology.

[85]  J. Berriman,et al.  Molecular portrait of lens gap junction protein MP70. , 1990, Journal of structural biology.

[86]  I. Wilson,et al.  Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution , 1981, Nature.

[87]  P. Unwin.  Three-dimensional model of membrane-bound ribosomes obtained by electron microscopy , 1977, Nature.

[88]  A. Martonosi,et al.  Crystallization of Ca2+-ATPase in detergent-solubilized sarcoplasmic reticulum. , 1987, The Journal of biological chemistry.

[89]  R. Kornberg,et al.  Three-dimensional structure of Escherichia coli RNA polymerase holoenzyme determined by electron crystallography , 1989, Nature.

[90]  S. N. Timasheff,et al.  In vitro vinblastine-induced tubulin paracrystals. , 1982, The Journal of biological chemistry.

[91]  R. Henderson,et al.  Measurement and evaluation of electron diffraction patterns from two-dimensional crystals , 1984 .

[92]  R. Henderson,et al.  Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. , 1990, Journal of molecular biology.

[93]  H. Gaub,et al.  A miniaturized micro-fluorescence film balance for protein-containing lipid monolayers spread from a vesicle suspension. , 1991, Journal of biochemical and biophysical methods.

[94]  G. Mosser,et al.  Structural analysis of two-dimensional arrays of cholera toxin B-subunit. , 1991, Journal of electron microscopy technique.

[95]  A. Klug,et al.  A low resolution structure for the histone core of the nucleosome , 1980, Nature.

[96]  S. Karasaki.  Studies on amphibian yolk 1. The ultrastructure of the yolk platelet. , 1963 .

[97]  W. Welte,et al.  Deoxylysolecithin and a new biphenyl detergent as solubilizing agents for bovine rhodopsin. Functional test by formation of metarhodopsin II and binding of G-protein. , 1987, Biochemistry.

[98]  A. Engel,et al.  Localization of the lipopolysaccharides in metal-shadowed reconstituted lipid-porin membranes , 1990 .

[99]  A C Steven,et al.  Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli , 1977, The Journal of cell biology.

[100]  Charles Tanford,et al.  The hydrophobic effect , 1980 .

[101]  D. Dorset.  Electron crystallography of organic molecules , 1991 .

[102]  B. Jap,et al.  Three-dimensional electron diffraction of PhoE porin to 2.8 A resolution. , 1990, Journal of molecular biology.

[103]  C. Mannella.  Phospholipase-induced crystallization of channels in mitochondrial outer membranes. , 1984, Science.

[104]  Crystallization and preliminary crystallographic data of chicken gizzard G-actin . DNase I complex and Physarum G-actin . DNase I complex. , 1979, Journal of biochemistry.

[105]  Shigeru Endo,et al.  Hexagonal Structure of Two-Dimensional Crystals of the α3β3 Complex of Thermophilic ATP Synthase , 1989 .

[106]  R. Henderson,et al.  Temperature-dependent aggregation of bacteriorhodopsin in dipalmitoyl- and dimyristoylphosphatidylcholine vesicles. , 1978, Journal of molecular biology.

[107]  J. Israelachvili.  Intermolecular and surface forces , 1985 .

[108]  A. Lustig,et al.  Rapid isolation of OmpF porin-LPS complexes suitable for structure-function studies. , 1989, Biochemistry.

[109]  J. Deisenhofer,et al.  Detergent structure in crystals of a bacterial photosynthetic reaction centre , 1989, Nature.

[110]  W Baumeister,et al.  Two-dimensional crystallization of a bacterial surface protein on lipid vesicles under controlled conditions. , 1992, Biophysical journal.

[111]  C. Stetson.  THE STATE OF HEMOGLOBIN IN SICKLED ERYTHROCYTES , 1966, Journal of Experimental Medicine.

[112]  C. Mannella.  Fusion of the mitochondrial outer membrane: use in forming large, two-dimensional crystals of the voltage-dependent, anion-selective channel protein. , 1989, Biochimica et biophysica acta.

[113]  T. Pollard,et al.  Structure of the actin molecule determined from electron micrographs of crystalline actin sheets with a tentative alignment of the molecule in the actin filament. , 1983, Journal of molecular biology.

[114]  W. Kühlbrandt,et al.  High-resolution electron crystallography of light-harvesting chlorophyll a/b-protein complex in three different media. , 1991, Journal of molecular biology.

[115]  A. Engel,et al.  Gene 20 product of bacteriophage T4 its purification and structure. , 1981, Journal of molecular biology.

[116]  J. Weisel,et al.  Crystals of modified fibrinogen: size, shape and packing of molecules. , 1978, Journal of molecular biology.

[117]  H. Larsson,et al.  Induction of a sheet polymer of tubulin by Zn2+. , 1976, Experimental cell research.

[118]  H. Yamada,et al.  Reconstitution of an ordered structure from major outer membrane constituents and the lipoprotein-bearing peptidoglycan sacculus of Escherichia coli , 1978, Journal of bacteriology.

[119]  Å. Kjaerheim.  Crystallized tubules in the mitochondrial matrix of adrenal cortical cells. , 1967, Experimental cell research.

[120]  M. Zulauf,et al.  Light scattering of proteins as a criterion for crystallization , 1992 .

[121]  U. Lindberg,et al.  Crystallization of a non-muscle actin. , 1976, Journal of molecular biology.

[122]  E. Buhle,et al.  The structure of the Ca2+ ATPase as revealed by electron microscopy and image processing of ordered arrays. , 1983, Journal of ultrastructure research.

[123]  Evaporated carbon stabilizes thin, frozen-hydrated specimens , 1989 .

[124]  J. Vonck,et al.  Electron microscopy and image analysis of two-dimensional crystals and single molecules of alcohol oxidase from Hansenula polymorpha. , 1990, Biochimica et biophysica acta.

[125]  Three-dimensional structure of the surface protein of Clostridium thermosaccharolyticum , 1987 .

[126]  H. Ringsdorf,et al.  Interaction between biotin lipids and streptavidin in monolayers: formation of oriented two-dimensional protein domains induced by surface recognition. , 1989, Biochemistry.

[127]  A. Engel,et al.  Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. , 1979, Journal of molecular biology.

[128]  R. Kornberg,et al.  Three-dimensional structure of cholera toxin penetrating a lipid membrane. , 1988, Science.

[129]  C. Blake,et al.  X-Ray Investigation of Fragment 1 of Bovine Prothrombin , 1977, Thrombosis and Haemostasis.

[130]  P. Schultz,et al.  Two‐dimensional crystallization of DNA gyrase B subunit on specifically designed lipid monolayers , 1990, FEBS letters.

[131]  J. Frank,et al.  Structure of the Channels in the Outer Mitochondrial Membrane: Electron Microscopic Studies of the Periodic Arrays Induced by Phospholipase a(2) Treatment of the Neurospora membrane. , 1986, Biophysical journal.

[132]  A. Engel,et al.  Characterization of complexes between recA protein and duplex DNA by electron microscopy. , 1982, Journal of molecular biology.

[133]  U. Aebi,et al.  The Three‐Dimensional Structure of the Actin Filament Revisited a , 1986, Annals of the New York Academy of Sciences.

[134]  R. Henderson,et al.  Three-dimensional structures of cytochrome c oxidase vesicle crystals in negative stain. , 1982, Journal of molecular biology.

[135]  J. Rosenbusch,et al.  Two-dimensional crystal packing of matrix porin. A channel forming protein in Escherichia coli outer membranes. , 1983, Journal of molecular biology.

[136]  P. Fromherz.  Electron Microscopic Studies of Lipid Protein Films , 1971, Nature.

[137]  R. Kornberg,et al.  Two-dimensional crystals of streptavidin on biotinylated lipid layers and their interactions with biotinylated macromolecules. , 1991, Biophysical journal.

[138]  D. Papahadjopoulos.  Effects of Bivalent Cations and Proteins on Thermotropic Properties of Phospholipid Membranes: Implications for the Molecular Mechanism of Fusion and Endocytosis , 1977 .

[139]  G. Büldt,et al.  Densely packed β-structure at the protein-lipid interface of porin is revealed by high-resolution cryo-electron microscopy , 1989 .

[140]  P. L. Jørgensen,et al.  Crystallization of membrane-bound Na+,K+-ATPase in two dimensions. , 1988, Methods in enzymology.

[141]  W. Keegstra,et al.  Two‐dimensional crystallization experiments * , 1986, Journal of microscopy.

[142]  K. Namba,et al.  Monolayer crystallization of flagellar L-P rings by sequential addition and depletion of lipid , 1991, Science.

[143]  T. Sun,et al.  Large scale purification and immunolocalization of bovine uroplakins I, II, and III. Molecular markers of urothelial differentiation. , 1990, The Journal of biological chemistry.

[144]  W. J. Grip,et al.  [38] Thermal stability of rhodopsin and opsin in some novel detergents , 1982 .

[145]  S. Fleischer,et al.  Alteration of synaptic membrane cholesterol/phospholipid ratio using a lipid transfer protein. Effect on gamma-aminobutyric acid uptake. , 1983, The Journal of biological chemistry.

[146]  B. Trus,et al.  Naturally crystalline porin in the outer membrane of Bordetella pertussis. , 1988, Journal of molecular biology.

[147]  M. Thelestam,et al.  Crystalline layers and three-dimensional structure ofStaphylococcus aureus α-toxin , 1990 .

[148]  E. Uzgiris.  Self-organization of IgE immunoglobulins on phospholipid films. , 1987, The Biochemical journal.

[149]  P. R. Smith,et al.  Novel crystalline sheets of Na,K-ATPase induced by phospholipase A2. , 1985, Journal of ultrastructure research.

[150]  T. Pollard,et al.  Crystalline actin sheets: their structure and polymorphism , 1981, The Journal of cell biology.

[151]  G. Vanderkooi,et al.  Biological membrane structure. 3. The lattice structure of membranous cytochrome oxidase. , 1972, Biochimica et biophysica acta.

[152]  K. Leonard,et al.  Three-dimensional structure of NADH: ubiquinone reductase (complex I) from Neurospora mitochondria determined by electron microscopy of membrane crystals. , 1987, Journal of molecular biology.

[153]  W. Baumeister,et al.  Structure of the porin from a bacterial stalk , 1987, FEBS letters.

[154]  G. Zampighi,et al.  Structure of the junction between communicating cells , 1980, Nature.

[155]  K. Gehring,et al.  Structural architecture of an outer membrane channel as determined by electron crystallography , 1991, Nature.

[156]  R. Horne,et al.  A negative staining-carbon film technique for studying viruses in the electron microscope. II. Application to adenovirus type 5. , 1975, Journal of ultrastructure research.

[157]  K. Taylor,et al.  [21] Analysis of two-dimensional crystals of Ca2+-ATPase in sarcoplasmic reticulum , 1988 .

[158]  W. Chiu,et al.  Electron imaging of crotoxin complex thin crystal at 3.5 A. , 1984, Journal of molecular biology.

[159]  R. Kornberg,et al.  Two-dimensional crystals of enzyme-effector complexes: ribonucleotide reductase at 18-A resolution. , 1987, Biochemistry.

[160]  Dirk Hoenig,et al.  Direct visualization of monolayers at the air-water interface by Brewster angle microscopy , 1991 .

[161]  Hideyuki Yoshimura,et al.  Two-dimensional crystallization of proteins on mercury , 1990 .