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Solid State NMR for Studying Membrane Proteins

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Supramolecular Structure and Function 9

Solid state NMR is now established as a method for resolving structural information for large biomolecular complexes such as membrane-embedded proteins. In principle, there is no molecular weight limit to the use of the approach, although the complexity and volume of data is still outside complete assignment and structural determinations for any large (Mr > ~40k) complex, unless specific methods are used to reduce the information content. Such methods include specific residue type labelling, labelling of putative segments of a protein, probing ligand binding sites with labelled ligands, or examination of complexes made up of smaller, manageable units, such as oligomeric ion channels. Labelling possibilities often follow models from a bioinformatics approach. In all cases, and in common with most membrane studies, sample preparation is vital, and this activity alone can take considerable effort before NMR can be applied – peptide or protein production (synthesis or expression) followed by reconstitution into bilayers and/or chemical synthesis, and then resolution of suitable sample geometry, is still technically challenging. As experience is gained in the field, this development time should decrease. Here, a brief overview of the use of solid state NMR for membrane protein structural determinations will be presented.

Keywords: Solid state NMR, biomembranes, ion channels, GPCR, drugreceptor interactions, protein structure.

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References

  • Ahmed, Z., D.G. Reid, A. Watts, and D.A. Middleton. (2000) A solid-state NMR study of the phospholamban transmembrane domain: local structure and interactions with Ca(2+)-ATPase. Biochim. Biophys. Acta 1468(1-2): 187-198.

    Article  Google Scholar 

  • Andrew, E.R., A. Bradbury, and R.G. Eades. (1959) Removal of dipolar broadening of Nuclear Magnetic Resonance Spectra of Solids by Specimen Rotation. Nature 183 (4678): 1802-1803.

    Article  ADS  Google Scholar 

  • Arkin, I.T., A.T. Brünger, and D.M. Engelman. (1997) Are there dominant membrane protein families with a given number of helices? Protein: Structure, Function and Genetics 28: 465-466.

    Article  Google Scholar 

  • Bak, M., J.T. Rasmussen, and N.C. Nielsen. (2000) SIMPSON: A general simulation program for solid-state NMR spectroscopy. J. Magn. Res. 147: 296-330.

    Article  ADS  Google Scholar 

  • Bak, M., R. Schultz, T. Vosegaard, and N.C. Nielsen. (2002) Specification and visualization of anisotropic interaction tensors in polypeptides and numerical simulations in biological solid-state NMR. J. Magn. Res. 154(1): 28-45.

    Article  ADS  Google Scholar 

  • Baldus, M. (2002) Correlation experiments for assignment and structure elucidation of immobilized polypeptides under magic angle spinning. Progress in Nuclear Magn. Res. Spectros. 41: 1-47.

    Google Scholar 

  • Bennett, A.E., L.R. Becerra, and R.G. Griffin. (1994) Frequency-selective heteronuclear recoupling in rotating solids. J. Chem. Phys. 100(2): 812-814.

    Article  ADS  Google Scholar 

  • Bennett, A.E., C.M. Rienstra, M. Auger, K.V. Lakshmi, and R.G. Griffin. (1995) Heteronuclear Decoupling in Rotating Solids. J. Chem. Phys. 103(16): 6951-6958.

    Article  ADS  Google Scholar 

  • Borhan, B., M.L. Souto, H. Imai, Y. Shichida, and K. Nakanishi. (2000) Movement of Retinal Along the Visual Transduction Path. Science 288: 2209-2212.

    Article  ADS  Google Scholar 

  • Bower, P.V., N. Oyler, M.A. Mehta, J.R. Long, P.S. Stayton, and G.P. Drobny. (1999) Determination of torsion angles in proteins and peptides using solid state NMR. J. Amer. Chem, Soc. 121(36): 8373-8375.

    Article  Google Scholar 

  • Brejc, K., W.J.v. Dijk, R.V. Klaassen, M. Schuurmans, J.v.d. Oost, A.B. Smit, and T.K. Sixma. (2001) Crystal structure of an ACh-binding protein reveals the ligandbinding domain of nicotinic receptors. Nature 411: 269-276.

    Article  ADS  Google Scholar 

  • Carravetta, M., M. Eden, X. Zhao, A. Brinkmann, and M.H. Levitt. (2000) Symmetry principles for the design of radiofrequency pulse sequences in the nuclear magnetic resonance of rotating solids. Chem. Phys. Lett. 321: 205-215.

    Article  ADS  Google Scholar 

  • Castellani, F., B.v. Rossum, A. Diehl, M. Schubert, K. Rehbein, and H. Oschkinat. (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420: 98.

    Article  ADS  Google Scholar 

  • Colombo, M.G., B.H. Meier, and R.R. Ernst. (1988) Rotor-driven spin diffusion in natural abundance 13C spin systems. Chem. Phys. Lett. 146: 189-196.

    Article  ADS  Google Scholar 

  • Costa, P.R., J.D. Gross, M. Hong, and R.G. Griffin. (1997) Solid-state NMR measurement of Psi in peptides: a NCCN 2Q-heteronuclear local field experiment. Chem. Phys. Lett. 280(1-2): 95-103.

    Article  ADS  Google Scholar 

  • Creemers, A.F., S. Kiihne, P.H. Bovee-Geurts, W.J. DeGrip, J. Lugtenburg, and H.J. de Groot. (2002) (1)H and (13)C MAS NMR evidence for pronounced ligand-protein interactions involving the ionone ring of the retinylidene chromophore in rhodopsin. Proc. Nat. Acad. Sci. USA 99(14): 9101-9106.

    Google Scholar 

  • Creemers, A.F.L., C.H.W. Klaassen, P.H.M. Bovee-Geurts, R. Kelle, U. Kragl, J. Raap, W.J. de Grip, J. Lugtenburg, and H.J.M. de Groot. (1999) Solid State 15N NMR Evidence for a Complex Schiff Base Counterion in the Visual G-Protein-Coupled Receptor Rhodopsin. Biochemistry 38(22): 7195-7199.

    Article  Google Scholar 

  • Davis, J.H., and M. Auger. (1999) Static and magic angle spinning NMR of membrane peptides and proteins. Progress Nucl. Magn. Res. Spectros. 35: 1-84.

    Article  Google Scholar 

  • de Groot, H.J. (2000) Solid-State NMR Spectroscopy Applied to Membrane Proteins. Curr. Opin. Biotechnol. 10: 593-600.

    Google Scholar 

  • Denny, J.K., J. Wang, T.A. Cross, and J.R. Quine. (2001) PISEMA powder patterns and PISA wheels. J. Magn. Res. 152(2): 217-226.

    Article  ADS  Google Scholar 

  • Detken, A., E.H. Hardy, M. Ernst, and B.H. Meier. (2002) Simple and efficient decoupling in magic-angle spinning solid-state NMR: the XiX scheme. Chem. Phys. Lett. 356(3-4): 298-304.

    Article  ADS  Google Scholar 

  • Dusold, S., and A. Sebald. (2000) Double-Quantum Filtration under Rotational-Resonance Conditions: Numerical Simulations and Experimental Results. J. Magn. Res. 145: 340-356.

    Article  ADS  Google Scholar 

  • Eden, M., and M.H. Levitt. (1999) Pulse sequence symmetries in the nuclear magnetic resonance of spinning solids: Application to heteronuclear decoupling. J. Chem. Phys. 111(4): 1511-1519.

    Article  ADS  Google Scholar 

  • Edman, K., P. Nollert, A. Royant, H. Belrhali, E. Pebay-Peyroula, J. Hajdu, R. Neutze, and E.M. Landau. (1999) High-resolution x-ray structure of an early intermediate in the bacteriorhodopsin photocycle. Nature 401: 822-826.

    Article  ADS  Google Scholar 

  • Eilers, M., P.J. Reeves, W. Ying, H.G. Gobind Khorana, and S.O. Smith. (1999) Magic angle spinning NMR of the protonated retinylidene Schiff base nitrogen in rhodopsin: Expression of 15N-lysine- and 13C-glycine-labeled opsin in a stable cell line. Proc. Nat. Acad. Sci. USA 93(2): 487-492.

    Article  ADS  Google Scholar 

  • Faham, S., and J.U. Bowie. (2002) Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol. 316 (1): 1-6.

    Article  Google Scholar 

  • Fares, C., F.J. Sharom, and J.H. Davis. (2002) 15N, 1H heteronuclear correlation NMR of gramicidin A in DMPC-d 67. J. Am. Chem. Soc. 124: 11232-11233.

    Article  Google Scholar 

  • Feng, X., M. Eden, A. Brinkmann, H. Luthman, L. Ericksson, A. Graslund, O.N. Antzutkin, and M.H. Levitt. (1997) Direct Determination of a peptide torsion angle psi by double-quantum solid-state NMR. J. Am. Chem. Soc. 119: 12006-12007.

    Article  Google Scholar 

  • Feng, X., Y.K. Lee, D. Sandstroem, M. Eden, H. Maisel, A. Sebald, and M.H. Levitt. (1996) Direct determination of a molecular torsional angle by solid-state NMR. Chem. Phys. Lett. 257(3,4): 314-320.

    Article  ADS  Google Scholar 

  • Feng, X., P.J. Verdegem, M. Eden, D. Sandstrom, Y.K. Lee, G. Bovee, G. de, J. Lugtenburg, H.J. de Groot, and M.H. Levitt. (2000) Determination of a molecular torsional angle in the metarhodopsin-I photointermediate of rhodopsin by doublequantum solid-state NMR. J. Biomol. NMR 16(1): 1-8.

    Article  Google Scholar 

  • Feng, X., P.J.E. Verdegem, Y.K. Lee, M. Helmle, S.C. Shekar, H.J.M. de Groot, J. Lugtenburg, and M.H. Levitt. (1999) Rotational resonance NMR of 13C2-labelled retinal quantitative internuclear distance determination. Solid State Nucl. Magn. Res. 14: 81-90.

    Article  Google Scholar 

  • Feng, Y., and P. Gregor. (1997) Cloning of a novel member of the G protein-coupled receptor family related to peptide receptors. Biochem. Biophys. Res. Commun. 231(3): 651-654.

    Article  Google Scholar 

  • Fitter, J., R.E. Lechner, and N.A. Dencher. (1999) Interactions of hydration water and biological membranes studied by neutron scattering. J. Phys. Chem. 103: 8036-8050.

    Google Scholar 

  • Gallivan, J.P., and D.A. Dougherty. (1999) Cation-pi Interactions in Structural Biology. Proc. Natl. Acad. Sci. USA 96: 9459-9464.

    Article  ADS  Google Scholar 

  • Glaubitz, C., G. Gröbner, and A. Watts. (2000) Structural and orientational information of the membrane embedded M13 coat protein by 13C-MAS NMR spectroscopy. Biochim. Biophys. Acta 1463: 151-161.

    Article  Google Scholar 

  • Glaubitz, C., and A. Watts. (1998) Magic angle-oriented sample spinning (MAOSS): A new approach toward biomembrane studies. J. Magn. Res. 130: 305-316.

    Article  ADS  Google Scholar 

  • Goetz, J., B. Poliks, D. Studelska, M. Fischer, K. Kugelbrey, A. Bacher, M. Cushman, and J. Schaefer. (1999) Investigation of the binding of fluoroluminazes to the 1-MDa capsid of luminaze synthase by 15N{19F} REDOR NMR. J. Am. Chem. Soc. 121: 7500-7508.

    Article  Google Scholar 

  • Goetz, J.M., and J. Schaefer. (1997) Orientational information in solids from REDOR sidebands. J. Magn. Res. 129: 222-223.

    Article  ADS  Google Scholar 

  • Goto, N.K., and L.E. Kay. (2000) New developments in isotope labeling strategies for protein solution NMR spectroscopy. Curr. Opin. Struc. Biol. 10: 585-592.

    Article  Google Scholar 

  • Gregory, D.M., M.A. Mehta, J.C. Shiels, and G.P. Drobny. (1997) Determination of local structure in solid nucleic acids using double quantum nuclear magnetic resonance spectroscopy. J. Chem. Phys. 107(1): 28-42.

    Article  ADS  Google Scholar 

  • Griffin, R.G. (1998) Dipolar recoupling in MAS spectra of biological solids. Nature Struct. Biol. (NMR supplement): 508-512.

    Google Scholar 

  • Gröbner, G., I.J. Burnett, C. Glaubitz, G. Chol, A.J. Mason, and A. Watts. (2000) Observation of light-induced structural changes of retinal within rhodopsin. Nature 405: 810-813.

    Article  ADS  Google Scholar 

  • Gullion, T. (1998) Introduction to rotational-echo, double-resonance NMR. Concepts in Magn. Res. 10(5): 277-289.

    Article  Google Scholar 

  • Gullion, T., and J. Schaefer. (1989a) Detection of weak heteronuclear dipolar coupling by rotational-echo double-resonance nuclear magnetic resonance. Adv. Nucl. Magn. Res. 13: 57-83.

    Google Scholar 

  • Gullion, T., and J. Schaefer. (1989b) Rotational-echo double resonance NMR. J. Magn. Res. 81: 196-200.

    Google Scholar 

  • Hartmann, S., and E.L. Hahn. (1962) Nuclear double resonance in the rotating frame. Phys. Rev. 128: 2042-2053.

    Article  MATH  ADS  Google Scholar 

  • Hediger, S., B.H. Meier, N.D. Kurur, G. Bodenhausen, and R.R. Ernst. (1994) NMR cross polarization by adiabatic passage through the Hartmann-Hahn condition (APHH). Chem. Phys. Lett. 223(4): 283-288.

    Article  ADS  Google Scholar 

  • Herzfeld, J., and J.C. Lansing. (2002) Magnetic resonance studies of the bacterio-rhodopsin pump cycle. Ann. Rev. Biophys. Biomol. Struc. 31: 73-95.

    Article  Google Scholar 

  • Hong, M. (2006) Solid-State NMR Studies of the Structure and Dynamics of Disordered and Membrane-Bound Peptides and Proteins. Acc. Chem. Res. 39: 176-183.

    Article  Google Scholar 

  • Hong, M., J.D. Gross, and R.G. Griffin. (1997a) Site-resolved determination of peptide torsion angle g from the relative orientations of backbone N-H and C-H bonds by solid-state NMR. J. Phys. Chem. B 101(30): 5869-5874.

    Article  Google Scholar 

  • Hong, M., J.D. Gross, C.M. Rienstra, R.G. Griffin, K.K. Kumashiro, and K. SchmidtRohr. (1997b) Coupling amplification in 2D MAS NMR and its application to torsion angle determination in peptides. J. Magn. Res. 129(1): 85-92.

    Article  ADS  Google Scholar 

  • Huster, D., K. Arnold, and K. Gawrisch. (2000a) Strength of Ca(2+) binding to retinal lipid membranes: consequences for lipid organization. Biophys. J. 78(6): 3011-3018.

    Article  Google Scholar 

  • Huster, D., S. Yamaguchi, and M. Hong. (2000b) Efficient b-sheet identification in proteins by solid-state NMR spectroscopy. J. Am. Chem. Soc. 122(46): 11320-11327.

    Article  Google Scholar 

  • Kamihira, M., T. Vosegaard, A.J. Mason, S.K. Straus, N.C. Nielsen, and A. Watts. (2005) Structural and orientational constraints of bacteriorhodopsin in purple membranes determined by oriented-sample solid-state NMR spectroscopy. J. Struc. Biol. 149: 7-16.

    Article  Google Scholar 

  • Kim, S., J. Quine, and R. Cross. (2001) Complete Cross-Validation and R-Factor Calculation of a Solid-State NMR Derived Structure. J. Am. Chem. Soc. 123(30): 7292-7298.

    Article  Google Scholar 

  • Lakshimi, K.V., M. Auger, J. Raap, J. Lugtenburg, R.G. Griffin, and J. Herzfeld. (1993) Internuclear distance measurement in a reaction intermediate: solid-state 13C NMR rotational resonance determination of the Shiff base configuration in the M photo-intermediate of bacteriorhodopsin. J. Am. Chem. Soc. 115: 8515-8516.

    Article  Google Scholar 

  • Lam, Y.-H., C.J. Morton, and F. Separovic. (2002) Solid-state NMR Conformational Studies of a Melittin-inhibitor Complex. Eur. Biophys. J. 31: 383-388.

    Article  Google Scholar 

  • Lam, Y.-H., S.R. Wassall, C.J. Morton, R. Smith, and F. Separovic. (2001) Solid-state NMR structure determination of melittin in a lipid environment. Biophys. J. 81: 2752-2761.

    Article  Google Scholar 

  • Lanyi, J., and B. Schobert. (2002) Crystallographic structure of the retinal and the protein after deprotonation of the Schiff base: the switch in the bacteriorhodopsin photocycle. J. Mol. Biol. 321(4): 727-737.

    Article  Google Scholar 

  • Levitt, M.H., D.P. Raleigh, F. Creuzet, and R.G. Griffin. (1990) Theory and simulations of homonuclear spin pair systems in rotating solids. J. Chem. Phys. 92(11): 6347-6364.

    Article  ADS  Google Scholar 

  • Lowe, I.J. (1959) Free Induction Decay of Rotating Solids. Phys. Rev. Lett. 2(7): 285-287.

    Article  ADS  Google Scholar 

  • Luecke, H., B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi. (1999) Structure of bacteriorhodopsin at 1.55Å resolution. J. Mol. Biol. 291(4): 899-911.

    Article  Google Scholar 

  • Marassi, F.M. (2001) A simple approach to membrane protein secondary structure and topology based on NMR spectroscopy. Biophys. J. 80(2): 994-1003.

    Article  ADS  Google Scholar 

  • Marassi, F.M., and S.J. Opella. (2000) A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Res. 144: 150-155.

    Article  ADS  Google Scholar 

  • Marassi, F.M., A. Ramamoorthy, and S.J. Opella. (1997) Complete resolution of the solid-state NMR spectrum of a uniformly 15N-labeled membrane protein in phospholipid bilayers. Proc. Nat. Acad. Sci. USA 94: 8551-8556.

    Article  ADS  Google Scholar 

  • Mason, A.J., S.L. Grage, C. Glaubitz, S.K. Strauss, and A. Watts. (2003) Identifying anisotropic constraints in multiply labelled membrane proteins by 15N MAS NMR. Biophys. J. 86: 1610-1617.

    Article  Google Scholar 

  • McDermott, A.E., F. Creuzet, R. Gebhard, K. van der Hoef, M.H. Levitt, J. Herzfeld, J. Lugtenburg, and R.G. Griffin. (1994) Determination of internuclear distances and the orientation of functional groups by solid-state NMR: rotational resonance study of the conformation of retinal in bacteriorhodopsin. Biochemistry 33(20): 6129-6136.

    Article  Google Scholar 

  • Mehring, M. (1983) Fluck E, Diehl P, Kosfeld R, eds. Principles of High Resolution NMR Solids. Springer, New York.

    Google Scholar 

  • Metz, G., X. Wu, and S.O. Smith. (1994) Ramped-amplitude cross polarization in magic-angle-spinning NMR. J. Magn. Res. 110: 219-227.

    Article  Google Scholar 

  • Middleton, D.A., S. Rankin, M. Esmann, and A. Watts. (2000) Structural insights into the binding of cardiac glycosides to the digitalis receptor revealed by solid-state NMR. Proc. Nat. Acad. Sci. USA 97(25): 13602-13607.

    Article  ADS  Google Scholar 

  • Middleton, D.A., D.G. Reid, and A. Watts. (1995) The conformations of a functional spin-labelled derivative of gastric H/K-ATPase investigated by EPR spectroscopy. Biochemistry 34: 7420-7429.

    Article  Google Scholar 

  • Middleton, D.A., R. Robins, X. Feng, M. Levitt, I.D. Spiers, C. Schwalbe, D.G. Reid, and A. Watts. (1997) The conformation of an inhibitor bound to the gastric proton pump. FEBS Lett. 410: 269-274.

    Article  Google Scholar 

  • Moltke, S., I. Wallat, N. Sakai, K. Nakanishi, M.F. Brown, and M.P. Heyn. (1999) The angles between the C(1)-, C(5)-, and C(9)-methyl bonds of the retinylidene chromophore and the membrane normal increase in the M intermediate of bacteriorhodopsin: direct determination with solid-state (2)H NMR. Biochemistry 38(36): 11762-11772.

    Article  Google Scholar 

  • Montal, M., and S.J. Opella. (2002) The structure of the M2 channel-lining segment from the nicotinic acetylcholine receptor. Biochim. Biophys. Acta 1565(2): 287-293.

    Article  Google Scholar 

  • Munson, K.B., and G. Sachs. (1988) Inactivation of H+,K+-ATPase by a K+ competitive photoaffinity inhibitor. Biochemistry 27: 3932-3938.

    Article  Google Scholar 

  • Nishimura, K., S.G. Kim, L. Zhang, and T.A. Cross. (2002) The closed state of a H+ channel helical bundle combining precise orientational and distance restraints from solid state NMR-1. Biochemistry 41: 13170-13177.

    Article  Google Scholar 

  • Nomura, K., K. Takegoshi, T. Terao, K. Uchida, and M. Kainosho. (1999) Determination of the Complete Structure of a Uniformly Labeled Molecule by Rotational Resonance Solid-State NMR in the Tilted Rotating Frame. J. Am. Chem. Soc. 121: 4064-4065.

    Article  Google Scholar 

  • Oesterhelt, D., C. Brauchle, and N. Hampp. (1991) Bacteriorhodopsin: a biological material for information processing. Quart. Rev. Biophys. 24: 425-478.

    Article  Google Scholar 

  • Oesterhelt, D., and W. Stoeckenius. (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Meth. Enzymol. 31: 667-678.

    Article  Google Scholar 

  • Opella, S.J., F.M. Marassi, J.J. Gesell, A.P. Valente, Y. Kim, M. Oblatt-Montal, and M. Montal. (1999) Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nature Struct. Biol. 6: 374-379.

    Google Scholar 

  • Palczewski, K., T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, B.A. Fox, I. Le Trong, D.C. Teller, T. Okada, R.E. Stenkamp, M. Yamamoto, and M. Miyano. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 277: 687-690.

    Google Scholar 

  • Pang, Y.P., B. Cusack, K. Groshan, and E. Richelson. (1996) Proposed ligand binding site of the transmembrane receptor for neurotensin (8-13). J. Biol. Chem. 271: 15060-15068.

    Article  Google Scholar 

  • Peersen, O.B., M. Groesbeek, S. Aimoto, and S. Smith. (1995) Analysis of rotational resonance magnetization exchange curves from crystalline peptides. J. Am. Chem. Soc. 117: 7228-7237.

    Article  Google Scholar 

  • Peersen, O.B., and S.O. Smith. (1993) Rotational resonance NMR of biological membranes. Concepts in Magn. Res. 5: 303-317.

    Article  Google Scholar 

  • Pines, A., M.G. Gibby, and J.S. Waugh. (1973) Protein-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59: 569-590.

    Article  ADS  Google Scholar 

  • Raleigh, D.P., M.H. Levitt, and R.G. Griffin. (1988) Rotational resonance in solid state NMR. Chem. Phys. Lett. 146: 71-76.

    Article  ADS  Google Scholar 

  • Ramamoorthy, A., C.H. Wu, and S.J. Opella. (1999) Experimental aspects of multidimensional solid-state NMR correlation spectroscopy. J. Magn. Res. 140: 131-140.

    Article  ADS  Google Scholar 

  • Royant, A., K. Edman, T. Ursby, E. Pebay-Peyroula, E.M. Landau, and R. Neutze. (2001) Spectroscopic characterization of bacteriorhodopsin’s L-intermediate in 3D crystals cooled to 170K. Photochem. Photobiol. 74(6): 794-804.

    Article  Google Scholar 

  • Sack, I., A. Goldbourt, S. Vega, and G. Buntkowsky. (1999) Deuterium REDOR: principles and applications for distance measurements. J. Magn. Res. 138: 54-65.

    Article  ADS  Google Scholar 

  • Sass, H., G. Buldt, R. Gessenich, D. Hehn, D. Neff, J. Schlesinger, J. Berendzen, and P. Ormos. (2000) Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature 40: 649-653.

    ADS  Google Scholar 

  • Schmidt-Rohr, K. (1996) Double-Quantum Solid-state NMR technique for determining torsion angles in polymers. Macromolecules 29(11): 3975-3981.

    Article  ADS  Google Scholar 

  • Schobert, B., J. Cupp-Vickery, V. Hornak, S. Smith, and J. Lanyi. (2002) Crystallographic structure of the K intermediate of bacteriorhodopsin: conservation of free energy after photoisomerization of the retinal. J. Mol. Biol. 321(4): 715-726.

    Article  Google Scholar 

  • Seiff, F., I. Wallat, P. Ermann, and M.P. Heyn. (1985) A neutron diffraction study on the location of the polyene chain of retinal in bacteriorhodopsin. Proc. Nat. Acad. Sci. USA 82: 3227-3231.

    Article  ADS  Google Scholar 

  • Shoji, A., T. Ozaki, T. Fujito, K. Deguchi, S. Ando, and I. Ando. (1990) N chemical shift tensors and conformation of solid polypeptides containing 15N-labeled L-alanine residues by 15N NMR. 2. Secondary structure reflected in sigma22. J. Am. Chem. Soc. 112: 4693-4697.

    Article  Google Scholar 

  • Shull, G.E., A. Schwartz, and J.B. Lingrel. (1985) Amino-acid sequence of the catalytic subunit of the (Na+ + K+)ATPase deduced from a complementary DNA 691. Nature 316: 691-695.

    Article  ADS  Google Scholar 

  • Singh, D., B.S. Hudson, C. Middleton, and R.B. Birge. (2001) Conformation and Orientation of the Retinyl Chromophore in Rhodopsin: A Critical Evaluation of Recent NMR Data on the Basis of the Theoretical Calculations Results in a Refined Picture Consistent with all Experimental Data. Biochemistry 40: 4201-4204.

    Article  Google Scholar 

  • Smith, S.O., K. Aschheim, and M. Groesbeek. (1996) Magic angle spinning NMR spectroscopy of membrane proteins. Quart. Rev. Biophys. 29: 395-449.

    Article  Google Scholar 

  • Smith, S.O., I. Palings, M.E. Miley, J. Courtin, H.J. de Groot, J. Lugtenburg, R. A. Mathies, and R.G. Griffin. (1990) Solid-state NMR studies of the mechanism of the opsin shift in the visual pigment rhodopsin. Biochemistry 29: 8158-8164.

    Article  Google Scholar 

  • Smith, S.O., O.B. Peersen, S. Yoshimura, and S. Aimoto. (1995) Determination of peptide structure in membranes by rotational resonance NMR. Peptide Chem. 32: 109-112.

    Google Scholar 

  • Spooner, P.J.R., J.M. Sharples, M.A. Verhoeven, J. Lugtenburg, C. Glaubitz, and A. Watts. (2002) Relative orientation between the beta-ionone ring and the polyene chain for the chromophore of rhodopsin in native membranes. Biochemistry 41: 7549-7555.

    Article  Google Scholar 

  • Straus, S.K., T. Bremi, and R.R. Ernst. (1998) Experiments and strategies for the assignment of fully 13C/15N-labelled polypeptides by solid state NMR. J. Biomol. NMR 12: 39-40.

    Article  Google Scholar 

  • Straus, S.K., W. Scott, and A. Watts. (2003) Assessing the effects of time- and spatialaveraging in 15N chemical shift/15N-1H dipolar correlation solid state NMR experiments. J. Biomol. NMR 26: 283-295.

    Article  Google Scholar 

  • Subramaniam, S., and R. Henderson. (2000) Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 406(6796): 653-657.

    Article  ADS  Google Scholar 

  • Terstappen, G.C., and A. Reggiani. (2001) In silico research in drug discovery. TRENDS in Pharmacol. Sci. 22(1): 23-26.

    Article  Google Scholar 

  • Thompson, L.K., A.E. McDermott, J. Raap, C.M. van der Wielen, J. Lugtenburg, J. Herzfeld, and R.G. Griffin. (1992) Rotational resonance NMR study of the active site structure in bacteriorhodopsin: conformation of the Schiff base linkage. Biochemistry 31(34): 7931-7938.

    Article  Google Scholar 

  • Tian, C., K. Tobler, R.A. Lamb, L.H. Pinto, and T.A. Cross. (2002) Expression and initial structural insights from solid state NMR of the M2 proton channel from influenza A virus. Biochemistry 41: 11294-11300.

    Article  Google Scholar 

  • Toyoshima, C., M. Nakasako, H. Nomura, and H. Ogawa. (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405: 647-655.

    Article  ADS  Google Scholar 

  • Ulrich, A.S., M.P. Heyn, and A. Watts. (1992) Structure determination of the cyclohexene ring of retinal in bacteriorhodopsin by solid-state deuterium NMR. Biochemistry 31: 10390-10399.

    Article  Google Scholar 

  • Ulrich, A.S., I. Wallat, M.P. Heyn, and A. Watts. (1995) Re-orientation of retinal in the M-photointermediate of bacteriorhodopsin. Nature Struct. Biol. 2(3): 190-192.

    Article  Google Scholar 

  • Ulrich, A.S., A. Watts, I. Wallat, and M.P. Heyn. (1994) Distorted structure of the retinal chromophore in bacteriorhodopsin resolved by 2H-NMR. Biochemistry 33: 5370-5375.

    Article  Google Scholar 

  • Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346: 967-989.

    Article  Google Scholar 

  • Vosegaard, T., and N.C. Nielsen. (2002) Towards high-resolution solid-state NMR on large uniformly 15N- and [13C, 15N]-labeled membrane proteins in oriented lipid bilayers. J. Biomol. NMR 22: 225-247.

    Article  Google Scholar 

  • Wang, J., J. Denny, C. Tian, S. Kim, Y. Mo, F. Kovacs, Z. Song, K. Nishimura, Z. Gan, R. Fu, J.R. Quine, and T.A. Cross. (2000) Imaging membrane protein helical wheels. J. Magn. Res. 144: 162-167.

    Article  ADS  Google Scholar 

  • Wang, J.F., F. Kovacs, and T.A. Cross. (2001) Structure of the transmembrane region of the M2 protein H+ channel. Protein Sci. 10: 2241-2250.

    Article  Google Scholar 

  • Watts, A. (2005) Solid state NMR in drug design and discovery for membrane embedded targets. Nature Rev. Drug Discovery 4: 555-568.

    Article  Google Scholar 

  • Watts, A., S.K. Straus, S. Grage, M. Kamihira, Y.-H. Lam, and Z. Xhao. (2004) Membrane protein structure determination using solid state NMR. In: Downing K, ed., Methods in Molecular Biology - Techniques in Protein NMR. Humana Press, New Jersey, pp. 403-474.

    Chapter  Google Scholar 

  • Williamson, P.T.F., S. Bains, C. Chung, R. Cooke, and A. Watts. (2002) Probing the environment of neurotensin whilst bound to the neurotensin receptor by solid state NMR. FEBS Letts. 518: 111-115.

    Article  Google Scholar 

  • Williamson, P.T.F., G. Gröbner, P.J.R. Spooner, K.W. Miller, and A. Watts. (1998) Probing the agonist binding pocket on the nicotinic acetylcholine receptor: a high resolution solid state NMR approach. Biochemistry 37: 10854-10859.

    Article  Google Scholar 

  • Williamson, P.T.F., B.H. Meier, and A. Watts. (2004) Structural and functional studies of the nicotinic acetylcholine receptor by solid-state NMR. Eu. Biophys. J. 33: 247-254.

    Google Scholar 

  • Williamson, P.T.F., J.A. Watts, G.H. Addona, K.W. Miller, and A. Watts. (2001) Dynamics and orientation of N+(CD3)3-bromoacetylcholine bound to its binding site on the nicotinic acetylcholine receptor. Proc. Nat. Acad. Sci. USA 98: 2346-2351.

    Article  ADS  Google Scholar 

  • Wüthrich, K. (1998) The second decade - into the third millenium. Nature Struct. Biol. 5: 492-495.

    Google Scholar 

  • Yao, X.L., and M. Hong. (2001) Dipolar filtered 1H-13C heteronuclear correlation spectroscopy for resonance assignment of proteins. J. Biomol. NMR 20: 263-274.

    Article  Google Scholar 

  • Yao, X.L., K. Schmidt-Rohr, and M. Hong. (2001) Medium- and long-distance 1H-13C heteronuclear correlation NMR in solids. J. Magn. Res. 149: 139-143.

    Article  ADS  Google Scholar 

  • Zhong, W., J.P. Gallivan, Y. Zhang, L. Li, H.A. Lester, and D.A. Dougherty. (1998) From ab initio quantum mechanics to molecular neurobiology: A cation-1 binding site in the nicotinic receptor. Proc. Nat. Acad. Sci. USA 95: 12088-12093.

    Article  ADS  Google Scholar 

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  1. Department of Biochemistry, University of Oxford, South Parks Road, OX1 3QU, Oxford, UK

    Anthony Watts

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  1. Rudjer Boškovic Institute, Zagreb, Croatia

    Greta Pifat-Mrzljak

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Watts, A. (2007). Solid State NMR for Studying Membrane Proteins. In: Pifat-Mrzljak, G. (eds) Supramolecular Structure and Function 9. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6466-1_4

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