Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-05-01T13:39:30.932Z Has data issue: false hasContentIssue false
  • English
  • Français

Three-dimensional crystallization of membrane proteins

Published online by Cambridge University Press:  17 March 2009

W. Kühlbrandt
W. Kühlbrandt
Affiliation:
Biophysics Section, Department of Physics, Imperial College, London SW7 2BZ, England
Get access Rights & Permissions [Opens in a new window]

Extract

As recently as 10 years ago, the prospect of solving the structure of any membrane protein by X-ray crystallography seemed remote. Since then, the threedimensional (3-D) structures of two membrane protein complexes, the bacterial photosynthetic reaction centres of Rhodopseudomonas viridis (Deisenhofer et al. 1984, 1985) and of Rhodobacter sphaeroides (Allen et al. 1986, 1987 a, 6; Chang et al. 1986) have been determined at high resolution. This astonishing progress would not have been possible without the pioneering work of Michel and Garavito who first succeeded in growing 3-D crystals of the membrane proteins bacteriorhodopsin (Michel & Oesterhelt, 1980) and matrix porin (Garavito & Rosenbusch, 1980). X-ray crystallography is still the only routine method for determining the 3-D structures of biological macromolecules at high resolution and well-ordered 3-D crystals of sufficient size are the essential prerequisite.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 21 , Issue 4 , November 1988 , pp. 429 - 477
Copyright
Copyright © Cambridge University Press 1988

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

Allen, J. P. & Feher, G. (1984). Crystallization of reaction center from Rhodopseudomonas sphaeroides: preliminary characterization. Proc. natn. Acad. Sci. U.S.A. 81, 4795–4799.Google Scholar
Allen, J. P.Feher, G., Yeates, T. O., Rees, D. C., Deisenhofer, J., Michel, H. & Huber, R. (1986). Structural homology of reaction centres from Rhodopseudomonas spaheroides and Rohodpseudomonas viridis as determined by X-ray diffraction. Proc. natn. Acad. Sci. U.S.A. 83, 8589–8593.CrossRefGoogle ScholarPubMed
Allen, J. P.Feher, G., Yeates, T. O., Komyia, H. & Rees, D. C. (1987 a). Structure of the reaction centre from Rhodobacter sphaeroides R-26: the cofactors. Proc. natn. Acad. Sci. U.S.A. 84, 5730–5734.Google Scholar
Allen, J. P.Feher, G., Yeates, T. O., Komyia, H. & Rees, D. C. (1987 b). Structure of the reaction centre from Rhodobacter sphaeroides R-26: the protein subunits. 1Proc. natn. Acad. Sci. U.S.A. 84, 6162–6166.Google Scholar
Amos, L. A., Henderson, R. & Unwin, P. N. T. (1982). Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Proc. Biophys. molec. Biol. 39, 183–231.Google Scholar
Attwood, D. & Florence, A. T. (1983). Surfactant Systems. London: Chapman and Hall.Google Scholar
Baldwin, J. M., Henderson, R., Beckmann, E. & Zemlin, F. (1988). Electron microscopy of purple membrane at 2.8 Å resolution. J. molec. Biol. (in the press).Google Scholar
Boekema, E. J., van Heel, M., & van Bruggen, E. F. J. (1986). Preparation of twodimensional crystals of complex I and image analysis. Meth. Enzymol. 126, 344–353.Google Scholar
Brisson, A. & Unwin, P. N. T. (1984). Tubular crystals of acetylecholine receptor. J. Cell Biol. 99, 1202–1211.Google Scholar
Brisson, A. & Unwin, P. N. T. (1985). Quarternary structure of the acetylcholine receptor. Nature 315, 474–477.Google Scholar
Brudvig, G. W., Worland, S. T. & Sauer, K. (1983). New rapid procedure for isolating photosynthetic reaction centres using cytochrome c affinity chromatography. Proc. natn. Acad. Sci. U.S.A. 80, 683–686.CrossRefGoogle Scholar
Burke, J. J., Ditto, C. L. & Arntzen, C. J. (1978). Involvement of the light-harvesting complex in cation regulation of excitation energy distribution of chloroplasts. Arch. Biochem. Biophys. 187, 252–263.Google Scholar
Butler, P. J. G. & Kühlbrandt, 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. Sci. U.S.A. 85, 3797–3801.Google Scholar
Chang, C.-H., Schiffer, M., Tiede, D., Smith, U. & Norris, J. (1985). Characterization of bacterial photosynthetic reaction centre crystals from Rhodopseudomonas sphaeroides R-26 by X-ray diffraction. J. molec. Biol. 186, 201–203.Google Scholar
Chang, C.-H., Tiede, D., Tang, J., Smith, U., Norris, J. & Schiffer, M. (1986). Structure of Rhodopseudomonas sphaeroides R-26 reaction center. FEBS Lett. 205, 82–86.Google Scholar
Cogdell, R. A., Woolley, K. J., Ferguson, L. A. & Dawkins, D. J. (1988). Crystallization or purple bacterial antenna complexes. In Crystallization of Membrane Proteins (ed. Michel, H.). Boca Raton, Florida, U.S.A.: CRC Press (in the press).Google Scholar
De Grip, W. (1982). Thermal stability of rhodopsin and opsin in some novel detergents. Meth. Enzymol. 81, 256–265.Google Scholar
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 center from Rhodopseudomonas viridis. J. molec. Biol. 180, 385–398.Google Scholar
Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. (1985). X-ray structure analysis at 3 Å resoltuion of a membrane protein complex: Folding of the protein subunits in the photosynthetic reaction centre from Rhodopseudomans viridis. Nature 318, 618–624.Google Scholar
Ducruix, A. & Reiss-Husson, F. (1987). Preliminary characterization by X-ray diffraction of crystals of photochemical reaction centres from wild-type Rhodop-seudomonas sphaeroides. J. molec. Biol. 193, 419–421.CrossRefGoogle Scholar
Eisenberg, D., Schwarz, E., Komaromy, M. & Wall, R. (1984). Analysis of membrane and surface protein sequences with the hydrophobic moment. J. molec. Biol. 179, 125–142.CrossRefGoogle ScholarPubMed
Fillingame, R. H. & Foster, D. L. (1986). Purification of F1F0H+-ATPase from Escherichia coli. Meth. Enzymol. 126, 545–557.Google Scholar
Ford, R. C., Picot, D. & Garavito, R. M. (1987). Crystallization of the photosystem I reaction centre. EMBO J. 6, 1581–1586.Google Scholar
Foster, D. L., Mosher, M. E., Futai, M. & Fillingame, R. H. (1980). Subunits of the H+-ATPase of Escherichia coli. Overproduction of an eight-subunit F1F0-ATPase following induction of a λ-transducing phage carrying the unc operon. J. biol. Chem. 255, 12037–12041.Google Scholar
Frank, H. A., Taremi, S. & Knox, J. R. (1987). Crystallization and preliminary X-ray and optical spectroscopic characterization of the photochemical reaction center from Rhodobacter sphaeroides strain 2.4.1. J. molec. Biol. 198, 139–141.Google Scholar
Frey, T. G., Chan, S. M. P. & Schatz, G. (1978). Structure and orientation of cytochrome-c oxidase in crystalline membranes – Studies by electron microscopy and by labelling with subunit-specific antibodies. J. biol. Chem. 253, 4389–4395.CrossRefGoogle ScholarPubMed
Garavito, R. M., Jenkins, J., Jansonius, J. N., Karlsson, R. & Rosenbusch, J. P. (1983). X-ray diffraction analysis of matrix porin, an integral membrane protein from Escherichia coli outer membranes. J. molec. Biol. 164, 313–327.CrossRefGoogle ScholarPubMed
Garavito, R. M., Hinz, U. & Neuhaus, J. M. (1984). The crystallization of outer membrane proteins from E. coli. Studies on lam B and omp A products. J. biol. Chem. 259, 4254–4257.Google Scholar
Garavito, R. M., Markovic-Housley, Z. & Jenkins, J. (1986). The growth and characterization of membrane protein crystals. J. Crystal Growth 76, 701–109.Google Scholar
Garavito, R. M. & Rosenbusch, J. P. (1980). Three-dimensional crystals of an integral membrane protein. J. Cell Biol. 86, 327–329.Google Scholar
Garavito, R. M. & Rosenbusch, J. P. (1986). Isolation and crystallization of bacterial porin. Meth. Enzymol. 125, 309–328.Google Scholar
Gilliland, G. L. & Davies, D. R. (1984). Protein crystallization: The growth of largescale single crystals. Meth. Enzymol. 104, 370–381.Google Scholar
Gorenne, A. R. & Ernst, R. (1978). Solubilization of membrane proteins by sulfobetaines, novel zwitterionic surfactants. Anal. Biochem. 87, 28–37.CrossRefGoogle Scholar
Gros, P., Groendijk, H., Drenth, J. & Hol, W. G. J. (1988). Experiences in membrane protein crystallization. J. Crystal Growth (in the press).Google Scholar
Helenius, A. & Simons, K. (1975). Solubilization of membranes by detergents. Biochim. Biophys. Acta 415, 29–79.Google Scholar
Helenius, A., McCaslin, D. R., Fries, E. & Tanford, C. (1979). Properties of detergents. Meth. Enzymol. 56, 734–749.Google Scholar
Henderson, R. & Shotton, D. (1980). Crystallization of purple membrane in three dimensions. J. molec. Biol. 139, 99–109.Google Scholar
Henderson, R. & Unwin, P. N. T. (1975). Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28–32.Google Scholar
Hendrickson, W. A. & Teeter, M. M. (1981). Structure of the hyrophobic protein crambin determined directly from the anomalous scattering of sulphur. Nature 291, 107–113.Google Scholar
Herrmann, K. W. (1962). Non-ionic-cationic micellar properties of dimethyl dodecylamine oxide. J. Phys. Chem. 66, 295–300.Google Scholar
Hovmöller, S., Slaughter, M., Berriman, J., Karlsson, B., Weiss, H. & Leonard, K. (1983). Structural studies of cytochrome oxidase. Improved membrane crystals of the enzyme complex and crystallization of a subcomplex. J. molec. Biol. 165, 401–406.CrossRefGoogle Scholar
Ide, J., Klug, D., Kühlbrandt, W., Giorgi, L. B. & Porter, G. (1987). The state of detergent solubilized light-harvesting chlorophyll a/b protein complex as monitored by picosecond time-resolved fluorescence spectroscopy. Biochim. Biophys. Acta 893, 349–384.Google Scholar
Kleffel, B., Garavito, R. M., Baumeister, W. & Rosenbusch, J. P. (1985). Secondary structure of a channel-forming protein: porin from E. coli outer membranes. EMBO J. 4, 1589–1592.Google 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). Three-dimensional crystals of the light-harvesting chlorophyll a/b protein complex from pea chloroplasts. J. molec. Biol. 194, 757–762.Google Scholar
Kühlbrandt, W. (1988 a). The structure of light-harvesting chlorophyll a/b protein complex from plant photosynthetic membranes at 7 Å resolution in projection. J. molec. Biol. (in the press).CrossRefGoogle Scholar
Kühlbrandt, W. (1988 b). Crystallization of the light-harvesting chlorophyll a/b protein complex from chloroplast membranes. In Crystallization of Membrane Proteins (ed. Michel, H.). Boca Raton, Florida, U.S.A.: CRC Press (in the press).Google Scholar
Kühlbrandt, W., Thaler, T. & Wehrli, E. (1983). The stucture of membrane crystals of the light-harvesting cholorphyll a/b protein complex. J. Cell Biol. 96, 1414–1424.Google Scholar
Kushner, L. M. & Hubbard, W. D. (1964). Viscometric and turbidometric measurements on dilute aqueous solutions of a non-ionic detergent. J. Phys. Chem. 58, 1163–1167.Google Scholar
Lehn, J. M. (1985). Supramolecular chemistry: receptors, catalysts and carriers. Science 227, 849–856.Google Scholar
Lemire, B. D. & Weiner, J. H. (1986). Fumarate reductase of Escherichia coli. Meth. Enzymol. 126, 377–386.CrossRefGoogle ScholarPubMed
Leonard, K., Wingfield, P.Arad, T. & Weiss, W. (1981). Three-dimensional structure of ubiquinol: cytochrome c reductase from Neurospora mitochondria determined by electron microscopy of membrane crystals J. molec. Bio. 149, 259–274.Google Scholar
Li, J. & Hollingshead, C. (1982). Formation of crystalline arrays of chlorophyll a/blight-harvesting protein by membrane reconstitution. Biophys. J. 37, 363–370.Google Scholar
McPherson, A. (1982). Preparation and Analysis of Protein Crystals. New York: J. Wiley & Sons.Google Scholar
Michel, H. (1982 a). Three-dimensional crystals of a membrane protein complex. The photosynthetic reaction centre from Rhodopseudomonas viridis. J. molec. Biol. 158, 567–572.Google Scholar
Michel, H. (1982 b). Characterization and crystal packing of three-dimensional bacteriorhodopsin crystals. EMBO J. 1, 1267–1271.Google Scholar
Michel, H. (1983). Crystallization of membrane proteins. Trends Biochem. Sci. 8, 56–59.Google Scholar
Michel, H. (ed.) (1988). Crystallization of Membrane Proteins. Boca Raton, Florida, U.S.A.: CRC Press (in the press).Google Scholar
Michel, H. & Oesterhelt, D. (1980). Three-dimensional crystals of membrane proteins: bacteriorhodopsin. Proc. natn. Acad. Sci. U.S.A. 77, 1283–1285.Google Scholar
Miller, K. R. & Jacob, J. S. (1983). Two-dimensional crystals formed from photosynthetic reaction centers. J. Cell Biol. 97, 1266–1270.CrossRefGoogle ScholarPubMed
Mullet, J. E., Burke, J. J. & Arntzen, C. J. (1980). Chlorophyll proteins of photosystem I. Plant Physiol. 65, 814–822.CrossRefGoogle ScholarPubMed
Nelson, D. R. & Robinson, N. C. (1983). Membrane proteins: a summary of known structural information. Meth. Enzymol. 97, 571–618.Google Scholar
Oesterhelt, D. & Stoeckenius, W. (1973). Functions of a new photoreceptor membrane. Proc. natn. Acad. Sci. U.S.A. 70, 2852–2857.CrossRefGoogle ScholarPubMed
Oesterhelt, D. & Stoeckenius, W. (1974). Isolation of the cell membrane from Halobacterium halobium and its fractionation into red and purple membrane. Meth. Enzymol. 31, 667–678.CrossRefGoogle ScholarPubMed
Paul, C. & Rosenbusch, J. P. (1985). Folding pattern of porin and bacteriorhodopsin. EMBO J. 4, 1593–1597.CrossRefGoogle ScholarPubMed
Rivas, E., Reiss-Husson, F. & le Maire, M. (1980). Physicochemical properties of detergent-solubilized photochemical reaction centres from two strains of Rhodopseudomonas sphaeroides. Biochemistry 19, 2943–2950.Google Scholar
Rosenbusch, J. P. (1974). Characterization of the major envelope protein from Escherichia coli. J. biol. Chem. 249, 8019–8029.Google Scholar
Saito, S. & Tsuchiya, T. (1984). Characteristics of n-octyl-β-D-thioglucopyranoside, a new non-ionic detergent useful for membrane biochemistry. Biochim.J. 222, 829–835.Google Scholar
Schatz, G. H. & Witt, H. T. (1982). Extraction and characterization of oxygen-evolving photosystem II complexes from a thermophilic cyanobacterium Synechococcus species. Photobiochem. Photobiophys. 7, 1–14.Google Scholar
Schleicher, A., Franke, R., Hofmann, K. P., Finkelmann, H. & Welte, W. (1987). Deoxylysolecithin and a new biphenyl detergent as solubilizing agents for bovine rhodopsin. Functional test by formation of metarhodopsin II and binding of Gprotein. Biochemistry 26, 5908–5916.Google Scholar
Seki, S., Hayashi, H. & Oda, T. (1970). Studies on cytochrome oxidase. I. Fine structure of cytochrome oxidase-rich submitochondrial membranes. Arch. Biochem. Biophys. 138, 110–121.Google Scholar
Stewart, A. C. & Bendall, D. S. (1979). Preparation of an active oxygen-evolving photosystem 2 particle from blue-green algae. FEBS Lett. 107, 308–312.Google Scholar
Tanford, C. (1980). The Hydrophobic Effect, 2nd edn. New York: John Wiley & Sons.Google Scholar
Teather, R. M., Bramhall, J.Riede, I., Wright, J. K., Fürst, M., Aichele, G., Wilhelm, U. & Overath, P. (1980). Lactose carrier protein of E. coli. Structure and expression of plasmides carrying the y gene of the lac operon. Eur. J. Biochem. 108, 223–231.Google Scholar
Thornber, J. P. (1975). Chlorophyll proteins: Light-harvesting and reaction centre components of plants. Ann. Rev. Plant Physiol. 26, 127–158.CrossRefGoogle Scholar
Traube, J. (1896). Über das molekulare Lösungsvolumen und Molekularvolumen organischer Verbindungen. Liebigs Annalen der Chemie 290, 43–122.Google Scholar
Unwin, P. N. T. & Zampighi, G. (1980). Structure of the junction between communicating cells. Nature 283, 545–549.Google Scholar
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
Wacker, T., Gad'on, N., Becker, A., Mäntele, W., Kreutz, W., Drews, G. & Welte, W. (1986). Crystallization and spectroscopic investigation with polarized light of the reaction centre-B875 light-harvesting complex from Rhodopseudomonas palustris. FEBS Lett. 197, 267–273.Google Scholar
Welte, W. & Wacker, T. (1988). Protein–detergent micellar solutions for the crystallization of a membrane protein. Some general approaches and experiences with the crystallization of pigment-protein complexes from purple bacteria. In Crystallization of Membrane Proteins (ed Michel, H.). Boca Raton, Florida, U.S.A.: CRC Press (in the press).Google Scholar
Welte, W., Wacker, T., Leis, M., Kreutz, W., Shiozawa, J., Gad'on, N. & Drews, G. (1985). Crystallizaton of the photosynthetic light-harvesting pigment-protein complex B800–850 of Rhodopseudomonas capsulata. FEBS Lett. 182, 260–264.Google Scholar
Welte, W., Wacker, T. & Becker, A. (1988). Crystallization and spectroscopic investigation of purple bacterial B800–850 and RC–B875 complexes. In Photosynthetic light-harvesting systems – structure and function (ed. Scheer, H. and Schneider, S.). Berlin: W. de Gruyter & Co.Google Scholar
Weltzien, H. U., Richter, G. & Faber, E. (1979). Detergent properties of watersoluble choline phosphatides. J. biol Chem. 254, 3652–3657.Google Scholar
Wennerström, H. & Lindmann, B. (1979). Micelles: physical chemistry of surfactant association. Physics Reports 52, 1–86.CrossRefGoogle Scholar
Wilson, I. A., Skehel, J. J. & Wiley, D. C. (1981). Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289, 366–378.CrossRefGoogle ScholarPubMed
Wingfield, P., Arad, T., Leonard, K., & Weiss, H. (1979). Membrane crystals of ubiquinone: cytochrome c reductase from Neurospora mitochondria. Nature 280, 696–697.Google Scholar
Witt, I., Witt, H. T., Gerken, S., Saenger, W., Dekker, J. P. & Rögner, M. (1987). Crystallization of rection center I of photosynthesis. Low-concentrations crystallization of photoactive protein complexes from the cyanobacterium Synechococcus sp. FEBS Lett. 221, 260–264.Google Scholar
Yeates, T. O., Komyia, H., Rees, D. C., Allen, J. P. & Feher, G. (1987). Structure of the reaction centre from Rhodobacter sphaeroides R-26: Membrane–protein interactions. Proc. natn. Acad. Sci. U.S.A. 84, 6438–6442.CrossRefGoogle ScholarPubMed
Yedgar, S., Barenholz, Y. & Cooper, V. G. (1974). Molecular weight, shape and structure of mixed micelles of Triton X-100 and sphingomyelin. Biochim. Biophys. Acta 363, 98–111.Google Scholar
Zulauf, M. (1988). Detergent phenomena in membrane protein crystallization. In Crystallization of Membrane Proteins (ed. Michel, H.). Boca Raton, Florida, U.S.A: CRC Press (in the press).Google Scholar
Zulauf, M., Timmins, P. A. & Garavito, R. M. (1986). Neutron crystallography of a membrane protein. Localization of detergent and protein at 20 Å resolution. Biophys. J. 49, 96–98.Google Scholar