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Magic angle spinning NMR spectroscopy of membrane proteins

  • Steven O. Smith (a1), Kathryn. Aschheim (a1) and Michel Groesbeek (a1)


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.



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Abragam, A. (1961). The Principles of Nuclear Magnetism. Oxford: Clarendon Press.
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, 57305734.
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, 61626166.
Andrew, E. R., Bradbury, A. & Eades, R. G. (1958). Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182, 1659.
Andrew, E. R. & Szczesniak, E. (1995). A historical account of NMR in the solid state. Progress in NMR Spectroscopy 28, 1136.
Antzutkin, O. N., Shekar, S. & Levitt, M. H. (1995). Two-dimensional sideband separation in magic angle spinning NMR. J. Magn. Reson. A 115, 715.
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, 130140.
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, 6569.
Baldwin, J. M. (1993) The probable arrangement of the helices in G-protein coupled receptors. EMBO J. 12, 16931703.
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, 649657.
Bargmann, C. I., Hung, M.-C. & Weinberg, R. A. (1986 b). The neu oncogene encodes an epidermal growth factor receptor-related protein. Nature 319, 226230.
Barlow, D. J. & Thorton, J. M. (1988). Helix geometry in proteins. J. Mol. Biol. 201, 601619.
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, 86248627.
Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V. & Griffin, R. G. (1996). Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103, 69516958.
Bogomolni, R. A., Stubbs, L. & Lanyi, J. K. (1978). Illumination dependent changes in the intrinsic fluorescence of bacteriorhodopsin. Biochemistry 17, 10371041.
Bormann, B. J., Knowles, W. J. & Marchesi, V. T. (1989). Synthetic peptides mimic the assembly of transmembrane glycoproteins. J. Biol. Chem. 264, 40334037.
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, 19331938.
Braiman, M. S. & Rothschild, K. J. (1988). Fourier transform infrared techniques for probing membrane protein structure. Annu. Rev. Biophys. Biophys. Chem. 17, 541570.
Brandl, C. J. & Deber, C. M. (1986). Hypothesis about the function of membraneburied proline residues in transport proteins. Proc. Natl. Acad. Sci. USA 83, 917921.
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, 2712227126.
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, 55235530.
Burum, D. P. & Bielecki, A. (1991). An improved experiment for heteronuclear correlation 2D NMR in solids. J. Magn. Reson. 94, 645652.
Christensen, A. M. & Schaefer, J. (1993). Solid state NMR determination of intramolecular 31P−13C distances for shikimate 3-phosphate. Biochemistry 32, 28682873.
Cosson, P. & Bonifacino, J. S. (1992). Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 258, 659662.
Cosson, P., Lankford, S. P., Bonifacino, J. S. & Klausner, R. D. (1991). Membrane protein association by potential intramembrane charge pairs. Nature 351, 414416.
Cowan, S. W. (1993). Bacterial porins: lessons from three high-resolution structures. Curr. Opin. Struct. Biol. 3, 501507.
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, 727733.
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, 783786.
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, 123167.
Cross, T. A. & Opella, S. J. (1994). Solid state NMR structural studies of peptides and proteins in membranes. Curr. Opin. Struct. Biol. 4, 574581.
Davis, J. H., Auger, M. & Hodges, R. S. (1995). High-resolution 1H NMR of a transmembrane peptide. Biophys. J. 69, 19171932.
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, 251257.
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, 33463353.
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, 1244612450.
Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. (1984). X-ray structure analysis of a membrane protein complex. J. Mol. Biol. 180, 385398.
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, 618624.
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, 341345.
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, 65246533.
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, 275280.
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, 39673975.
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, 1724.
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, 321353.
Ernst, R. R., Bodenhausen, G. & Wokaun, A.. (1987). Principles of Nuclear Magnetic Resonance in One and Two Dimensions. Clarendon Press, Oxford.
Facelli, J. C., Grant, D. M. & Michl, J. (1987). Carbon-13 shielding tensors: Experimental and theoretical determination. Ace. Chem. Res. 20, 152158.
Fujiwara, T., Ramamoorthy, A., Nagayama, K., Hioka, K. & Fujito, T. (1993). Dipolar HOHAHA under MAS conditions for solid state NMR. Chem. Phys. Lett. 212, 8184.
Furthmayr, H. & Marchesi, V. T. (1976). Subunit structure of human erythrocyte glycophorin A. Biochemistry 15, 11371144.
Galzi, J.-L. & Changeux, J.-P. (1994). Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr. Opin. Struct. Biol. 4, 554565.
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, 59545962.
Garavito, R. M., Picot, D. & Loll, P. J. (1996). Strategies for crystallizing membrane proteins. J. Bioenerg. Biomemb. 28, 1327.
Garbow, J. & Gullion, T. (1995). Carbon-13 NMR Spectroscopy of Biological Systems. San Diego: Academic Press.
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, 238244.
Gennis, R. B. (1989). Biomembranes: Molecular Structure and Function. New York: Springer-Verlag.
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, 94949497.
Gerwert, K., Hess, B. & Engelhard, M. (1990). Proline residues undergo structural changes during proton pumping in bacteriorhodopsin. FEBS Lett. 261, 449454.
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, 1216712177.
Gouaux, E. (1996). Structure and function of alpha-hemolysin: a heptameric transmembrane pore. Biophys. J. 70, A121.
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, 1282812831.
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, 654663.
Griffiths, J. M. & Griffin, R. G. (1993). Nuclear magnetic resonance methods for measuring dipolar couplings in rotating solids. Anal. Chim. Acta 283, 10811101.
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, 1017810181.
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, 393421.
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, 187190.
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, 63686372.
Gullion, T. (1995 a). Detecting 13C−17O dipolar interactions by rotation-echo, adiabatic-passage, double resonance NMR. J. Magn. Reson. A117, 326329.
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, 325330.
Gullion, T. & Schaefer, J. (1989 a). Detection of weak heteronuclear dipolar coupling by rotational echo double-resonance nuclear magnetic resonance. Adv. Magn. Reson. 13, 5783.
Gullion, T. & Schaefer, J. (1989 b). Rotational-echo double-resonance NMR. J. Magn. Reson. 81, 196200.
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, 423428.
Han, M. & Smith, S. O. (1995). NMR constraints on the location of the retinal chromophore in rhodopsin and bathorhodopsin. Biochemistry 34, 14251432.
Han, M., Dedecker, B. S. & Smith, S. O. (1993). Localization of the retinal protonated Schiffs base counterion in rhodopsin. Biophys. J. 65, 899906.
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, 11791186.
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.
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.
Harbison, G. S., Herzfeld, J. & Griffin, R. G. (1983). Solid state nitrogen-15 NMR study of the Schiff's base in bacteriorhodopsin. Biochemistry 22, 15.
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, 72217223.
Hartmann, S. R. & Hahn, E. L. (1962). Nuclear double resonance in the rotating frame. Phys. Rev. 128, 20422053.
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, 40004008.
Henderson, R. & Unwin, P. N. T. (1975). Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 2832.
Henry, G. D. & Sykes, B. D. (1994). Methods to study membrane protein structure. Methods in Enzymology 239C, 515535.
Herzfeld, J. & Berger, A. E. (1980). Sideband intensities in NMR spectra of samples spinning at the magic angle. J. Chem. Phys. 73, 60216030.
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, 55675574.
Hing, A. W., Vega, S. & Schaefer, J. (1992). Transferred-echo double resonance NMR. J. Magn. Reson. 96, 205209.
Hing, A. W., Vega, S. & Schaefer, J. (1993). Measurement of heteronuclear dipolar coupling by transferred-echo double resonance NMR. J. Magn. Reson. 103, 151162.
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, 86518661.
Hong, J. & Harbison, G. S. (1993). MAS sideband elimination by temporary interruption of the chemical shift. J. Magn. Reson. A105, 128136.
Honig, B. H. & Hubbell, W. L. (1984). Stability of ‘salt bridges’ in membrane proteins. Proc. Natl. Acad. Sci. USA 81, 54125416.
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.
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.
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, 210222.
Hynes, N. E. & Stern, D. F. (1994). The biology of erbB-2/neu/HER-2 and its role in cancer. Biochim. Biophys. Acta 1198, 165184.
Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660669.
Jap, B. K. (1988). High-resolution electron diffraction of reconstituted PhoE porin. J. Mol. Biol. 199, 229231.
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, 53305331.
Jeener, J. (1971). Ampere International Summer School, Basko Polje, Yugoslavia, unpublished.
Joers, J., Rosanske, R., Gullion, T. & Garbow, J. (1994). Detection of dipolar interactions by Crown NMR. J. Magn. Reson. A106, 123126.
Kantor, H. L. & Prestegard, J. H. (1978). Fusion of phosphatidylcholine bilayer vesicles: role of free fatty acid. Biochemistry 17, 35923597.
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, 14571460.
Kolbert, A. C. & Bielecki, A. (1995). Broadband Hartmann-Hahn matching in magicangle spinning NMR via an adiabatic frequency sweep. J. Magn. Reson. A116, 2935.
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, 109118.
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, 5863.
Kühlbrandt, W. (1992). Two-dimensional crystallization of membrane proteins. Quart. Rev. Biophys. 25, 149.
Kühlbrandt, W., Wang, D. G. & Fujiyoshi, Y. (1994). Atomic model of plant lightharvesting complex by electron crystallography. Nature 367, 614621.
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, 505511.
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, 85158516.
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, 304309.
Lemmon, M. A. & Engelman, D. M. (1994). Specificity and promiscuity in membranehelix interactions. FEBS Lett. 346, 1720.
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, 76837689.
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, 1271912725.
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, 63476364.
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, 46714679.
Lowe, I. J. (1959). Free induction decays of rotating solids. Phys. Rev. Lett. 2, 285287.
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, 17281736.
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, 423433.
Maciel, G. E., Bronnimann, C. E. & Hawkins, B. L. (1990). High-resolution 1HNMR in solids via CRAMPS. Advan. Magn. Reson. 14, 125150.
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, 256260.
Madden, T. D. (1986). Current concepts in membrane protein reconstitution. Chem. Phys. Lipids 40, 207222.
Manolios, N. (Bonifacino, J. S. & Klausner, R. D. (1990). Transmembrane helical interactions and the assembly of the T cell receptor complex. Science 249, 274277.
Maricq, M. M. & Waugh, J. S. (1979). NMR in rotating solids. J. Chem. Phys. 70, 33003316.
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, 83668371.
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, 61296136.
McDonnel, P. A., Shon, K., Kim, Y. & Opella, S. J. (1993). fd coat protein structure in membrane environments. J. Mol. Biol. 233, 447463.
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, 53955403.
Mehring, M. (1983). Principles of High-resolution NMR in Solids. Berlin: Springer-Verlag.
Metz, G., Wu, X. & Smith, S. O. (1994). Ramped-amplitude cross polarization in magic angle spinning NMR. J. Magn. Reson. A110, 219227.
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.
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, 55975603.
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, 535542.
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, 25292533.
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, 11921196.
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, 93799385.
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, 18051812.
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, 182188.
Opella, S. J., Kim, Y. & McDonnel, P. (1994). Experimental NMR studies of membrane proteins. Methods in Enzymology 239C, 536560.
Peersen, O., Wu, X., Kustanovich, I. & Smith, S. O. (1993). Variable amplitude cross polarization MAS NMR. J. Magn. Reson. A104, 334339.
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, 127131.
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, 72287237.
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, 190196.
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, 571583.
Pines, A., Gibby, M. G. & Waugh, J. S. (1973). Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59, 569590.
Popot, J. L. & Engelman, D. M. (1990). Membrane protein folding and oligomerization: the two stage model. Biochemistry 29, 40314037.
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, 269270.
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, 109111.
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, 387397.
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, 14671471.
Raleigh, D. P., Levitt, M. H. & Griffin, R. G. (1988). Rotational resonance in solid state NMR. Chem. Phys. Lett. 146, 7176.
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, 112116.
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, 329334.
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, 102106.
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, 8184.
Rashin, A. A., Iofin, M. & Honig, B. H. (1986). Internal cavities and buried waters in globular proteins. Biochemistry 25, 36193625.
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, 51105117.
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, 98329835.
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.
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, 421444.
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, 171175.
Schaefer, J. & Stejskal, E. O. (1976). Carbon-13 nuclear magnetic resonance of polymers spinning at the magic angle. J. Am. Chem. Soc. 98, 10311032.
Schertler, G. F. X. & Hargrave, P. A. (1995). Projection structure of frog rhodopsin in two crystal forms. Proc. Natl. Acad. Sci. USA 92, 1157811582.
Schertler, G. F., Villa, C. & Henderson, R. (1993). Projection structure of rhodopsin. Nature 362, 770772.
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, 135144.
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, 13031305.
Sigworth, F. J. (1993). Voltage gating of ion channels. Quart. Rev. Biophys. 27, 140.
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, 322329.
Slichter, C. P. (1990). Principles of Magnetic Resonance, 3rd edn.Berlin: Springer Verlag.
Smith, S. O. & Bormann, B. J. (1995). Determination of helix–helix interactions in membranes by rotational resonance NMR. Proc. Natl. Acad. Sci. USA 92, 488491.
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, 16061611.
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, 961964.
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, 74097415.
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, 10351039.
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, 63276333.
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, 252258.
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, 1377713781.
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, 512517.
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, 687691.
Spiess, H. W. (1978). Rotation of molecules and nuclear spin relaxation. In: NMR Basic Principles and Progress. Vol. 15, pp. 55214. Diehl, P., Fluck, E., and Kosfeld, R., editors. Springer Verlag Berlin.
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, 38773881.
Sternberg, M. J. E. & Gullick, W. J. (1989). Neu receptor dimerization. Nature 339, 587.
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, 245248.
Subramaniam, S., Gerstein, M., Oesterhelt, D. & Henderson, R. (1993). Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12, 18.
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, 702707.
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, 191198.
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.
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, 70367037.
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, 129133.
Torbet, J. (1987). Using magnetic orientation to study structure and assembly. Trends Biochem. Sci. 12, 327330.
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, 469471.
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, 1272612733.
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, 459468.
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, 75207527.
Tycko, R. & Dabbagh, G. (1990). Measurement of nuclear magnetic dipole—dipole couplings in magic angle spinning NMR. Chem. Phys. Lett. 173, 461465.
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, 932943.
Unwin, N. (1993). Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229, 11011124.
Unwin, N. (1995). Acetylcholine receptor channel imaged in the open state. Nature 373, 3743.
Unwin, P. N. T. & Ennis, P. D. (1984). Two configurations of a channel-forming membrane protein. Nature 307, 609612.
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, 3638.
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, 1022910236.
Von Heijne, G. (1986). The distribution of positively charged residues in bacterial inner membrane proteins correlates with the transmembrane topology. EMBO J. 5, 30213027.
Wallace, B. A. (1990). Gramicidin channels and pores. Annu. Rev. Biophys. Biophys. Chem. 19, 127157.
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, 691699.
Watts, A. (1994). High-resolution, non-crystallographic structural studies of large integral membrane proteins. Biochem. Soc. Trans. 22, 801805.
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, 13941397.
Weintraub, O., Vega, S., Hoelger, Ch. & Limbach, H.-H. (1994). Distance measurements between homonuclear spins in rotating solids. J. Magn. Reson. A 109, 1425.
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, 268272.
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, 64696474.
Williams, K. A. & Deber, C. M. (1991). Proline residues in transmembrane helices: Structural or dynamic role? Biochemistry 30, 89198923.
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.
Wu, X. & Zilm, K. H. (1991). Heterogeneity of cross relaxation in solid state NMR. J. Magn. Reson. 93, 265.
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.
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, 252265.
Zhukovsky, E. A. & Oprian, D. D. (1989). Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246, 928930.
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, 58675873.

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Magic angle spinning NMR spectroscopy of membrane proteins

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