Hostname: page-component-7479d7b7d-68ccn Total loading time: 0 Render date: 2024-07-08T17:30:12.191Z Has data issue: false hasContentIssue false
  • English
  • Français

Structure and dynamics of polypeptides and proteins in lipid membranes

Published online by Cambridge University Press:  17 March 2009

Horst Vogel
Horst Vogel
Affiliation:
Swiss Federal Institute of Technology, Lausanne
Get access Rights & Permissions [Opens in a new window]

Extract

The elucidation of the molecular mechanisms whereby ions and polar molecules are translocated across the hydrophobic barrier of a lipid bilayer in biological membranes is one of the most challenging problems in biological research. Specific membrane proteins, such as pumps, carriers and channels, play the central role in the various translocation pathways. Recent progress in expression cloning has provided the sequence of a number of biologically important membrane proteins and in principle the door is open to investigate every protein which might be of importance in the central signal transduction and transport processes. Unfortunately, to date there are only a few examples where the three-dimensional structure of membrane proteins are known at atomic resolution. The photosynthetic reaction centres from purple bacteria (Deisenhofer et al. 1985), bacteriorhodopsin (Henderson et al. 1990) and the large porin channel of Rhodobacter capsulata (Weiss et al. 1991). According to these structural data membrane proteins seem to fold in general in membrane-spanning α-helices and β-strands in order to saturate hydrogen bonds. Only these two motifs seem to form stable structures which can be in contact with the hydrophobic lipid interior of a membrane.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 25 , Issue 4 , November 1992 , pp. 433 - 457
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

Baenziger, J. E., Miller, K. W. & Rothschild, K. J. (1992). Incorporation of the nicotinic acetylcholine receptor into planar multilamellar films: characterization by fluorescence and Fourier transform infrared difference spectroscopy. Biophys. J. 61, 983–992.CrossRefGoogle ScholarPubMed
Birge, R. R. (1990). Photophysics and molecular electronic applications of the rhodopsins. Annu. Rev. phys. Chem. 41, 683–733.CrossRefGoogle ScholarPubMed
Boheim, G. & Kolb, A. (1978). Analysis of the multi-pore system of alamethicin in a lipid membrane: Voltage-jump current-relaxation experiments. J. Membrane Biol. 38, 99–150.CrossRefGoogle Scholar
Boheim, G., Jung, G. & Manestrina, G. (1987). α-Helical ion channels reconstituted into planar bilayers. In Ion Transport through Membranes, (ed. Yagi, K. and Pullman, B.). Tokyo: Academic Press. 131–145.Google Scholar
Braiman, M. S. & Rothschild, K. J. (1988). Fourier transform infrared techniques for probing membrane protein structure. Annu. Rev. Biophys. biophys. Chem. 17, 541–570.CrossRefGoogle ScholarPubMed
Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S. & Karplus, M. (1983). CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. comput. Chem. 4, 187–217.CrossRefGoogle Scholar
Chiu, S. W., Jakobsson, E., Subramaniam, S. & McCammon, J. A. (1991). Time-correlation analysis of simulated water motion in flexible and rigid gramicidin channels. Biophys. J. 60, 273–285.CrossRefGoogle ScholarPubMed
Chothia, C. (1984). Principles that determine the structure of proteins. Annu. Rev. Biochem. 53, 537–572.CrossRefGoogle ScholarPubMed
Chou, P. Y. & Fasman, G. D. (1978). Empirical predictions of protein conformation. Annu. Rev. Biochem. 47, 251–276.CrossRefGoogle ScholarPubMed
De Grado, W. F. & Lear, J. D. (1990). Conformational constrained α-helical peptide models for protein ion channels. Biopolymers 29, 205–213.CrossRefGoogle ScholarPubMed
Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. (1985). Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618–624.CrossRefGoogle Scholar
Dornmair, K. & Jähnig, F. (1989). Internal dynamics of lactose permease. Proc. natl. Acad. Sci. U.S.A. 86, 9827–9831.CrossRefGoogle ScholarPubMed
Dorset, D. L., Engel, A., Haener, M., Massalski, A. & Rosenbusch, J. P. (1983). Two-dimensional crystal packing of matrix porin. A channel forming protein in Escherichia coli outer membrane. J. mol. Biol. 165, 701–710.CrossRefGoogle Scholar
Ehrenberg, M. & Rigler, R. (1972). Polarized fluorescence and rotational Brownian motion. Chem. Phys. Lett. 14, 539–544.CrossRefGoogle Scholar
Eisenberg, D., Weiss, R. M. & Terwilliger, T. C. (1984). The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. natl. Acad. Sci. U.S.A. 81, 140–144.CrossRefGoogle ScholarPubMed
Esposito, G., Carver, J. A., Boyd, J. & Campbell, I. D. (1987). High-resolution 1H NMR study of the solution structure of alamethicin. Biochemistry 26, 1043–1050.CrossRefGoogle ScholarPubMed
Finer-Moore, J. & Stroud, R. M. (1984). Amphipathic analysis and possible formation of the ion channel in an acetylcholine receptor. Proc. natl. Acad. Sci. U.S.A. 81, 155–159.CrossRefGoogle Scholar
Frauenfelder, H., Parak, F. & Young, R. D. (1988). Conformational substrates in proteins. Annu. Rev. Biophys. biophys. Chem. 17, 451–479.CrossRefGoogle ScholarPubMed
Galzi, J. L., Revah, F., Bessis, A. & Changeux, J. P. (1991). Functional architecture of the nicotinic acetylcholine receptor: From electric organ to brain. Annu. Rev. Pharmacol. 31, 37–72.CrossRefGoogle ScholarPubMed
Ghosh, P. & Stroud, R. M. (1991). Ion channels by a highly charged peptide. Biochemistry 30, 3551–3557.CrossRefGoogle ScholarPubMed
Haas, E., Wilchek, M., Katchalski-Katzir, E. & Steinberg, I. Z. (1975). Distribution of end-to-end distances of oligopeptides in solution as estimated by energy transfer. Proc. natl. Acad. Sci. U.S.A. 72, 1807–1811.CrossRefGoogle ScholarPubMed
Hanke, W. & Boheim, G. (1980). The lowest conductance state of the alamethicin pore. Biochim. biophys. Acta 596, 456–462.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 cryomicroscopy. J. mol. Biol. 213, 899–929.CrossRefGoogle Scholar
Hennessy, J. P. & Johnson, W. C. Jr. (1981). Information content in the circular dichroism of proteins. Biochemistry 20, 1085–1094.CrossRefGoogle Scholar
Jung, G., Franz, B., Boheim, G., Helbig, I., Meder, S., Nilsson, L., Rigler, R. & Vogel, H. (1989). Synthetic helical polypeptides model the acetylcholine receptor channel function.Proceedings of the 3rd Akobari Conference. (ed. Wünsch, E.) 140–145.Google Scholar
Kaback, H. R., Bibi, E. & Roepe, P. D. (1990). β-Galactoside transport in E. coli: a functional dissection of lac permease. Trends biochem. Sci. 15, 309–314.CrossRefGoogle Scholar
Karplus, M. & Petsko, G. A. (1990). Molecular dynamics simulation in biology. Nature 347, 631–639.CrossRefGoogle ScholarPubMed
Krimm, S. & Bandekar, I. (1986). Vibrational spectroscopy and conformation of peptides, polypeptides and proteins. Adv. Protein Chem. 38, 183–364.Google ScholarPubMed
Kyte, J. & Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J. mol. Biol. 157, 105–132.CrossRefGoogle ScholarPubMed
Lakowicz, J. R., Gryczynski, I., Wiczk, W., Laczko, G., Prendergast, F. C. & Johnson, M. L. (1990). Conformational distributions of melittin in water/methanol mixtures from frequency-domain measurements of nonradiative energy transfer. Biophys. Chem. 36, 99–115.CrossRefGoogle ScholarPubMed
Langosch, D., Hartung, K., Grell, E., Bamberg, E. & Betz, H. (1991). Ion channel formation by synthetic transmembrane segments of the inhibitory glycine receptor – a model study. Biochim. biophys. Acta 1063, 36–44.CrossRefGoogle ScholarPubMed
Lear, J. D., Wasserman, Z. R. & de Grado, W. F. (1988). Synthetic amphiphilic peptide models for protein ion channels. Science 240, 1177–1181.CrossRefGoogle ScholarPubMed
Lee, D. C., Harris, P. I., Chapman, D. & Mitchell, R. C. (1991). Quantitative determination of the secondary structure of soluble and membrane proteins from factor analysis of infrared spectra. In Spectroscopy of Biological Molecules, (ed. Hester, R. E. and Girling, R. B.). The Royal Society of Chemistry pp.7–10.Google Scholar
MacArthur, M. W. & Thornton, J. M. (1991). Influence of proline residues on protein conformation. J. mol. Biol. 218, 397–412.CrossRefGoogle ScholarPubMed
Manestrina, G., Voges, K. P., Jung, G. & Boheim, G. (1986). Voltage-dependent channel formation by rods of helical polypeptides. J. Membrane Biol. 93, 111–132.CrossRefGoogle Scholar
Montal, M., Montal, M. S. & Tomich, J. M. (1990). Synporins – synthetic proteins that emulate the pore structure of biological ionic channels. Proc. natl. Acad. Sci. U.S.A. 87, 6929–6933.CrossRefGoogle ScholarPubMed
Morona, R., Krämer, C. & Henning, U. (1985). Bacteriophage receptor area of outer membrane protein OmpA of Escherichia coli K-12. J. Bacteriol. 164, 539–543.CrossRefGoogle ScholarPubMed
Nikaido, H. & Vaara, M. (1985). Molecular basis of bacterial outer membrane permeability. Mikrobiol. Rev. 49, 1–32.Google ScholarPubMed
Oiki, S., Danho, W. & Montal, M. (1988). Channel protein engineering: Synthetic 22-mer peptide from the primary structure of the voltage-sensitive sodium channel from ionic channels in lipid bilayers. Proc. natl. Acad. U.S.A. 85, 2393–2397.CrossRefGoogle ScholarPubMed
Oiki, S., Madison, V. & Montal, M. (1990). Bundles of amphipathic transmembrane α-helices as a structural motif for ion-conducting channel proteins: Studies on sodium channels and acetylcholine receptors. Proteins 8, 226–236.CrossRefGoogle ScholarPubMed
Opella, S. J., Stewart, P. L. & Valentine, K. G. (1987). Protein structure by solidstate NMR spectroscopy. Q. Rev. Biophys. 19, 7–49.CrossRefGoogle ScholarPubMed
Pastore, A., Harvey, T. S., Dempsey, C. E. & Campbell, I. D. (1989). The dynamic properties of melittin in solution. Europ. Biophys. J. 16, 363–367.CrossRefGoogle ScholarPubMed
Piela, L., Nemethy, G. & Scheraga, H. A. (1987). Proline-induced constraints in α-helices. Biopolymers 26, 1587–1600.CrossRefGoogle ScholarPubMed
Provencher, S. W. (1982). A constrained regularization method for inverting data represented by linear algebraic or integral equations. Comp. Phys. Commun. 27, 213–227.CrossRefGoogle Scholar
Provencher, S. W. & Glöckner, I. (1981). Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20, 33–37.CrossRefGoogle ScholarPubMed
Roepe, P. D. & Kaback, H. R. (1989). Site-directed mutagenesis of tyrosine residues in the lac permease of Escherichia coli. Biochemistry 28, 6127–6132.Google Scholar
Sakmann, B. (1992). Elementary steps in synaptic transmission revealed by currents through single ion channels. Science 256, 503–512.CrossRefGoogle ScholarPubMed
Shon, K., Kim, Y., Colnago, L. A. & Opella, S. J. (1991). NMR studies of the structure and dynamics of membrane-bound bacteriophage Pf1 coat protein. Science 252, 1303–1305.CrossRefGoogle ScholarPubMed
Steven, A. C., Ten Heggeler, B., Mueller, R., Kistler, I. & Rosenbusch, J. P. (1977). Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli. J. Cell Biol. 72, 292–301.CrossRefGoogle ScholarPubMed
Stroud, R. M., McCarthy, M. P. & Shuster, M. (1990). Nicotinic acetylcholine receptor superfamily of ligand-gated ion channels. Biochemistry 29, 11009–11023.CrossRefGoogle ScholarPubMed
Sugawara, E. & Nikaido, H. (1992). Pore-forming activity of OmpA protein of Escherichia coli. J. biol. Chem. 267, 2507–2511.CrossRefGoogle ScholarPubMed
Surewicz, W. K. & Mantsch, H. H. (1988). New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. biophys. Acta 952, 115–130.CrossRefGoogle ScholarPubMed
Szabo, A. (1984). Theory of fluorescence depolarization in macromolecules and membranes. J. chem. Phys. 81, 150–167.CrossRefGoogle Scholar
Thiaudière, E., Siffert, O., Talbot, J. C., Bolard, J., Alouf, J. E. & Dufourcq, J. (1991). The amphiphilic α-helix concept. Consequences in the structure of δ-toxin in solution and bound to lipids. Eur. J. Biochem. 195, 203–213.CrossRefGoogle ScholarPubMed
Tomita, M. & Marchesi, V. T. (1975). Amino-acid sequence and oligosaccaride attachment sites of human erythrocyte glycophorin. Proc. natl. Acad. Sci. U.S.A. 72, 2964–2968.CrossRefGoogle Scholar
Treutlein, H., Schulten, K., Brunger, A. T., Karplus, M., Deisenhofer, J. & Michel, H. (1992). Chromophore-protein interactions and function of the photosynthetic reaction center: A molecular dynamics study. Proc. natl. Acad. Sci. U.S.A. 89, 75–79.CrossRefGoogle ScholarPubMed
Van der Meer, W., Pottel, H., Herremann, W., Ameloot, M., Hendrickx, H. & Schroeder, H. (1984). Effect of orientational order on the decay of the fluorescence anisotropy in membrane suspensions. A new approximate solution of the rotational diffusion equation. Biophys. J. 46, 515–523.CrossRefGoogle ScholarPubMed
Vogel, H. (1987). Comparison of the conformation and orientation of alamethicin and melittin in lipid membranes. Biochemistry 26, 4562–4572.CrossRefGoogle ScholarPubMed
Vogel, H. & Gärtner, W. (1987). The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy. J. biol. Chem. 262, 11464–11469.CrossRefGoogle ScholarPubMed
Vogel, H. & Jähnig, F. (1986 a). Models for the structure of outer-membrane proteins of Escherichia coli derived from Raman spectroscopy and prediction methods. J. mol. Biol. 190, 191–199.CrossRefGoogle ScholarPubMed
Vogel, H. & Jähnig, F. (1986 b). The structures of melittin in membranes. Biophys. J. 50, 573–582.CrossRefGoogle ScholarPubMed
Vogel, H. & Rigler, R. (1987). Orientational fluctuations of melittin in lipid membranes as detected by time-resolved fluorescence anisotropy measurements. In Structure, Dynamics and Function of Biomolecules. (ed. Ehrenberg, A., Rigler, R., Gräslund, A. & Nilsson, L.) pp. 289–294, Berlin: Springer Verlag.CrossRefGoogle Scholar
Vogel, H., Wright, J. K. & Jähnig, F. (1985). The structure of the lactose permease derived from Raman spectroscopy and prediction methods. EMBO J. 4, 3625–3631.CrossRefGoogle ScholarPubMed
Vogel, H., Nilsson, L., Rigler, R., Voges, K. P. & Jung, G. (1988). Structural fluctuations of a helical polypeptide traversing a lipid bilayer. Proc. natl. Acad. Sci. U.S.A. 85, 5067–5071.CrossRefGoogle ScholarPubMed
Vogel, H., Nilsson, L., Thyberg, P., Rigler, R., Franz, B. & Jung, G. (1989). Structure and dynamics of membrane-spanning helices. Proceedings of the 3rd European Conference on Spectroscopy of Biological Molecules. (ed. Bertoluzza, A., Fagnano, C. and Monti, P.) pp. 219–222.Google Scholar
Vogel, H., Nilsson, L., Rigler, R., Meder, S., Boheim, G., Kurth, H. H. & Jung, G. (1992). Structural fluctuations between two conformational states of a transmembrane helical peptide are related to its channel forming properties in planar lipid membranes. (Submitted).Google Scholar
Voges, K. P., Jung, G. & Sawyer, W. H. (1987). Depth-dependent fluorescent quenching of a tryptophan residue located at defined positions on a rigid 21-peptide helix in liposomes. Biochim. biophys. Acta 896, 64–76.CrossRefGoogle ScholarPubMed
Heijne, Von (1991). Proline kinks in transmembrane α-helices. J. mol. Biol. 218, 499–503.CrossRefGoogle Scholar
Weiss, M. S., Kreusch, A., Schiltz, E., Nestel, U., Welte, W., Weckesser, I. & Schultz, G. E. (1991). The structure of porin from Rhodobacter capsulatus at 1·8 Å resolution. FEBS Lett. 280, 379–382.CrossRefGoogle ScholarPubMed
Williams, A. F. & Beyers, D. (1992). At grips with interactions. Nature 356, 746–747.CrossRefGoogle ScholarPubMed
Williams, K. A. & Deber, C. M. (1991). Proline residues in transmembrane helices: Structural dynamic role? Biochemistry 30, 8919–8923.CrossRefGoogle ScholarPubMed
Williams, R. W. (1983). Estimation of protein secondary structure from the laser Raman amide. I. Spectrum. J. mol. Biol. 166, 581–603.CrossRefGoogle ScholarPubMed
Williams, R. W. (1986). Protein secondary structure analysis using Raman amide I and amide III. Spectra. Methods Enzymol. 130, 311–331.CrossRefGoogle ScholarPubMed
Williams, R. W., Starman, R., Taylor, K. M. P., Gable, K., Beeler, T., Zasloff, M. & Covell, D. (1990). Raman spectroscopy of synthetic antimicrobial frog peptides magainin 2a and PGLa. Biochemistry 29, 4490–4496.CrossRefGoogle ScholarPubMed
Yamamoto, T., Davis, C. G., Brown, M. S., Schneider, W. J., Casey, M. L., Goldstein, I. L. & Russell, D. W. (1984). The human LDL receptor: A cysteinerich protein with multiple Alu sequences in its mRNA. Cell 39, 27–38.CrossRefGoogle ScholarPubMed