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Magic angle spinning NMR spectroscopy of membrane proteins

Published online by Cambridge University Press:  17 March 2009

Steven O. Smith ,
Kathryn. Aschheim  and
Michel Groesbeek
Steven O. Smith
Affiliation:
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520–8114
Kathryn. Aschheim
Affiliation:
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520–8114
Michel Groesbeek
Affiliation:
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520–8114
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Extract

The passage of molecules and information across cell membranes is mediated largely by membrane-spanning proteins acting as channels, pumps, receptors and enzymes. These proteins perform many tasks: they control electrochemical gradients across the membrane, receive signals from the environment or from other cells, convert light energy into chemical signals, transport small molecules into and out of cells, and harness proton gradients to generate the energy consumed in metabolism. Indeed, of the estimated 50000–100000 genes in the human genome, fully 20–40 % are thought to encode integral membrane proteins. If one also includes membrane-associated proteins, which are attached to the membrane surface through fatty acyl chains or electrostatic interactions, this percentage is likely to be much higher.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 29 , Issue 4 , December 1996 , pp. 395 - 449
Copyright
Copyright © Cambridge University Press 1996

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References

Abragam, A. (1961). The Principles of Nuclear Magnetism. Oxford: Clarendon Press.Google Scholar
Allen, J. P., Feher, G., Yeates, T. O., Komiya, H. & Rees, D. C. (1987 a). Structure of the reaction centre from Rhodobacter sphaeroides R-26: the cofactors. Proc. Natl. Acad. Sci. USA 84, 5730–5734.CrossRefGoogle ScholarPubMed
Allen, J. P., Feher, G., Yeates, T. O., Komiya, H. & Rees, D. C. (1987 b). Structure of the reaction centre from Rhodobacter sphaeroides R-26: the protein subunits. Proc. Natl. Acad. Sci. USA 84, 6162–6166.CrossRefGoogle ScholarPubMed
Andrew, E. R., Bradbury, A. & Eades, R. G. (1958). Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182, 1659.CrossRefGoogle Scholar
Andrew, E. R. & Szczesniak, E. (1995). A historical account of NMR in the solid state. Progress in NMR Spectroscopy 28, 11–36.CrossRefGoogle Scholar
Antzutkin, O. N., Shekar, S. & Levitt, M. H. (1995). Two-dimensional sideband separation in magic angle spinning NMR. J. Magn. Reson. A 115, 7–15.CrossRefGoogle Scholar
Antzutkin, O. N., Song, Z., Feng, X. & Levitt, M. H. (1995). Suppression of sidebands in magic angle spinning NMR: general principles and analytical solutions. J. Chem. Phys. 100, 130–140.CrossRefGoogle Scholar
Baldus, M. & Meier, B. H. (1996). Total correlation spectroscopy in the solid state: the use of J-couplings to determine the through-bond connectivity. J. Magn. Reson. A121, 65–69.CrossRefGoogle Scholar
Baldwin, J. M. (1993) The probable arrangement of the helices in G-protein coupled receptors. EMBO J. 12, 1693–1703.CrossRefGoogle ScholarPubMed
Bargmann, C. I., Hung, M.-C. & Weinberg, R. A. (1986 a). Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of P185. Cell 45, 649–657.CrossRefGoogle ScholarPubMed
Bargmann, C. I., Hung, M.-C. & Weinberg, R. A. (1986 b). The neu oncogene encodes an epidermal growth factor receptor-related protein. Nature 319, 226–230.CrossRefGoogle ScholarPubMed
Barlow, D. J. & Thorton, J. M. (1988). Helix geometry in proteins. J. Mol. Biol. 201, 601–619.CrossRefGoogle ScholarPubMed
Bennett, A. E., Ok, J. H., Griffin, R. G. & Vega, S. (1992). Chemical shift correlation spectroscopy in rotating solids: radio frequency-driven dipolar recoupling and longitudinal exchange. J. Chem. Phys. 96, 8624–8627.CrossRefGoogle Scholar
Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V. & Griffin, R. G. (1996). Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103, 6951–6958.CrossRefGoogle Scholar
Bogomolni, R. A., Stubbs, L. & Lanyi, J. K. (1978). Illumination dependent changes in the intrinsic fluorescence of bacteriorhodopsin. Biochemistry 17, 1037–1041.CrossRefGoogle ScholarPubMed
Bormann, B. J., Knowles, W. J. & Marchesi, V. T. (1989). Synthetic peptides mimic the assembly of transmembrane glycoproteins. J. Biol. Chem. 264, 4033–4037.CrossRefGoogle ScholarPubMed
Bouchard, M., Davis, J. H. & Auger, M. (1995). High-speed MAS solid state 1H NMR study of the conformation of gramicidin A in lipid bilayers. Biophys.J. 69, 1933–1938.CrossRefGoogle 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
Brandl, C. J. & Deber, C. M. (1986). Hypothesis about the function of membraneburied proline residues in transport proteins. Proc. Natl. Acad. Sci. USA 83, 917–921.CrossRefGoogle ScholarPubMed
Brown, L. S., Sasaki, J., Kandori, H., Maeda, A., Needleman, R. & Lanyi, J. K. (1995). Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270, 27122–27126.CrossRefGoogle ScholarPubMed
Brudler, R., De Groot, H. J. M., Van Liemt, W. B. S., Steggerda, W. F., Esmeijer, R., Gast, P., Hoff, A. J., Lugtenburg, J. & Gewert, K. (1994). Asymmetric binding of the 1 - and 4−13 C = O groups of QA in Rhodobacter sphaeroides R26 reaction centres monitored by Fourier transform infra-red spectroscopy using site-specific isotopically labelled ubiquinone-10. EMBO J. 13, 5523–5530.CrossRefGoogle Scholar
Burum, D. P. & Bielecki, A. (1991). An improved experiment for heteronuclear correlation 2D NMR in solids. J. Magn. Reson. 94, 645–652.Google Scholar
Christensen, A. M. & Schaefer, J. (1993). Solid state NMR determination of intramolecular 31P−13C distances for shikimate 3-phosphate. Biochemistry 32, 2868–2873.CrossRefGoogle ScholarPubMed
Cosson, P. & Bonifacino, J. S. (1992). Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 258, 659–662.CrossRefGoogle ScholarPubMed
Cosson, P., Lankford, S. P., Bonifacino, J. S. & Klausner, R. D. (1991). Membrane protein association by potential intramembrane charge pairs. Nature 351, 414–416.CrossRefGoogle ScholarPubMed
Cowan, S. W. (1993). Bacterial porins: lessons from three high-resolution structures. Curr. Opin. Struct. Biol. 3, 501–507.CrossRefGoogle Scholar
Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., Jansonius, J. N. & Rosenbusch, J. P. (1992). Crystal structures explain functional properties of two E. coli porins. Nature 358, 727–733.CrossRefGoogle ScholarPubMed
Creuzet, F., McDermott, A., Gebhard, R., Van Der Hoef, K., Spijker-Assink, M. B., Herzfeld, J., Lugtenburg, J., Levitt, M. H. & Griffin, R. G. (1991). Determination of membrane protein structure by rotational resonance NMR: bacteriorhodopsin. Science 251, 783–786.CrossRefGoogle ScholarPubMed
Cross, T. A. (1994). Structural biology of peptides and proteins in synthetic membrane environments by solid state NMR spectroscopy. Annual Reports on NMR Spectroscopy 29, 123–167.CrossRefGoogle Scholar
Cross, T. A. & Opella, S. J. (1994). Solid state NMR structural studies of peptides and proteins in membranes. Curr. Opin. Struct. Biol. 4, 574–581.CrossRefGoogle Scholar
Davis, J. H., Auger, M. & Hodges, R. S. (1995). High-resolution 1H NMR of a transmembrane peptide. Biophys. J. 69, 1917–1932.CrossRefGoogle ScholarPubMed
De Groot, H. J. M., Copié, V., Smith, S. O., Allen, P. J., Winkel, C., Lugtenburg, J., Herzfeld, J. & Griffin, R. G. (1988). Magic-angle-sample-spinning NMR difference spectroscopy. J. Magn. Reson. 77, 251–257.Google Scholar
De Groot, H. J. M., Harbison, G. S., Herzfeld, J. & Griffin, R. G. (1989). NMR study of the Schiff base in bacteriorhodopsin: counterion effects on the 15-N shift anisotropy. Biochemistry 28, 3346–3353.CrossRefGoogle Scholar
De Groot, H. J. M., Gebhard, G., Van Den Hoef, I., Hoff, A. J., Lugtenburg, J., Violette, C. A. & Frank, H. A. (1992). 13C magic angle spinning NMR evidence for a 15, 15′-cis configuration of the spheroidene in the Rhodobacter sphaeroides photosynthetic reaction centre. Biochemistry 31, 12446–12450.CrossRefGoogle Scholar
Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. (1984). X-ray structure analysis of a membrane protein complex. J. Mol. Biol. 180, 385–398.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
Dixon, W. T., Schaefer, J., Sefcik, M. D., Stejskal, E. O. & McKay, R. A. (1982). Total suppression of side bands in CPMAS C-13 NMR. J. Magn. Reson. 49, 341–345.Google Scholar
Dollinger, G., Eienstein, L., Lin, S. L., Nakanishi, K. & Termini, J. (1986). Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts regenerated with deuterated tyrosine. Biochemistry 25, 6524–6533.CrossRefGoogle ScholarPubMed
Doukas, A. G., Pande, A., Suzuki, T., Callender, R. H., Honig, B. & Ottolenghi, M. (1981). On the mechanism of hydrogen-deuterium exchange in bacteriorhodopsin. Biophys. J. 33, 275–280.CrossRefGoogle ScholarPubMed
Engelhard, M., Hess, B., Emeis, D., Metz, G., Kreutz, W. & Siebert, F. (1989). Magic angle sample spinning 13C nuclear magnetic resonance of isotopically labelled bacteriorhodopsin. Biochemistry 28, 3967–3975.CrossRefGoogle ScholarPubMed
Engelhard, M., Hess, B., Metz, G., Kreutz, W., Siebert, F., Soppa, J. & Oesterhelt, D. (1990). High-resolution 13-C-solid state NMR of bacteriorhodopsin: assignment of specific aspartic acids and structural implications of single site mutations. Eur. Biophys. J. 18, 17–24.CrossRefGoogle Scholar
Engelman, D. M., Steitz, T. A. & Goldman, A. (1986). Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15, 321–353.CrossRefGoogle ScholarPubMed
Ernst, R. R., Bodenhausen, G. & Wokaun, A.. (1987). Principles of Nuclear Magnetic Resonance in One and Two Dimensions. Clarendon Press, Oxford.Google Scholar
Facelli, J. C., Grant, D. M. & Michl, J. (1987). Carbon-13 shielding tensors: Experimental and theoretical determination. Ace. Chem. Res. 20, 152–158.CrossRefGoogle Scholar
Fujiwara, T., Ramamoorthy, A., Nagayama, K., Hioka, K. & Fujito, T. (1993). Dipolar HOHAHA under MAS conditions for solid state NMR. Chem. Phys. Lett. 212, 81–84.CrossRefGoogle Scholar
Furthmayr, H. & Marchesi, V. T. (1976). Subunit structure of human erythrocyte glycophorin A. Biochemistry 15, 1137–1144.CrossRefGoogle ScholarPubMed
Galzi, J.-L. & Changeux, J.-P. (1994). Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr. Opin. Struct. Biol. 4, 554–565.CrossRefGoogle Scholar
Ganter, U. M., Schmid, E. D., Perez-Sala, D., Rando, R. R. & Siebert, F. (1989). Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier transform infrared and biochemical investigation. Biochemistry 28, 5954–5962.CrossRefGoogle ScholarPubMed
Garavito, R. M., Picot, D. & Loll, P. J. (1996). Strategies for crystallizing membrane proteins. J. Bioenerg. Biomemb. 28, 13–27.CrossRefGoogle ScholarPubMed
Garbow, J. & Gullion, T. (1995). Carbon-13 NMR Spectroscopy of Biological Systems. San Diego: Academic Press.Google Scholar
Garbow, J. R. & McWherter, C. A. (1993). Determination of the molecular conformation of melanostatin using 13C-15N REDOR NMR spectroscopy. J. Am. Chem. Soc. 115, 238–244.CrossRefGoogle Scholar
Gennis, R. B. (1989). Biomembranes: Molecular Structure and Function. New York: Springer-Verlag.CrossRefGoogle Scholar
Gerfen, G. J., Becerra, L. R., Hall, D. A., Singel, D. J. & Griffin, R. G. (1995). High frequency (140 GHz) dynamic nuclear polarization: polarization transfer to a solute in a frozen aqueous solution. J. Chem. Phys. 102, 9494–9497.CrossRefGoogle Scholar
Gerwert, K., Hess, B. & Engelhard, M. (1990). Proline residues undergo structural changes during proton pumping in bacteriorhodopsin. FEBS Lett. 261, 449–454.CrossRefGoogle Scholar
Girvin, M. E. & Fillingame, R. H. (1993). Helical structure and folding of subunit c of FiFo ATP synthase: 1H NMR resonance assignments and NOE analysis. Biochemistry 32, 12167–12177.CrossRefGoogle Scholar
Gouaux, E. (1996). Structure and function of alpha-hemolysin: a heptameric transmembrane pore. Biophys. J. 70, A121.Google Scholar
Gouaux, J. E., Braha, O., Hobaugh, M. R., Song, L., Cheley, S., Shustak, C. & Bayley, H. (1994). Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc. Natl. Acad. Sci. USA 91, 12828–12831.CrossRefGoogle ScholarPubMed
Gregory, D. M., Mitchell, D. J., Stringer, J. A., Kiihne, S., Shiels, J. C., Callahan, J., Mehta, M. A. & Drobny, G. P. (1995). Windowless dipolar recoupling: the detection of weak dipolar couplings between spin 1/2 nuclei with large chemical shift anisotropies. Chem. Phys. Lett. 246, 654–663.CrossRefGoogle Scholar
Griffiths, J. M. & Griffin, R. G. (1993). Nuclear magnetic resonance methods for measuring dipolar couplings in rotating solids. Anal. Chim. Acta 283, 1081–1101.CrossRefGoogle Scholar
Griffiths, J. M., Lakshmi, K. V., Bennett, A. E., Raap, J., Van Der Wielen, C. M., Lugtenburg, J., Herzfeld, J. & Griffin, R. G. (1994). Dipolar correlation NMR spectroscopy of a membrane protein. J. Am. Chem. Soc. 116, 10178–10181.CrossRefGoogle Scholar
Grigorieff, N., Ceska, T. A., Downing, K. H., Baldwin, J. M. & Henderson, R. (1996). Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259, 393–421.CrossRefGoogle ScholarPubMed
Gross, J. D., Costa, P. R., Dubacq, J. P., Warschawski, D. E., Lirsac, P. N., Devaux, P. F. & Griffin, R. G. (1995). Multidimensional NMR in lipid systems. Coherence transfer through J couplings under MAS. J. Magn. Reson. B106, 187–190.CrossRefGoogle Scholar
Gu, Z., Zambrano, R. & McDermott, A. (1994). Hydrogen-bonding of carboxyl groups in solid state amino acids and peptides: comparison of carbon chemical shielding, infrared frequencies, and structures. J. Am. Chem. Soc. 116, 6368–6372.CrossRefGoogle Scholar
Gullion, T. (1995 a). Detecting 13C−17O dipolar interactions by rotation-echo, adiabatic-passage, double resonance NMR. J. Magn. Reson. A117, 326–329.CrossRefGoogle Scholar
Gullion, T. (1995 b). Measurement of dipolar interactions between spin-1/2 and quadrupolar nuclei by rotational, adiabatic passage, double-resonance NMR. Chem. Phys. Letters 246, 325–330.CrossRefGoogle Scholar
Gullion, T. & Schaefer, J. (1989 a). Detection of weak heteronuclear dipolar coupling by rotational echo double-resonance nuclear magnetic resonance. Adv. Magn. Reson. 13, 57–83.CrossRefGoogle Scholar
Gullion, T. & Schaefer, J. (1989 b). Rotational-echo double-resonance NMR. J. Magn. Reson. 81, 196–200.Google Scholar
Gullion, T. & Vega, S. (1992). A simple magic angle spinning NMR experiment for the dephasing of rotational echoes of dipolar coupled homonuclear spin pairs. Chem. Phys. Letters 194, 423–428.CrossRefGoogle Scholar
Han, M. & Smith, S. O. (1995). NMR constraints on the location of the retinal chromophore in rhodopsin and bathorhodopsin. Biochemistry 34, 1425–1432.CrossRefGoogle ScholarPubMed
Han, M., Dedecker, B. S. & Smith, S. O. (1993). Localization of the retinal protonated Schiffs base counterion in rhodopsin. Biophys. J. 65, 899–906.CrossRefGoogle ScholarPubMed
Han, B.-G., Vonck, J. & Glaeser, R. M. (1994). The bacteriorhodopsin photocycle: direct structural study of two substates of the M-intermediate. Biophys. J. 67, 1179–1186.CrossRefGoogle Scholar
Han, M., Lin, S. W., Smith, S. O. & Sakmar, T. P. (1996 a). The effects of amino acid replacements of glycine 121 on transmembrane helix 3 of rhodopsin. J. Biol. Chem. in press.CrossRefGoogle Scholar
Han, M., Lin, S. W., Minkova, M., Smith, S. O. & Sakmar, T. P. (1996 b). Functional helix-helix interactions in rhodopsin: replacement of phenylalanine 261 by alanine causes reversion of phenotype of a glycine 121 replacement mutant. J. Biol. Chem. in press.Google Scholar
Harbison, G. S., Herzfeld, J. & Griffin, R. G. (1983). Solid state nitrogen-15 NMR study of the Schiff's base in bacteriorhodopsin. Biochemistry 22, 1–5.CrossRefGoogle ScholarPubMed
Harbison, G. S., Roberts, J. E., Herzfeld, J. & Griffin, R. G. (1988). Solid state NMR detection of proton exchange between bacteriorhodopsin Schiff base and bulk water. J. Am. Chem. Soc. 110, 7221–7223.CrossRefGoogle Scholar
Hartmann, S. R. & Hahn, E. L. (1962). Nuclear double resonance in the rotating frame. Phys. Rev. 128, 2042–2053.CrossRefGoogle Scholar
Hediger, S., Meier, B. & Ernst, R. R. (1995). Rotor-synchronized amplitude-modulated NMR spin-lock sequences for improved cross polarization under fast magic angle spinning. J. Chem. Phys. 102, 4000–4008.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
Henry, G. D. & Sykes, B. D. (1994). Methods to study membrane protein structure. Methods in Enzymology 239C, 515–535.CrossRefGoogle Scholar
Herzfeld, J. & Berger, A. E. (1980). Sideband intensities in NMR spectra of samples spinning at the magic angle. J. Chem. Phys. 73, 6021–6030.CrossRefGoogle Scholar
Herzfeld, J., Das Gupta, S. K., Farrar, M. R., Harbison, G. S., McDermott, A. E., Pelletier, S. L., Raleigh, D. P., Smith, S. O., Winkel, C., Lugtenburg, J. & Griffin, R. G. (1990). Solid state 13C NMR study of tyrosine protonation in darkadapted bacteriorhodopsin. Biochemistry 29, 5567–5574.CrossRefGoogle ScholarPubMed
Hing, A. W., Vega, S. & Schaefer, J. (1992). Transferred-echo double resonance NMR. J. Magn. Reson. 96, 205–209.Google Scholar
Hing, A. W., Vega, S. & Schaefer, J. (1993). Measurement of heteronuclear dipolar coupling by transferred-echo double resonance NMR. J. Magn. Reson. 103, 151–162.CrossRefGoogle Scholar
Hing, A. W., Tjandra, N., Cottam, P. F., Schaefer, J. & HO, C. (1994). An investigation of the ligand-binding site of the glutamine-binding protein of E. coli using rotational-echo double-resonance NMR. Biochemistry 33, 8651–8661.CrossRefGoogle ScholarPubMed
Hong, J. & Harbison, G. S. (1993). MAS sideband elimination by temporary interruption of the chemical shift. J. Magn. Reson. A105, 128–136.CrossRefGoogle Scholar
Honig, B. H. & Hubbell, W. L. (1984). Stability of ‘salt bridges’ in membrane proteins. Proc. Natl. Acad. Sci. USA 81, 5412–5416.CrossRefGoogle ScholarPubMed
Hu, J. G., Sun, B. Q., Bizounok, M., Griffin, R. G. & Herzfeld, J. (1995 a). Solid state NMR detection of backbone structural change in the bacteriorhodopsin photocycle. Biophys. J. 68, A332.Google Scholar
Hu, J. G., Petkova, A. T., Sun, B. Q., Bizounok, M., Raap, J., Lugtenburg, J., Griffin, R. G. & Herzfeld, J. (1996). Solid state NMR studies of bacteriorhodopsin photointermediates.7th International Conference on Retinal Proteins 11,Zichron Yaacov, Israel.Google Scholar
Hu, J. Z., Wang, W., Liu, F., Solum, M. S., Alderman, D. W., Pugmire, R. J. & Grant, D. M. (1995 b). Magic-angle-turning experiments for measuring chemical shift tensor principal values in powdered solids. J. Magn. Reson. A113, 210–222.CrossRefGoogle Scholar
Hynes, N. E. & Stern, D. F. (1994). The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta 1198, 165–184.Google ScholarPubMed
Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660–669.CrossRefGoogle ScholarPubMed
Jap, B. K. (1988). High-resolution electron diffraction of reconstituted PhoE porin. J. Mol. Biol. 199, 229–231.CrossRefGoogle ScholarPubMed
Jarvie, T. P., Went, G. T. & Mueller, K. T. (1996). Simultaneous multiple distance measurements in peptides via solid state NMR. J. Am. Chem. Soc. 118, 5330–5331.CrossRefGoogle Scholar
Jeener, J. (1971). Ampere International Summer School, Basko Polje, Yugoslavia, unpublished.Google Scholar
Joers, J., Rosanske, R., Gullion, T. & Garbow, J. (1994). Detection of dipolar interactions by Crown NMR. J. Magn. Reson. A106, 123–126.CrossRefGoogle Scholar
Kantor, H. L. & Prestegard, J. H. (1978). Fusion of phosphatidylcholine bilayer vesicles: role of free fatty acid. Biochemistry 17, 3592–3597.CrossRefGoogle ScholarPubMed
Ketchem, R. R., Hu, W. & Cross, T. A. (1993). High-resolution conformation of gramicidin A in a lipid bilayer by solid state NMR. Science 261, 1457–1460.CrossRefGoogle Scholar
Kolbert, A. C. & Bielecki, A. (1995). Broadband Hartmann-Hahn matching in magicangle spinning NMR via an adiabatic frequency sweep. J. Magn. Reson. A116, 29–35.CrossRefGoogle Scholar
Koyama, Y., Kito, M., Takii, K., Saiki, K., Tsukida, K. & Yamashita, J. (1982). Configuration of the carotenoid in the reaction centres of photosynthetic bacteria. Comparison of the resonance Raman spectrum of Rhodopseudomonas sphaeroides with those of cis-trans isomers of beta-carotene. Biochim. Biophys. Ada 680, 109–118.CrossRefGoogle Scholar
Kreusch, A., Neubueser, E., Schiltz, J., Weckesser, J. & Schulz, G. E. (1994). The structure of the membrane channel porin from Rhodopseudomonas blastica at 2·0 Å resolution. Protein Science 3, 58–63.CrossRefGoogle ScholarPubMed
Kühlbrandt, W. (1992). Two-dimensional crystallization of membrane proteins. Quart. Rev. Biophys. 25, 1–49.CrossRefGoogle ScholarPubMed
Kühlbrandt, W., Wang, D. G. & Fujiyoshi, Y. (1994). Atomic model of plant lightharvesting complex by electron crystallography. Nature 367, 614–621.CrossRefGoogle ScholarPubMed
Kulke, R., Horwitz, B. H., Zibello, T. & Dimaio, D. (1992). The central hydrophobic domain of the bovine papillomavirus Es transforming protein can be functionally replaced by many hydrophobic amino acid sequences containing.a glutamine. J. Virology 66, 505–511.CrossRefGoogle Scholar
Lakshmi, K. V., Auger, M., Raap, J., Lugtenburg, J., Griffin, R. G. & Herzfeld, J. (1993). Internuclear distance measurements in a reaction intermediate: solid state 13C NMR rotational resonance determination of the Schiff base configuration in the M photointermediate of bacteriorhodopsin. J. Am. Chem. Soc. 115, 8515–8516.CrossRefGoogle Scholar
Lee, Y. K., Kurur, N. D., Helmle, M., Johannessen, O. G., Nielsen, N. C. & Levitt, M. H. (1995). Efficient dipolar recoupling in the NMR of rotating solids. A sevenfold symmetric radiofrequency pulse sequence. Chem. Phys. Letters 242, 304–309.CrossRefGoogle Scholar
Lemmon, M. A. & Engelman, D. M. (1994). Specificity and promiscuity in membranehelix interactions. FEBS Lett. 346, 17–20.CrossRefGoogle Scholar
Lemmon, M. A., Flanagan, J. M., Hunt, J. F., Adair, B. D., Bormann, B. J., Dempsey, C. E. & Engelman, D. M. (1992 a). Glycophorin A dimerization is driven by specific interactions between transmembrane α-helices. J. Biol. Chem. 267, 7683–7689.CrossRefGoogle ScholarPubMed
Lemmon, M. A., Flanagan, J. M., Treutlein, H. R., Zhang, J. & Engelman, D. M. (1992 b). Sequence specificity in the dimerization of transmembrane a-helices. Biochemistry 31, 12719–12725.CrossRefGoogle Scholar
Levitt, M. H., Raleigh, D. P., Creuzet, F. & Griffin, R. G. (1990). Theory and simulations of homonuclear spin pair systems in rotating solids. J. Chem. Phys. 92, 6347–6364.CrossRefGoogle Scholar
Lewis, B. A., Harbison, G. S., Herzfeld, J. & Griffin, R. G. (1985). NMR structural analysis of a membrane protein: bacteriorhodopsin peptide backbone orientation and motion. Biochemistry 24, 4671–4679.CrossRefGoogle ScholarPubMed
Lowe, I. J. (1959). Free induction decays of rotating solids. Phys. Rev. Lett. 2, 285–287.CrossRefGoogle Scholar
Ludlam, C.Arkin, I. T., Liu, X.-M., Rothman, M. S., Rath, P., Aimoto, S., Smith, S. O., Engelman, D. & Rothschild, K. J. (1996). Fourier transform infrared spectroscopy and site-directed isotope labeling as a probe of local secondary structure in the transmembrane domain of phospholamban. Biophys. J. 70, 1728–1736.CrossRefGoogle ScholarPubMed
Lutz, M., Szaponarski, W., Berger, G., Robert, B. & Neumann, J. M. (1987). The stereoisomerism of bacterial reaction centre bound carotenoids revisited: an electronic absorption, resonance Raman and 1H-NMR study. Biochim. Biophys. Acta 894, 423–433.CrossRefGoogle Scholar
Maciel, G. E., Bronnimann, C. E. & Hawkins, B. L. (1990). High-resolution 1HNMR in solids via CRAMPS. Advan. Magn. Reson. 14, 125–150.CrossRefGoogle Scholar
Mackenzie, K., Prestegard, J. H. & Engelman, D. M. (1996). Leucine side-chain rotamers in a glycophorin A transmembrane peptide as revealed by three-bond carbon-carbon couplings and 13C chemical shifts. J. Biomol. NMR 7, 256–260.CrossRefGoogle Scholar
Madden, T. D. (1986). Current concepts in membrane protein reconstitution. Chem. Phys. Lipids 40, 207–222.CrossRefGoogle ScholarPubMed
Manolios, N. (Bonifacino, J. S. & Klausner, R. D. (1990). Transmembrane helical interactions and the assembly of the T cell receptor complex. Science 249, 274–277.CrossRefGoogle ScholarPubMed
Maricq, M. M. & Waugh, J. S. (1979). NMR in rotating solids. J. Chem. Phys. 70, 3300–3316.CrossRefGoogle Scholar
McDermott, A. E., Thompson, L. K., Winkel, C., Farrar, M. R., Pelletier, S., Lugtenburg, J., Herzfeld, J. & Griffin, Ŕ G. (1991). Mechanism of proton pumping in bacteriorhodopsin by solid state NMR: the protonation state of tyrosine in the light-adapted and M states. Biochemistry 30, 8366–8371.CrossRefGoogle ScholarPubMed
McDermott, A., Creuzet, F., Gebhard, R., Van Der Hoef, K., Levitt, M. H., Hertzfeld, J., Lugtenburg, J. & Griffin, R. G. (1994). Determination of intemuclear distances and the orientation of functional groups by solid state NMR: rotational resonance study of the conformation of retinal in bacteriorhodopsin. Biochemistry 33, 6129–6136.CrossRefGoogle Scholar
McDonnel, P. A., Shon, K., Kim, Y. & Opella, S. J. (1993). fd coat protein structure in membrane environments. J. Mol. Biol. 233, 447–463.CrossRefGoogle Scholar
McDowell, L. M., Klug, C. A., Beusen, D. D. & Schaefer, J. (1996). Ligand geometry of the ternary complex of 5-enolpyruvylshikimate-3-phosphate synthase from rotational-echo double-resonance NMR. Biochemistry 35, 5395–5403.CrossRefGoogle ScholarPubMed
Mehring, M. (1983). Principles of High-resolution NMR in Solids. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Metz, G., Wu, X. & Smith, S. O. (1994). Ramped-amplitude cross polarization in magic angle spinning NMR. J. Magn. Reson. A110, 219–227.CrossRefGoogle Scholar
Middleton, D. A., Robins, R., Reid, D. G. & Watts, A. (1996). Characterization of a small exchangeable inhibitor bound to a large membrane protein using highresolution solid state NMR spectroscopy. Biophys. J. 70, A19.Google Scholar
Mueller, D. D., Schmidt, A., Pappan, K. L., McKay, R. A. & Schaefer, J. (1995 a). Activator carbamino carbon to inhibitor phosphorus intemuclear distances in ribulose 1, 5-bisphosphate carboxylase/oxygenase. Biochemistry 34, 5597–5603.CrossRefGoogle Scholar
Mueller, K. T., Jarvie, T. P., Aurentz, D. J. & Roberts, B. W. (1995 b). The REDOR transform: direct calculation of internuclear couplings from dipolardephasing NMR data. Chem. Phys. Lett. 242, 535–542.CrossRefGoogle Scholar
Munowitz, M. G., Griffin, R. G., Bodenhausen, G. & Huang, T. H. (1981). Twodimensional rotational spin-echo NMR in solids: correlation of chemical shift and dipolar interactions. J. Am. Chem. Soc. 103, 2529–2533.CrossRefGoogle Scholar
Munowitz, M., Bachovchin, W. W., Herzfeld, J., Dobson, C. M. & Griffin, R. G. (1992). Acid-base tautomeric equilibria in the solid state: 15-N NMR spectroscopy of histidine and imidazole. Biochemistry 194, 1192–1196.Google Scholar
Nicholson, L. K. & Cross, T. A. (1989). Gramicidin cation channel: an experimental determination of the right-handed helix sense and verification of β-type hydrogenbonding. Biochemistry 28, 9379–9385.CrossRefGoogle Scholar
Nielsen, N. C., Bildsoe, H., Jakobsen, H. J. & Levitt, M. H. (1994). Double quantum homonuclear rotary resonance: efficient dipolar recovery in MAS NMR. J. Chem. Phys. 101, 1805–1812.CrossRefGoogle Scholar
Noren, C. J., Anthony-Cahill, S. J., Griffith, M. C. & Schultz, P. G. (1989). A general method for site-specific incorporation of unnatural amino acids into proteins. Science 244, 182–188.CrossRefGoogle ScholarPubMed
Opella, S. J., Kim, Y. & McDonnel, P. (1994). Experimental NMR studies of membrane proteins. Methods in Enzymology 239C, 536–560.CrossRefGoogle Scholar
Peersen, O., Wu, X., Kustanovich, I. & Smith, S. O. (1993). Variable amplitude cross polarization MAS NMR. J. Magn. Reson. A104, 334–339.CrossRefGoogle Scholar
Peersen, O. B., Wu, X. & Smith, S. O. (1994). Enhancement of CP-MAS-signals by variable amplitude cross polarization: compensation for inhomogeneous B1 fields. J. Magn. Reson. A106, 127–131.CrossRefGoogle Scholar
Peersen, O. B., Groesbeek, M., Aimoto, S. & Smith, S. O. (1995). Analysis of rotational resonance magnetization exchange curves from crystalline peptides. J. Am. Chem. Soc. 117, 7228–7237.CrossRefGoogle Scholar
Pervushin, K. V. & Arseniev, A. S. (1992). 3D structures of (1–36)bacterioopsin in organic mixture and SDS micelles determined from NMR data. FEBS Lett. 308, 190–196.CrossRefGoogle Scholar
Pervushin, K. V., Orekhov, V. Yu., Popov, A. I., Musina, L. Yu. & Arseniev, A. S. (1994). 3D structure of (1–71)bacterioopsin solubilized in organic mixture and SDS micelles determined by 1H− 15N NMR. Eur. J. Biochem. 219, 571–583.CrossRefGoogle Scholar
Pines, A., Gibby, M. G. & Waugh, J. S. (1973). Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59, 569–590.CrossRefGoogle Scholar
Popot, J. L. & Engelman, D. M. (1990). Membrane protein folding and oligomerization: the two stage model. Biochemistry 29, 4031–4037.CrossRefGoogle ScholarPubMed
Prosser, R. S., Hunt, S. A., Dinatale, J. A. & Vold, R. R. (1996 a). Magnetically aligned membrane model systems with positive order parameter: switching the sign of σ22 with paramagnetic ions. J. Am. Chem. Soc. 118, 269–270.CrossRefGoogle Scholar
Prosser, R. S., Hunt, S. A. & Vold, R. R. (1996 b). Improving sensitivity in mechanically oriented phospholipid bilayers using ultrathin glass plates–a deuterium solid state NMR study. J. Magn. Reson. B109, 109–111.Google Scholar
Ptak, M., Egret-Charlier, M., Sanson, A. & Bouloussa, O. (1980). A NMR study of the ionization of fatty acids, fatty amines and N-acylamino acids incorporated in phosphatidylcholine vesicles. Biochim. Biophys. Acta 600, 387–397.CrossRefGoogle ScholarPubMed
Puttner, I. B. & Kaback, H. R. (1988). Lac permease of Escherichia coli containing a single histidine residue is fully functional. Proc. Natl. Acad. Sci. USA 85, 1467–1471.CrossRefGoogle ScholarPubMed
Raleigh, D. P., Levitt, M. H. & Griffin, R. G. (1988). Rotational resonance in solid state NMR. Chem. Phys. Lett. 146, 71–76.CrossRefGoogle Scholar
Ramamoohthy, A., Gierasch, L. M. & Opella, S. J. (1995 a). Four-dimensional solid state NMR experiment that correlates the chemical shift and dipolar coupling frequencies of two heteronuclei with the exchange of dilute spin magnetization. J. Magn. Reson. B 109, 112–116.CrossRefGoogle Scholar
Ramamoorthy, A., Marassi, F. M., Zasloff, M. & Opella, S. J. (1995 b). Threedimensional solid state NMR spectroscopy of a peptide oriented in membrane bilayers. J. Biomol. NMR 6, 329–334.CrossRefGoogle ScholarPubMed
Ramamoorthy, A., Gierasch, L. M. & Opella, S. J. (1996 a). Resolved twodimensional anisotropic-chemical stift/heteronuclear dipolar coupling powder pattern spectra by three-dimensional solid state NMR spectroscopy. J. Magn. Reson. B 110, 102–106.CrossRefGoogle Scholar
Ramamoorthy, A., Gierasch, L. M. & Opella, S. J. (1996 b). Three-dimensional solid-state NMR correlation experiment with 1H homonuclear spin exchange. J. Magn. Reson. B 111, 81–84.CrossRefGoogle ScholarPubMed
Rashin, A. A., Iofin, M. & Honig, B. H. (1986). Internal cavities and buried waters in globular proteins. Biochemistry 25, 3619–3625.CrossRefGoogle ScholarPubMed
Roepe, P. D., Ahl, P. L., Herzfeld, J., Lugtenburg, J. & Rothschild, K. J. (1988). Tyrosine protonation changes in bacteriorhodopsin: a FTIR study of BR548 and its primary photoproduct. J. Biol. Chem. 263, 5110–5117.CrossRefGoogle ScholarPubMed
Rothschild, K. J., He, Y.-W., Gray, D., Roepe, P. D., Pelletier, S. L., Brown, R. S. & Herzfeld, J. (1989). Fourier transform infrared evidence for proline structural changes during the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA 86, 9832–9835.CrossRefGoogle ScholarPubMed
Sakmar, T. P., Franke, R. R. & Khorana, H. G. (1989). Glutamic acid 113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. USA 86, 8309.CrossRefGoogle ScholarPubMed
Sanders, C. R., Hare, B. J., Howard, K. & Prestegard, J. H. (1993). Magneticallyoriented phospholipid micelles as a tool for the study of membrane-associated molecules. Progress in NMR Spectroscopy 26, 421–444.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. Mol. Biol. 209, 171–175.CrossRefGoogle ScholarPubMed
Schaefer, J. & Stejskal, E. O. (1976). Carbon-13 nuclear magnetic resonance of polymers spinning at the magic angle. J. Am. Chem. Soc. 98, 1031–1032.CrossRefGoogle Scholar
Schertler, G. F. X. & Hargrave, P. A. (1995). Projection structure of frog rhodopsin in two crystal forms. Proc. Natl. Acad. Sci. USA 92, 11578–11582.CrossRefGoogle ScholarPubMed
Schertler, G. F., Villa, C. & Henderson, R. (1993). Projection structure of rhodopsin. Nature 362, 770–772.CrossRefGoogle ScholarPubMed
Schochat, S., Gast, P., Hoff, A. J., Boender, G. J., Van Leeuwen, S., Van Liemt, W. B. S., Vijgenboom, E., Raap, J., Lugtenburg, J. & De Groot, H. J. M. (1995). 13C MAS NMR evidence for a homogeneously ordered environment of tyrosine M210 in reaction centres of Rhodobacter sphaeroides. Spectrochimica Acta 51A, 135–144.Google Scholar
Shon, K.-J., Kim, Y., Colnago, L. & Opella, S. J. (1991). NMR studies of the structure and dynamics of membrane-bound bacteriophage Pf1 coat protein. Science 252, 1303–1305.CrossRefGoogle ScholarPubMed
Sigworth, F. J. (1993). Voltage gating of ion channels. Quart. Rev. Biophys. 27, 1–40.CrossRefGoogle Scholar
Simmerman, H. K. B., Lovelace, D. E. & Jones, L. R. J. (1989). Secondary structure of detergent-solubilized phospholamban a phosphorylatable oligomeric protein of cardiac sarcoplasmic reticulum. Biochim. Biophys. Acta 997, 322–329.CrossRefGoogle ScholarPubMed
Slichter, C. P. (1990). Principles of Magnetic Resonance, 3rd edn.Berlin: Springer Verlag.CrossRefGoogle Scholar
Smith, S. O. & Bormann, B. J. (1995). Determination of helix–helix interactions in membranes by rotational resonance NMR. Proc. Natl. Acad. Sci. USA 92, 488–491.CrossRefGoogle ScholarPubMed
Smith, S. O., Palings, I., Copié, V., Raleigh, D. P., Courtin, J., Pardoen, J. A., Lugtenburg, J., Mathies, R. A. & Griffin, R. G. (1987). Low-temperature solid state 13-C NMR studies of the retinal chromophore in rhodopsin. Biochemistry 26, 1606–1611.CrossRefGoogle Scholar
Smith, S. O., FArr-Jones, S., Griffin, R. G. & Bachovchin, W. W. (1989). Crystal versus solution structures of enzymes: NMR spectroscopy of a crystalline serine protease. Science 244, 961–964.CrossRefGoogle ScholarPubMed
Smith, S. O., Courtin, J., De Groot, H. J. M., Gebhard, R. & Lugtenburg, J. (1991). 13C magic angle spinning NMR studies of bathorhodopsin the primary photoproduct of rhodopsin. Biochemistry 30, 7409–7415.CrossRefGoogle ScholarPubMed
Smith, S. O., De Groot, H. J. M., Gebhard, R. & Lugtenburg, J. (1992). Magic angle spinning NMR studies on the metarhodopsin II intermediate of bovine rhodopsin: evidence for an unprotonated Schiff's base. Photochemistry & Photobiology 56, 1035–1039.CrossRefGoogle Scholar
Smith, S. O., Hamilton, J., Salmon, A. & Bormann, B. J. (1994). Rotational resonance NMR determination of intra- and intermolecular distances in dipalmitoylphosphatidylcholine bilayers. Biochemistry 33, 6327–6333.CrossRefGoogle ScholarPubMed
Smith, S. O., Smith, C. S. & Bormann, B. J. (1996). Strong hydrogen-bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor. Nature Struct. Biol. 3, 252–258.CrossRefGoogle ScholarPubMed
Sonar, S., Patel, N., Fisher, W. & Rothschild, K. J. (1993). Cell-free synthesis, functional refolding, and spectroscopic characterization of bacteriorhodopsin, an integral membrane protein. Biochemistry 32, 13777–13781.CrossRefGoogle ScholarPubMed
Sonar, S., Lee, C. P., Coleman, M., Patel, N., Liu, X., Marti, T., Khorana, H. G., Rajbhandary, U. L. & Rothschild, K. J. (1994). Site-directed isotope labelling and FTIR spectroscopy of bacteriorhodopsin. Nature Struct. Biol. 1, 512–517.CrossRefGoogle ScholarPubMed
Speyer, J. B., Sripada, P. K., Das Gupta, S. K., Shipley, G. G. & Griffin, R. G. (1987). Magnetic orientation of spingomyelin-lecithin bilayers. Biophys. J. 51, 687–691.CrossRefGoogle ScholarPubMed
Spiess, H. W. (1978). Rotation of molecules and nuclear spin relaxation. In: NMR Basic Principles and Progress. Vol. 15, pp. 55–214. Diehl, P., Fluck, E., and Kosfeld, R., editors. Springer Verlag Berlin.Google Scholar
Spooner, P. J. R., Rutherford, N. G., Watts, A. & Henderson, P. J. F. (1994). NMR observation of substrate in the binding site of an active sugar-H+ symport protein in native membranes. Proc. Natl. Acad. Sci. USA 91, 3877–3881.CrossRefGoogle ScholarPubMed
Sternberg, M. J. E. & Gullick, W. J. (1989). Neu receptor dimerization. Nature 339, 587.CrossRefGoogle ScholarPubMed
Sternberg, M. J. E. & Gullick, W. J. (1990). A sequence motif in the transmembrane region of growth factor receptors with tyrosine kinase activity mediates dimerization. Protein Engineering 3, 245–248.CrossRefGoogle ScholarPubMed
Subramaniam, S., Gerstein, M., Oesterhelt, D. & Henderson, R. (1993). Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12, 1–8.CrossRefGoogle ScholarPubMed
Sun, B.-Q., Costa, P. R., Kocisko, D., Lansbury, P. T. & Griffin, R. G. (1995 a). Internuclear distance measurements in solid state nuclear magnetic resonance: dipolar recoupling via rotor synchronized spin locking. J. Chem. Phys. 102, 702–707.CrossRefGoogle Scholar
Sun, B.-Q., Costa, P. R. & Griffin, R. G. (1995b). Heteronuclear polarization transfer by radiofrequency driven dipolar recoupling under magic angle spinning. J. Magn. Resort. A112, 191–198.CrossRefGoogle Scholar
Sun, B. Q., Rienstra, C. M., Costa, P., Williamson, J. S., Herzfeld, J. & Griffin, R. G. (1996). 3D 15N-13C-13C chemical shift correlation spectroscopy in rotating solids. J. Chem. Phys., in press.Google Scholar
Tadesse, L., Nazarbaghi, R. & Walters, L. (1991). Isotopically enhanced infrared spectroscopy: a novel method for examining secondary structure at specific sites in conformationally heterogeneuos peptides. J. Am. Chem. Soc. 113, 7036–7037.CrossRefGoogle Scholar
Tekely, P., Palmas, P. & Canet, D. (1994). Effect of proton spin exchange on the residual 13C MAS NMR linewidths. Phase modulated irradiation for efficient heteronuclear decoupling in rapidly rotating solids. J. Magn. Reson. 107, 129–133.CrossRefGoogle Scholar
Torbet, J. (1987). Using magnetic orientation to study structure and assembly. Trends Biochem. Sci. 12, 327–330.CrossRefGoogle Scholar
Toyoshima, C., Sasabe, H. & Stokes, D. L. (1993). Three-dimensional cryo-electron microscopy of the calcium ion pump in the sarcoplasmic reticulum membrane. Nature 362, 469–471.CrossRefGoogle ScholarPubMed
Treutlein, H. R., Lemmon, M. A., Engelman, D. M. & Brunger, A. T. (1992). The glycophorin A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices. Biochemistry 31, 12726–12733.CrossRefGoogle ScholarPubMed
Tsui, F. C., Ojcius, D. M. & Hubbell, W. L. (1986). The intrinsic pKa values for phosphatidylserine and phosphatidylethanolamine in phosphatidylcholine host bilayers. Biophys. J. 49, 459–468.CrossRefGoogle ScholarPubMed
Tuzi, S., Yamaguchi, S., Naito, A., Needleman, R., Lanyi, J. K. & Saito, H. (1996). Conformation and dynamics of [3−13C]Ala-labelled bacteriorhodopsin and bacterioopsin, induced by interaction with retinal and its analogs, as studied by 13C nuclear magnetic resonance. Biochemistry 35, 7520–7527.CrossRefGoogle Scholar
Tycko, R. & Dabbagh, G. (1990). Measurement of nuclear magnetic dipole—dipole couplings in magic angle spinning NMR. Chem. Phys. Lett. 173, 461–465.CrossRefGoogle Scholar
Tycko, R. & Smith, S. O. (1993). Symmetry principles in the design of pulse sequences for structural measurements in magic angle spinning NMR. J. Chem. Phys. 98, 932–943.CrossRefGoogle Scholar
Unwin, N. (1993). Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229, 1101–1124.CrossRefGoogle ScholarPubMed
Unwin, N. (1995). Acetylcholine receptor channel imaged in the open state. Nature 373, 37–43.CrossRefGoogle ScholarPubMed
Unwin, P. N. T. & Ennis, P. D. (1984). Two configurations of a channel-forming membrane protein. Nature 307, 609–612.CrossRefGoogle ScholarPubMed
Valentine, K. G., Schneider, D. M., Leo, G. C., Colnago, L. A. & Opella, S. J. (1986). Structure and dynamics of fd coat protein. Biophys. J. 49, 36–38.CrossRefGoogle ScholarPubMed
Van Liemt, W. B. S., Boender, G. J., Gast, P., Hoff, A. J., Lugtenburg, J. & De Groot, H. J. M. (1995). 13C MAS NMR characterization of the functionally asymmetric Qa binding in Rhodobacter sphaeroides R26 photosynthetic reaction centres using site-specific 13C-labelled ubiquinone-10. Biochemistry 34, 10229–10236.CrossRefGoogle Scholar
Von Heijne, G. (1986). The distribution of positively charged residues in bacterial inner membrane proteins correlates with the transmembrane topology. EMBO J. 5, 3021–3027.CrossRefGoogle Scholar
Wallace, B. A. (1990). Gramicidin channels and pores. Annu. Rev. Biophys. Biophys. Chem. 19, 127–157.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. Mol. Biol. 217, 691–699.CrossRefGoogle ScholarPubMed
Watts, A. (1994). High-resolution, non-crystallographic structural studies of large integral membrane proteins. Biochem. Soc. Trans. 22, 801–805.CrossRefGoogle ScholarPubMed
Waugh, J. S. (1976). Uncoupling of local field spectra in nuclear magnetic resonance: Determinations of atomic positions in solids. Proc. Natl. Acad. Sci. USA 73, 1394–1397.CrossRefGoogle ScholarPubMed
Weintraub, O., Vega, S., Hoelger, Ch. & Limbach, H.-H. (1994). Distance measurements between homonuclear spins in rotating solids. J. Magn. Reson. A 109, 14–25.CrossRefGoogle Scholar
Weiss, M. S., Wacker, T., Weckesser, J., Welte, W. & Schulz, G. E. (1990). The three-dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett. 267, 268–272.CrossRefGoogle ScholarPubMed
Wiedmann, T. S., Pates, R. D., Beach, J. M., Salmon, A. & Brown, M. F. (1988). Lipid–protein interactions mediate the photochemical function of rhodopsin. Biochemistry 27, 6469–6474.CrossRefGoogle ScholarPubMed
Williams, K. A. & Deber, C. M. (1991). Proline residues in transmembrane helices: Structural or dynamic role? Biochemistry 30, 8919–8923.CrossRefGoogle ScholarPubMed
Williamson, P., Groebner, G., Miller, K. & Watts, A. (1996). Solid state nuclear magnetic resonance (ss-NMR) of ligand protein interactions in the nicotinic acetylcholine receptor (nAChR). Biophys. J. 70, A221.Google Scholar
Wu, X. & Zilm, K. H. (1991). Heterogeneity of cross relaxation in solid state NMR. J. Magn. Reson. 93, 265.Google Scholar
Xia, D., Yu, C. A., Diesenhofer, J., Xia, J.-Z. & Yu, L. (1996). Three-dimensional structure of beef heart mitochondrial cytochrome bc1 complex. Biophys. J. 70, A253.Google Scholar
Yang, A.-S., Gunner, M. R., Sampogna, R., Sharp, K. & Honig, B. (1993). On the calculation of pKas in proteins. Proteins: Struct. Funct. Gene. 15, 252–265.CrossRefGoogle ScholarPubMed
Zhukovsky, E. A. & Oprian, D. D. (1989). Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246, 928–930.CrossRefGoogle ScholarPubMed
Zysmilich, M. G. & McDermott, A. (1996). Photochemically induced nuclear spin polarization in bacterial photosynthetic reaction centres: assignments of the 15N SSNMR spectra. J. Am. Chem. Soc. 118, 5867–5873.CrossRefGoogle Scholar