Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-12-05T02:17:36.883Z Has data issue: false hasContentIssue false
  • English
  • Français

Two-dimensional crystallization of membrane proteins

Published online by Cambridge University Press:  17 March 2009

W. Kühlbrandt
W. Kühlbrandt
Affiliation:
EMBL, Meyerhofstr. 1, D-6900 Heidelberg, Germany
Get access Rights & Permissions [Opens in a new window]

Extract

In spite of several great breakthroughs, the overall rate of progress in determining high-resolution structures of membrane proteins has been slow. This is entirely due to the scarcity of suitable, well-ordered crystals. Most membrane proteins are multimeric complexes with a composite molecular mass in excess of 50000 Da which puts them outside the range of current solution NMR techniques. For the foreseeable future, detailed information about the structure of large membrane proteins will therefore depend on crystallographic methods.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 25 , Issue 1 , February 1992 , pp. 1 - 49
Copyright
Copyright © Cambridge University Press 1992

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

Akiba, T., Yoshimura, H. & Namba, K. (1991). Monolayer crystallization of flagellar L-P rings by sequential addition and depletion of lipid. Science 252, 1544–1546.CrossRefGoogle Scholar
Amos, L. A., Henderson, R. & Unwin, P. N. T. (1982). Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Prog. Biophys. molec. Biol. 39, 183–231.CrossRefGoogle ScholarPubMed
Baldwin, J. & Henderson, R. (1984). Measurement and evaluation of electron diffraction patterns from two-dimensional crystals. Ultramicroscopy 14, 319–336.CrossRefGoogle Scholar
Baldwin, J. M., Henderson, R., Beckman, R. & Zemlin, F. (1988). Images of purple membrane at 2·8 Å resolution obtained by cryo-electron microscopy. J. molec. Biol. 202, 585–591.CrossRefGoogle ScholarPubMed
Barnakov, A. N., Demin, V. V., Kuzin, A. P., Zargarov, A. A., Zolotarev, A. S. & Abdulaev, N. G. (1990). Two-dimensional crystallization of reaction centres from Chloroflexus aurantiacus. FEBS Lett. 265, 126–128.CrossRefGoogle ScholarPubMed
Bassi, R., Magaldi, A. G., Tognon, G., Giacometti, G. M. & Miller, K. R. (1989). Two-dimensional crystals of the photosystem II reaction center complex from higher plants. Eur. J. Cell Biol. 50, 84–93.Google ScholarPubMed
Boekema, E. J. (1990). The present state of two-dimensional crystallization of membrane proteins. Electron Microsc. Rev. 3, 87–96.CrossRefGoogle ScholarPubMed
Brisson, A. & Unwin, P. N. T. (1984). Tubular crystals of acetylcholine receptor. J. Cell Biol. 99, 1202–1211.CrossRefGoogle ScholarPubMed
Brisson, A. & Unwin, P. N. T. (1985). Quaternary structure of the acetylcholine receptor. Nature 315, 474–477.CrossRefGoogle ScholarPubMed
Buldt, G., Mischel, M., Hentschel, M. P., Regenass, M. & Rosenbusch, J. P. (1986). Two-dimensional lattices of porin diffract to 6 Å resolution. FEBS Lett. 205, 29–31.CrossRefGoogle Scholar
Butler, P. J. G. & Kuhlbrandt, W. (1988). Determination of the aggregate size in detergent solution of the light-harvesting chlorophyll a/b-protein complex from chloroplast membranes. Proc. natn. Acad. Set. U.S.A. 85, 3797–3801.CrossRefGoogle ScholarPubMed
Cevc, G. & Marsh, D. (1987). Phospholipid Bilayers: Physical Principles and Models. New York: John Wiley & Sons.Google Scholar
Christie, W. W. (1982). Lipid Analysts. Oxford: Pergamon Press.Google Scholar
Cole, S. T., Condon, C., Lemire, B. D. & Weiner, J. H. (1985). Molecular biology, biochemistry and bioenergetics of fumarate reductase, a complex membrane-bound iron-sulfur flavoenzyme of Escherichia coli. Biochim. biophys. Acta 811, 381–403.CrossRefGoogle ScholarPubMed
Corless, J. M., McCaslin, D. R. & Scott, B. L. (1982). Two-dimensional rhodopsin crystals from disk membranes of frog retinal rod outer segments. Proc. natn. Acad. Sci. U.S.A. 79, 1116–1120.CrossRefGoogle ScholarPubMed
Deatherage, J. F., Henderson, R. & Capaldi, R. A. (1982). Three-dimensional structure of cytochrome c oxidase vesicle crystals in negative stain, J. molec. Biol. 158, 487–499.CrossRefGoogle ScholarPubMed
Deisenhofer, J. & Michel, H. (1989). The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 245, 1463–1473.CrossRefGoogle ScholarPubMed
Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. (1984). X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. molec. Biol. 180, 385–398.CrossRefGoogle Scholar
Deisenhofer, J., Epp, O., Miki, K., HUber, R. & Michel, H. (1985). X-ray structure analysis at 3 A resolution of a membrane protein complex: folding of the protein subunits in the photosynthetic reaction center from Rhodopseudomonas viridis. Nature 318, 618–624.CrossRefGoogle Scholar
Dekker, J. P., Betts, S. D., Yocum, C. F. & Boekema, E. J. (1990). Characterization by electron microscopy of isolated particles and two-dimensional crystals of the CP47-Di-D2-cytochrome b-559 complex of photosystem II. Biochemistry 29, 3220–3225.CrossRefGoogle ScholarPubMed
Derosier, D. J. & Moore, P. B. (1970). Reconstruction of three-dimensional images from electron micrographs of structures with helical symmetry. J. molec. Biol. 52, 355–369.CrossRefGoogle ScholarPubMed
Dorset, D. L., Engel, A., Haner, M., Massalski, A. & Rosenbusch, J. P. (1983). Two-dimensional crystal packing of matrix porin. A channel forming protein in Escherichia coli outer membranes. J. molec. Biol. 165, 701–710.CrossRefGoogle Scholar
Dratz, E. A., Van Breemen, J. F. L., Kamps, K. M. P., Keegstra, W. & Van Bruggen, E. F. J. (1985). Two-dimensional crystallization of bovine rhodopsin. Biochim. biophys. Acta 832, 337–342.CrossRefGoogle ScholarPubMed
Dubochet, J., Adrian, M., Chang, J.-J., Homo, J.-C, Lepault, J., McDowall, A. W. & Schultz, P. (1988). Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129–228.CrossRefGoogle ScholarPubMed
Dux, L., Pikula, S., Mullner, N. & Martonosi, A. (1987). Crystallization of Ca2+- ATPase in detergent-solubilized sarcoplasmic reticulum. J. biol. Chem. 262, 6439–6442.CrossRefGoogle ScholarPubMed
Engel, A., Massalski, A., Schindler, H., Dorset, D. L. & Rosenbusch, J. P. (1985). Porin channel triplets merge into single outlets in Escherichia coli outer membranes. Nature 317, 643–645.CrossRefGoogle ScholarPubMed
Engel, A., Holzenburg, A., Stauffer, K., Rosenbusch, J. & AEBI, U. (1988). A novel reconstitution method for inducing the formation of regular 2D arrays of membrane proteins and lipids (ed. Bailey, G. W.), pp. 152–153. Proceedings of the 46th Annual Meeting of the Electron Microscopical Society of America.San Francisco Press, Inc.CrossRefGoogle Scholar
Engelman, D. M., Steitz, T. A. & Goldman, A. (1986). Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Ann. Rev. Biophys. Chem. 15, 321–353.CrossRefGoogle ScholarPubMed
Ford, R. C., Hefti, A. & Engel, A. (1990). Ordered arrays of the photosystem I reaction centre after reconstitution: projections and surface reliefs of the complex at 2 nm resolution. EMBO J. 9, 3067–3075.CrossRefGoogle ScholarPubMed
Frey, T. G., Chan, S. H. P. & Schatz, G. (1978). Structure and orientation of cytochrome c oxidase in crystalline membranes. J. Biol. Chem. 253, 4389–4395.CrossRefGoogle ScholarPubMed
Frey, T. G., Costello, M. J., Karlsson, B., Haselgrove, J. C. & Leigh, J. S. (1982). Structure of the cytochrome c oxidase dimer: electron microscopy of two-dimensional crystals. J. molec. Biol. 162, 113–130.CrossRefGoogle ScholarPubMed
Fujiyoshi, Y., Mizusaki, T., Morikawa, K., Yamagishi, H., Aoki, Y., Kihara, H. & Harada, Y. (1991). Development of a superfluid helium stage for high-resolution electron microscopy. Ultramicroscopy (in the Press).CrossRefGoogle Scholar
Fuller, D. S., Capaldi, R. A. & Henderson, R. (1979). Structure of cytochrome c oxidase in deoxycholate-derived two-dimensional crystals. J. molec. Biol. 134, 3O5–327.CrossRefGoogle ScholarPubMed
Garavito, R. M., Markovic-Housley, Z. & Jenkins, J. A. (1986). The growth and characterization of membrane protein crystals. J. Crystal Growth 76, 701–709.CrossRefGoogle Scholar
Glaeser, R. M., Zilker, A., Radermacher, M., Gaub, H. E., Hartmann, T. & Baumeister, W. (1990). Interfacial energies and surface-tension forces involved in the preparation of thin flat crystals of biological macromolecules for high-resolution electron microscopy. J. Microscopy 161, 21–45.CrossRefGoogle Scholar
Haschemeyer, R. H. & Myers, R. J. (1972). Negative staining. In Principles and Techniques of Electron Microscopy, (ed. Hayat, M. S.), pp. 101–150. New York: Van Nostrand Reinhold.Google Scholar
Hayward, S. B. & Glaeser, R. M. (1980). High resolution cold stage for the JEOL 100B and 100C electron microscopes. Ultramicroscopy 5, 3–8.CrossRefGoogle ScholarPubMed
Henderson, R. (1975). The structure of the purple membrane from Halobacterium halobium: analysis of the X-ray diffraction pattern. J. molec. Biol. 93, 123–138.CrossRefGoogle Scholar
Henderson, R. & Unwin, P. N. T. (1975). Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28–32.CrossRefGoogle ScholarPubMed
Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E. & Downing, K. H. (1990). Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. molec. Biol. 213, 899–929.CrossRefGoogle ScholarPubMed
Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J. & Zemlin, F. (1986). Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3·5 Å resolution. Ultramicroscopy 19, 147–178.CrossRefGoogle Scholar
Hofhaus, G., Weiss, H. & Leonard, K. (1991). Electron microscopic analysis of the peripheral and membrane parts of mitochondrial NADH dehydrogenase (complex I). J. molec. Biol. 221, 1027–1043.CrossRefGoogle ScholarPubMed
Hovmöller, S., Leonard, K. & Weiss, H. (1981). Membrane crystals of a subunit complex of mitochondrial cytochrome reductase containing the cytochromes b and c 1. FEBS Lett. 123, 118–122.CrossRefGoogle ScholarPubMed
Hovmöller, S., Slaughter, M., Berriman, J., Karlsson, B., Weiss, H. & Leonard, K. (1983). Structural studies of cytochrome reductase. Improved membrane crystals of the enzyme complex and crystallization of a subcomplex. J. molec. Biol. 165, 401–406.CrossRefGoogle ScholarPubMed
Huang, L. & Berry, E. A. (1990). Purification and characterization of the proton translocating plasma membrane ATPase of red beet storage tissue. Biochim. biophys. Acta 1039, 241–252.CrossRefGoogle ScholarPubMed
Israelachvili, J. N., Mavcelja, S. & Hovu, R. G. (1980). Physical principles of membrane organization. Q. Rev. Biophys. 13, 121–200.CrossRefGoogle ScholarPubMed
Jap, B. K. (1988). High-resolution electron diffraction of reconstituted PhoE porin. J. molec. Biol. 199, 229–231.CrossRefGoogle ScholarPubMed
Jap, B. K. (1989). Molecular design of PhoE porin and its functional consequences. J. molec. Biol. 205, 407–419.CrossRefGoogle ScholarPubMed
Jap, B. K., Downing, K. H. & Walian, P. J. (1990). Structure of PhoE porin in projection at 3–5 Å resolution. J. Struct. Biol. 103, 57–63.CrossRefGoogle Scholar
Jap, B. K., Walian, P. J. & Gehring, K. (1991). Structural architecture of an outer membrane channel as determined by electron crystallography. Nature 350, 167–170.CrossRefGoogle ScholarPubMed
Kessel, M., Brennan, M. J., Trus, B. L., Bisher, M. E. & Steven, A. C. (1988). Naturally crystalline porin in the outer membrane of Bordetella pertussis. J. molec. Biol. 203, 275–278.CrossRefGoogle ScholarPubMed
Klug, A. & Crowther, R. A. (1972). 3D image reconstruction from the viewpoint of information theory. Nature (New Biology) 238, 435–440.CrossRefGoogle Scholar
Kornberg, R. D. & Darst, S. A. (1991). Two-dimensional crystals of proteins on lipid layers. Curr. Opinion in Struct. Biol. 1, 642–646.CrossRefGoogle Scholar
Kühlbrandt, W. (1984). Three-dimensional structure of the light-harvesting chlorophyll a/b-protein complex. Nature 307, 478–480.CrossRefGoogle Scholar
Kühlbrandt, W. (1987 a). Photosynthetic membranes and membrane proteins. In Electron Microscopy of Proteins. vol. 6 (ed. Harris, J. R. and Home, R. W.), pp. 155–207. London: Academic Press.Google Scholar
Kühlbrandt, W. (1987 b). Three-dimensional crystals of the light-harvesting chlorophyll a/b-protein complex from pea chloroplasts. J. molec. Biol. 194, 757–762.CrossRefGoogle ScholarPubMed
Kühlbrandt, W. (1988 a). Three-dimensional crystallization of membrane proteins. Q. Rev. Biophys. 21, 429–477.CrossRefGoogle ScholarPubMed
Kühlbrandt, W. (1988 b). Structure of light-harvesting chlorophyll a/b-protein complex from plant photosynthetic membranes at 7 Å resolution in projection. J. molec. Biol. 202, 849–864.CrossRefGoogle ScholarPubMed
Kühlbrandt, W. & Downing, K. H. (1989). Two-dimensional structure of plant lightharvesting complex at 3·7 Å resolution by electron crystallography. J. molec. Biol. 207, 823–828.CrossRefGoogle ScholarPubMed
Kühlbrandt, W. & Wang, D. N. (1991). Three-dimensional structure of plant lightharvesting complex determined by electron crystallography. Nature 350, 130–134.CrossRefGoogle ScholarPubMed
Kühlbrandt, W., Thaler, T. & Wehrli, E. (1983). The structure of membrane crystals of the light-harvesting chlorophyll a/b-protein complex. J. Cell Biol. 96, 1414–1424.CrossRefGoogle ScholarPubMed
Lefranc, G., Knapek, E. & Dietrich, I. (1982). Superconducting lens design. Ultramicroscopy 10, 111–124.CrossRefGoogle Scholar
Leifer, D. & Henderson, R. (1983). Three-dimensional structure of orthorhombic purple membrane at 6·5 Å resolution. J. molec. Biol. 163, 451–466.CrossRefGoogle ScholarPubMed
Leitch, B. & Finbow, M. E. (1990). The gap junction-like form of a vacuolar proton channel component appears not to be an artifact of isolation: an immunocytochemical localization study. Exp. Cell Res. 190, 218–226.CrossRefGoogle Scholar
Leonard, K., Haiker, H. & Weiss, H. (1987). Three-dimensional structure of NADH: ubiquinone reductase (complex I) from Neurospora mitochondria determined by electron microscopy of membrane crystals. J. molec. Biol. 194, 277–286.CrossRefGoogle ScholarPubMed
Leonard, K., Wingfield, P., Arad, T. & Weiss, H. (1981). Three-dimensional structure of ubiquinol: cytochrome c reductase from Neurospora mitochondria determined by electron microscopy of membrane crystals. J. molec. Biol. 149, 259–274.CrossRefGoogle ScholarPubMed
Lepault, J., Dargent, B., Tichelaar, W., Rosenbusch, J. P., Leonard, K. & Pattus, F. (1988). Three-dimensional reconstruction of maltoporin from electron microscopy and image processing. EMBO J. 7, 261–268.CrossRefGoogle ScholarPubMed
Li, J. (1985). Light-harvesting chlorophyll a/b-protein: three-dimensional structure of a reconstituted membrane lattice in negative stain. Proc. natn. Acad. Sci. U.S.A. 82, 386–390.CrossRefGoogle ScholarPubMed
Li, J. & Hollingshead, C. (1982). Formation of crystalline arrays of chlorophyll a/b light-harvesting protein by membrane reconstitution. Biophys. J. 37, 363–370.CrossRefGoogle ScholarPubMed
Lyon, M. K. & Miller, K. R. (1985). Crystallization of the light-harvesting chlorophyll a/b-complex within thylakoid membranes. J. Cell Biol. 100, 1139–1147.CrossRefGoogle ScholarPubMed
Lyon, M. K. & Unwin, P. N. T. (1988). Two-dimensional structure of the lightharvesting chlorophyll a/b-complex by cryolectron microscopy. J. Cell Biol. 106, 1515–1523.CrossRefGoogle ScholarPubMed
Mannella, C. A. (1984). Phospholipase-induced crystallization of channels in mitochondrial outer membranes. Science 224, 165–166.CrossRefGoogle ScholarPubMed
Mannella, C. A. (1989). Fusion of the mitochondrial outer membrane: use in forming large, two-dimensional crystals of the voltage-dependent, anion-selective channel protein. Biochim. biophys. Acta 981, 15–20.CrossRefGoogle ScholarPubMed
Marsh, D. (1990). Lipid-protein interactions in membranes. FEBS Lett. 268, 371–375.CrossRefGoogle ScholarPubMed
McPherson, A. (1990). Useful principles for the crystallization of proteins. In Crystallization of Membrane Proteins, chapter 1 (ed. Michel, H.). Boca Raton: CRC Press.Google Scholar
Michel, H. (1982). Three-dimensional crystals of a membrane protein complex. The photosynthetic reaction centre from Rhodopseudomonas viridis. J. tnolec. Biol. 158, 567–572.CrossRefGoogle ScholarPubMed
Michel, H. (1983). Crystallization of membrane proteins. Trends Biochem. Sci. 8, 56–59.CrossRefGoogle Scholar
Michel, H. (1990). General and practical aspects of membrane protein crystallization. In Crystallization of Membrane Proteins, chapter 3 (ed. Michel, H.). Boca Raton: CRC Press.Google Scholar
Michel, H., Oesterhelt, D. & Henderson, R. (1980). Orthorhombic two-dimensional crystal form of purple membrane. Proc. natn. Acad. Sci. U.S.A. 77, 338–342.CrossRefGoogle ScholarPubMed
Miller, K. R. & Jacob, J. S. (1983). Two-dimensional crystals formed from photosynthetic reaction centers. J. Cell Biol. 97, 1266–1270CrossRefGoogle ScholarPubMed
Mohraz, M., Yee, M. & Smith, P. R. (1985). Novel crystalline sheets of Na, K-ATPase induced by phospholipase A2. J. Ultrastruct. Res. 93, 17–26.CrossRefGoogle ScholarPubMed
Newman, R. (1991). Two-dimensional crystallization of proteins on lipid monolayers. Electron Microscopy Reviews (in the Press).CrossRefGoogle ScholarPubMed
Rachel, R., Engel, A. M., Huber, R., Stetter, K.-O. & Baumeister, W. (1990). A porin-type protein is the main constituent of the cell envelope of the ancestral eubacterium Thermotoga maritima. FEBS Lett. 262, 64–68.CrossRefGoogle Scholar
Reiländer, H., Boege, F., Vasudevan, S., Maul, G., Herman, M., Dees, C., Hampe, W., Helmreich, E. J. M. & Michel, H. (1991). Purification and functional characterization of the human β2-ardrenergic receptor produced in baculovirusinfected insect cells. FEBS Lett. 282, 441–444.CrossRefGoogle ScholarPubMed
Reiss-Husson, F. (1991). Crystallization of membrane proteins. In Crystallization of Proteins and Nucleic Acids : A Practical Approach, chapter 8 (eds. Ducruix, A. and Giegé, R.). Oxford: IRL Press.Google Scholar
Roth, M., Lewit-Bentley, A., Michel, H., Deisenhofer, J., Huber, R. & Oesterhelt, D. (1989). Detergent structure in crystals of a bacterial photosynthetic reaction centre. Nature 340, 659–662.CrossRefGoogle Scholar
Sass, H. J., Beckmann, E., Zemlin, F., Van Heel, M., Zeitler, E., Rosenbusch, J. P., Dorset, D. L. & Massalski, A. (1989). Densely packed β-structure at the proteinlipid interface of porin is revealed by high-resolution cryo-electron microscopy. J. molec. Biol. 209, 171–175.CrossRefGoogle ScholarPubMed
Sharp, K. A. (1991). The hydrophobic effect. Curr. Opinion Struct. Biol. 1, 171–174.CrossRefGoogle Scholar
Skriver, E., Maunsbach, A. B., Hebert, H. & Jørgensen, P. L. (1988). Crystallization of membrane-bound Na+, K+-ATPase in two dimensions. Methods Enzym. 156, 80–87.CrossRefGoogle ScholarPubMed
Skriver, E., Maunsbach, A. B., Hebert, H., Scheiner-Bobis, G. & Schoner, W. (1989). Two-dimensional crystalline arrays of Na, K-ATPase with new subunit interactions induced by cobalt-tetrammine-ATP. J. Ultrastruct. Mol. Struct. Res. 102, 189–195.CrossRefGoogle ScholarPubMed
Stark, W., Kühlbrandt, W., Wildhaber, I., Wehrli, E. & Mühlethaler, K. (1984). The structure of the photoreceptor unit of Rhodopseudomonas viridis. EMBO J. 3, 777–783.CrossRefGoogle ScholarPubMed
Stokes, D. L. & Green, N. M. (1990 a). Three-dimensional crystals of CaATPase from sarcoplasmic reticulum. Symmetry and molecular packing. Biophys. J. 57, 1–14.CrossRefGoogle ScholarPubMed
Stokes, D. L. & Green, N. M. (1990 b). Structure of CaATPase: Electron microscopy of frozen-hydrated crystals at 6 Å resolution in projection. J. molec. Biol. 213, 529–538.CrossRefGoogle ScholarPubMed
Sun, F. F., Prezbindowski, K. S., Crane, F. L. & Jacobs, E. E. (1968). Physical state of cytochrome oxidase. Relationship between membrane formation and ionic strength. Biochim. biophys. Acta 153, 804–818.CrossRefGoogle ScholarPubMed
Tanford, C. (1980). The Hydrophobic Effect: Formation of Micelles and Biological Membranes. New York: John Wiley & Sons Inc.Google Scholar
Taylor, K. A., Dux, L., Varga, S., Ting-Beall, H. P. & Martonosi, A. (1988). Analysis of two-dimensional crystals of Ca2+-ATPase in sarcoplasmic reticulum. Methods Enzymol. 157, 271–289.CrossRefGoogle ScholarPubMed
Toyoshima, C. & Unwin, N. (1988 a). Ion channel of acetylcholine receptor reconstructed from images of postsynaptic membranes. Nature 336, 247–250.CrossRefGoogle ScholarPubMed
Toyoshima, C. & Unwin, N. (1988 b). Contrast transfer for frozen-hydrated specimens: Determination from pairs of defocused images. Ultramicroscopy 25, 279–292.CrossRefGoogle ScholarPubMed
Unwin, P. N. T. & Ennis, P. D. (1983). Calcium-mediated changes in gap junction structure: evidence from the low-angle X-ray pattern. J. Cell Biol. 97, 1459–1466.CrossRefGoogle ScholarPubMed
Unwin, P. N. T. & Ennis, P. D. (1984). Two configurations of a channel-forming membrane protein. Nature 307, 609–612.CrossRefGoogle ScholarPubMed
Unwin, P. N. T. & Henderson, R. (1975). Molecular structure determination by electron microscopy of unstained crystalline specimens. J. molec. Biol. 94, 425–440.CrossRefGoogle ScholarPubMed
Valpuesta, J. M., Henderson, R. & Frey, T. G. (1990). Electron cryo-microscopic analysis of crystalline cytochrome oxidase. J. molec. Biol. 214, 237–251.CrossRefGoogle ScholarPubMed
Vanderkooi, G., Senior, A. E., Capaldi, R. A. & Hayashi, H. (1972). Biological membrane structure. III. The lattice structure of membranous cytochrome oxidase. Biochim. biophys. Acta 274, 38–48.CrossRefGoogle Scholar
Vasudevan, S., Reiländer, H., Maul., G. & Michel, H. (1991). Expression and cell membrane localization of rat M3 muscarinic acetylcholine receptor produced in Sf 9 insect cells using the baculovirus system. FEBS Lett. 283, 52–56.CrossRefGoogle Scholar
Walian, P. J. & Jap, B. K. (1990). Three-dimensional electron diffraction of PhoE porin to 2·8 Å resolution. J. molec. Biol. 215, 429–438.CrossRefGoogle ScholarPubMed
Wang, D. N. & Kühlbrandt, W. (1991). High-resolution electron crystallography of light-harvesting chlorophyll a/b-protein complex in three different media. J. molec. Biol. 217, 691–699.CrossRefGoogle ScholarPubMed
Weiss, H. & Leonard, K. (1990). Preparation of membrane crystals of mitochondrial NADH:ubiquinone reductase and ubiquinol: cytochrome c reductase and structure analysis by electron microscopy, chapter II. In Crystallization of Membrane Proteins (ed. Michel, H.). Boca Raton: CRC Press.Google Scholar
Weiss, M. S., Kreusch, A., Schiltz, E., Nestel, U., Welte, W., Weckesser, J. & Schulz, G. E. (1991). The structure of porin from Rhodobacter capsulatus at 1·8 Å resolution. FEBS Lett. 280, 379–382.CrossRefGoogle ScholarPubMed
Wilkinson, W. O., Walsh, J. P., Corless, J. M. & Bell, R. M. (1986). Crystalline arrays of the Escherichia coli sn-glycerol-3-phosphate acyltransferase, an integral membrane protein. J. biol. Chem. 261, 9951–9958.CrossRefGoogle Scholar
Wingfield, P., Arad, T., Leonard, K. & Weiss, H. (1979). Membrane crystals of ubiquinone: cyochrome c reductase from Neurospora mitochondria. Nature 280, 696–697.CrossRefGoogle Scholar
Zampighi, G., Kyte, I. & Freytag, W. (1984). Structural organization of (Na+ + K+)- ATPase in purified membranes. J. Cell Biol. 98, 1851–1864.CrossRefGoogle ScholarPubMed
Zampighi, G. & Unwin, P. N. T. (1979). Two forms of isolated gap junctions. J. molec. Biol. 135, 451–464.CrossRefGoogle ScholarPubMed
Zulauf, M. (1990). Detergent phenomena in membrane protein crystallization. In Crystallization of membrane proteins, chapter 2 (ed. Michel, H.). Boca Raton: CRC Press.Google Scholar