Techniques and applications of NMR to membrane proteins (Review)

References

• Almeida, F. C. L. and Opella, S. J., 1997, fd coat protein structure in membrane environments: Structural dynamics of the loop be- tween the hydrophobic trans-membrane helix and the amphipatic in-plane helix. J. Mol. Biol., 270, 481 –495.
   PubMed Web of Science ®Google Scholar
• Arora, A., Abildgaard, F., Bushweller, J. H. and Tamm, L. K., 2001, Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat. Struct. Biol., 8, 334 –338.
   PubMedGoogle Scholar
• Bak, M., Rasmussen, J. T. and Nielsen, N. C., 2000, SIMPSON: a general simulation program for solid-state NMR spectroscopy, J. Magn. Reson., 147, 296 –330. Open-source software, available at: http://www.bionmr.chem.au.dk.
   Google Scholar
• Bak, M., Bywater, R. P., Hohwy, M., Thomsen, J. K., Adelhorst, K., Jakobsen, H. J., Sørensen, O. W. and Nielsen, N. C., 2001, Conformation of alamethicin in oriented phospholipids bilayers determined by 15N solid-state nuclear magnetic resonance. Biophys. J., 81, 1684 -1698.
   PubMed Web of Science ®Google Scholar
• Bak, M., Schultz, R., Vosegaard, T. and Nielsen, N. C., 2002, Specification and visualization of anisotropic interaction tensors in polypeptides and numerical simulations in biological solid-state NMR, J. Magn. Reson., 154, 28 –45. Open-source software, available at: http://www.bionmr.chem.au.dk.
   Google Scholar
• Baldus, M., 2002, Correlation experiments for assignment and structure elucidation of immobilized polypeptides under magic angle spinning. Prog Nucl. Magn. Reson. Spectrosc., 41, 1 –47. Bechinger, B. and Sizun, C., 2003, Alignment and structural analysis of membrane polypeptides by 15N and 31P solid-state NMR spectroscopy. Concepts Magn. Reson., 18A, 130 -145.
   Google Scholar
• Bechinger, B., Zasloff, M. and Opella, S. J., 1993, Structure and orientation of the antibiotic peptide magainin in membranes by solid-state nuclear magnetic resonance spectroscopy. Prot. Sci., 7, 2077 -2084.
   Google Scholar
• Bechinger, B., Skladnev, D. A., Ogrel, A., Li, X., Rogozhkina, E. V., Ovchinnikova, T. V., O’Neil, D. J. and Raap, J., 2001, 15N and 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phoshatidylcholine membranes. Biochemistry, 40, 9428 -9437.
   Google Scholar
• Bennett, A. E., Griffin, R. G. and Vega, S., 1994, Recoupling of homo- and heteronuclear dipolar interactions in rotating solids. In NMR Basic Principles and Progress, Vol. 33. G. A. Webb, ed. (Springer-Verlag, Berlin), pp. 1 –77.
   Google Scholar
• Bernstein, F. C., Koetzle, T. F., Williams, G. J., Meier, E. E., Jr., Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. and Tasumi, M., 1977, The protein data bank: a computer based archival file for macromolecular structures, J. Mol. Biol., 112, 535 –542. Online. Available: http://www.rcsb.org/pdb.
   Google Scholar
• Bjerring, M., Vosegaard, T., Malmendal, A. and Nielsen, N. C., 2003, Methodological development of solid-state NMR for characterization of membrane proteins. Concepts Magn. Reson., 18A, 111 – 129.
   Google Scholar
• Bo¨ckmann, A., Lange, A., Galinier, A., Luca, S., Giraud, N., Juy, M., Heise, H., Montserret, R., Penin, F. and Baldus, M., 2003, Solid state NMR sequential resonance assignments and conforma- tional analysis of the 2 x10.4 kDa dimeric form of the Bacillus subtilis protein Crh. J. Biomol. NMR, 27, 323 –339.
   Google Scholar
• Braun, W., Wider, G., Lee, K. H. and Wu¨ thrich, K., 1983, Conforma- tion of glucagon in a lipid-water interphase by 1H nuclear magnetic resonance. J. Mol. Biol., 169, 921 –948.
   Google Scholar
• Castellani, F., van Rossum, B., Diehl, A., Schubert, M., Rehbein, K. and Oschkinat, H., 2002, Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature, 420, 98 –102.
   PubMed Web of Science ®Google Scholar
• Cavanagh, J., Fairbrother, W. J., Palmer, A. G., III and Skelton, N. J., 1996, Protein NMR Spectroscopy: Principles and Practice (Aca- demic Press, San Diego).
   Google Scholar
• Creuzet, F., McDermott, A. E., Gebhard, R., van der Hoef, K., Spijker-Assink, M. B., Herzfeld, J., Lugtenburg, J., Levitt, M. H. and Griffin, R. G., 1991, Determination of membrane protein structure by rotational resonance NMR: bacteriorhodopsin. Science, 251, 783 –786.
   PubMed Web of Science ®Google Scholar
• Davis, J. H. and Auger, M., 1999, Static and magic angle spinning NMR of membrane peptides and proteins. Prog. Nucl. Magn. Reson. Spectrosc., 35, 1 –84.
   Google Scholar
• deAzevedo, E. R., Bonagamba, T. J. and Schmidt-Rohr, K., 2000, Pure-exchange solid-state NMR. J. Magn. Reson., 142, 86 –96.
   Google Scholar
• Doyle, D. A., Cabral, J. M., Pfuetzner, Kuo, A. L., Gulbis, J. M., Cohen, S. L., Chait, B. T. and McKinnon, R., 1998, The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science, 280, 69 –77.
   Google Scholar
• Dusold, S. and Sebald, A., 2001, Dipolar recoupling under magic angle spinning conditions. Ann. Rep. NMR Spectrosc., 41, 185 – 264.
   Google Scholar
• Faham, S. and Bowie, J. U., 2002, Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol., 316, 1 –6.
   Web of Science ®Google Scholar
• Ferna´ ndez, C. and Wu¨ thrich, K., 2003, NMR solution structure determination of membrane proteins reconstituted in detergent micelles. FEBS Lett., 555, 144 –150.
   PubMed Web of Science ®Google Scholar
• Ferna´ ndez, C., Adeishvili, K. and Wu¨ thrich, K., 2001, Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Pro. Natl Acad. Sci. USA, 98, 2358 -2363.
   Google Scholar
• Ferna´ ndez, C., Hilty, C., Wider, G. and Wu¨ thrich, K., 2002, Lipid- protein interactions in DHPC micelles containing the integral membrane protein OmpX investigated by NMR spectroscopy. Proc. Natl Acad. Sci USA, 99, 13533–13537.
   PubMed Web of Science ®Google Scholar
• Fiaux, J., Bertelsen, E. B., Horwich, A. L. and Wu¨ thrich, K., 2002, NMR analysis of a 900K GroEL GroES complex. Nature, 418, 207 –211.
   Google Scholar
• Gardner, K. H., Rosen, M. K. and Kay, L. E., 1997, Global folds of highly deuterated, methyl-protonated proteins by multidimen- sional NMR. Biochemistry, 36, 1389 -1401.
   Google Scholar
• Girvin, M. E., Rastogi, V. K., Abildgaard, F., Markley, J. L. and Fillingame, R. H., 1998, Solution structure of the transmembrane H+-transporting subunit c of the F1Fo ATP synthase. Biochem- istry, 37, 8817–8824.
   PubMedGoogle Scholar
• Griffin, R. G., 1998, Dipolar recoupling in MAS spectra of biological solids. Nat. Struct. Biol., 5, 508 –512.
   PubMedGoogle Scholar
• Gro¨ bner, G., Taylor, A., Williamson, P. T., Choi, G., Glaubitz, C., Watts, J. A., de Grip, W. J. and Watts, A., 1997, Macroscopic orientation of natural and model membranes for structural studies. Analyt. Biochem., 254, 132 –138.
   Google Scholar
• Gro¨ bner, G., Burnett, I. J., Glaubitz, C., Choi, G., Mason, A. J. and Watts, A., 2000, Observations of light-induced structural changes of the retinal within rhodopsin. Nature, 405, 810 –813.
   PubMed Web of Science ®Google Scholar
• Haeberlen, U. and Waugh, J. S., 1968, Coherent averaging effects in magnetic resonance. Phys. Rev., 175, 453 –467.
   Web of Science ®Google Scholar
• Hebert, H., Purhonen, P., Vorum, H., Thomsen, K. and Maunsbach, A. B., 2001, Three-dimensional structure of renal Na,K-ATPase from cryo-electron microscopy of two-dimensional crystals. J. Mol. Biol., 314, 479 –494.
   Google Scholar
• Hohwy, M. and Nielsen, N. C., 1998, Systematic evaluation and design of multiple-pulse experiments in nuclear magnetic reso- nance spectroscopy using a semi-continuous Baker-Campbell- Hausdorff expansion. J. Chem. Phys., 109, 3780 -3791.
   Google Scholar
• Hohwy, M., Jakobsen, H. J., Ede´ n, M., Levitt, M. H. and Nielsen, N. C., 1998, Broadband dipolar recoupling in the nuclear magnetic resonance of rotating powders: A compensated C7 pulse se- quence. J. Chem. Phys., 108, 2686 –2694.
   Google Scholar
• Hwang, P. M., Choy, W.-Y., Eileen, I. L., Chen, L., Forman-Kay, J. D., Raetz, C. R. H., Prive´, G. G., Bishop, R. E. and Kay, L. E., 2002, Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl Acad. Sci. USA, 99, 13560- 13565.
   PubMed Web of Science ®Google Scholar
• Jaroniec, C. P., MacPhee, C. E., Baja, V. S., McMahon, M. T., Dobson, C. M. and Griffin, R. G., 2004, High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc. Natl Acad. Sci. USA, 101, 711 –716.
   PubMed Web of Science ®Google Scholar
• Ketchem, R. R., Lee, K. C., Huo, S. and Cross, T. A., 1996, Macromolecular structural elucidation with solid-state NMR-de- rived orientational constraints. J. Biomol. NMR, 8, 1 –14.
   PubMed Web of Science ®Google Scholar
• Lee, S., Mesleh, M. F. and Opella, S. J., 2003, Structure and dynamics of a membrane protein in micelles from three solution NMR experiments. J. Biomol. NMR, 26, 327 –334.Lee, Y. K., Kurur, N. D., Helmle, M., Johannesen, O. G., Nielsen, N. C. and Levitt, M. H., 1995, Efficient dipolar recoupling in the NMR of rotating solids. A sevenfold symmetric radiofrequency pulse sequence. Chem. Phys. Lett., 242, 304 –309.
   Google Scholar
• Levitt, M. H., 2002, Symmetry-based pulse sequences in magic- angle spinning solid-state NMR. In Encyclopedia of Nuclear Magnetic Resonance: Supplementary Volume. D. M. Grant andR. K. Harris, eds. (Wiley, Chichester), pp. 165 –196.
   Google Scholar
• Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P. and Lanyi, J. K., 1999, Structure of bacteriorhodopsin at 1.55 A resolution. J. Mol. Biol., 291, 899 –911.
   PubMed Web of Science ®Google Scholar
• Ma, C. and Opella, S. J., 2000, Lanthanide ions bind specifically to an added ‘EF-hand’ and orient a membrane protein in micelles for solution NMR spectroscopy. J. Magn. Reson., 146, 381 –384.McDermott, A. E., Polenova, T., Bo¨ ckmann, A, Zilm, K. W., Martin,
   Google Scholar
• R. W., Montelione, G. T. and Paulsen, E. K., 2000, Partial NMR assignments for uniformly (13C,15N)-enriched BPTI in the solid- state. J. Biomol. NMR, 16, 209 –219.
   Google Scholar
• McDowell, L. M., Lee, M. S., McKay, R. A., Anderson, K. S. and Schaefer, J., 1996, Intersubunit communication in tryptophan synthase by carbon-13 and fluorine-19 REDOR NMR. Biochem- istry, 35, 3328 -3334.
   Google Scholar
• MacKenzie, K. R., Prestegard, J. H. and Engelman, D. M., 1997, A transmembrane helix dimmer: structure and implications. Science, 276, 131 –133.
   PubMed Web of Science ®Google Scholar
• Marassi, F. M. and Opella, S. J., 2000, A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson., 144, 150 –155.
   PubMed Web of Science ®Google Scholar
• Marassi, F. M. and Opella, S. J., 2003, Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Prot. Sci., 12, 403 –411.
   PubMed Web of Science ®Google Scholar
• Marassi, F. M., Gesell, J. J., Valente, A. P., Kim, Y., Oblatt-Montal, M. and Opella, S. J., 1999, Dilute spin-exchange assignment of solid-state NMR spectra of oriented proteins: acetylcholine M2 in bilyaers. J. Biomol. NMR, 14, 141 –148.
   Google Scholar
• Martin, R. W. and Zilm, K. W., 2003, Preparation of protein nanocrystals and their characterization by solid state NMR. J. Magn. Reson., 165, 162 –174.
   PubMed Web of Science ®Google Scholar
• Matthey, U., Kaim, G., Braun, D., Wu¨ thrich, K. and Dimroth, P., 1999, NMR studies of subunit c of the ATP synthase from Propionigenium modestrum in dodecylsulphate micelles. Eur. J. Biochem., 261, 459 –467.
   Google Scholar
• Mesleh, M. F., Lee, S., Veglia, G., Thiriot, D. S., Marassi, F. and Opella, S. J., 2003, Dipolar waves map the structure and topology of helices in membrane proteins. J. Am. Chem. Soc., 125, 8928- 8935.
   Google Scholar
• Montal, M. and Opella, S. J., 2002, The structure of the M2 channel- lining segment from the nicotinic acetylcholine receptor. Biochem. Biophys. Acta, 1565, 287 –293.
   Google Scholar
• Murata, K., Kitsuoka, K., Hirai, T., Walz, T., Agre, P., Heymann, J. B., Engel, A. and Fujiyoshi, Y., 2000, Structural determinants of water permeation through aquaporin-1. Nature, 407, 599 –605.
   PubMed Web of Science ®Google Scholar
• Nielsen, G., Malmendal, A., Meissner, A., Møller, J. V. and Nielsen, N. C., 2003, NMR studies of the fifth transmembrane segment of sarcoplasmic reticulum Ca2+-ATPase reveals a hinge close to the Ca2+-ligating residues. FEBS Lett., 544, 50 –56.
   Google Scholar
• Nielsen, N. C., Bildsøe, H., Jakobsen, H. J. and Levitt, M. H., 1994, Double-quantum homonuclear rotary resonance: efficient dipolar recovery in magic-angle spinning nuclear magnetic resonance. J. Chem. Phys., 101, 1805 –1812.
   Web of Science ®Google Scholar
• Nielsen, N. C., Daugaard, P., Langer, V., Thomsen, J. K., Nielsen, S., Sørensen, O. W. and Jakobsen, H. J., 1995, A flat-coil NMR probe with hydration control of oriented phospholipid bilayer samples. J. Biomol. NMR, 5, 311 –314.
   Google Scholar
• Nishimura, K., Kim, S., Zhang, L. and Cross, T. A., 2002, The closed state of a H+ channel helical bundle combining precise orienta- tional and distance restraints from solid-state NMR. Biochemistry, 41, 13170–13177.
   PubMed Web of Science ®Google Scholar
• North, C. L, Barranger-Matthys, M. and Cafiso, D. S., 1995, Membrane orientation of the N-terminal segment of alamethicin determined by solid-state 15N NMR. Biophys. J., 69, 2392 –2397. Opella, S. J., 1997, NMR and membrane proteins. Nat. Struct. Biol., 4, 845 -848.
   Google Scholar
• Opella, S. J., Marassi, F. M., Gesell, J. J., Valente, A. P., Kim, Y., Oblatt-Montal, M. and Montal, M., 1999, Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol., 6, 374 –379.
   PubMedGoogle Scholar
• Oxenoid, K., So¨ nnichsen, F. D. and Sanders, C. R., 2002, Topology and secondary structure of the N-terminal domain of diacylgly- cerol kinase. Biochemistry, 41, 12876 –12882.
   Google Scholar
• Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M. and Miyano, M., 2000, Crystal structure of rhodopsin: a G-protein-coupled receptor. Science, 289, 739 –745. Papavoine, C. H. M., Christiaans, B. E. C., Folmer, R. H. A., Konings, R. N. H. and Hilbers, C. W., 1998, Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. J. Mol. Biol., 282, 401 -419.
   Google Scholar
• Park, S. H., Mrse, A. A., Nevzorov, A., Mesleh, M. F., Oblatt-Montal, M., Montal, M. and Opella, S. J., 2003, Three-dimensional structure of the channel-forming trans-membrane domain of virus protein ‘u’ (Vpu) from HIV-1. J. Mol. Biol., 333, 409 –424.
   PubMed Web of Science ®Google Scholar
• Pauli, J., van Rossum, B., Forster, H., de Groot, H. J. and Oschkinat, H., 2000, Sample optimization and identification of signal patterns of amino acid side chains in 2D RFDR spectra of the alpha- spectrin SH3 domain. J. Magn. Reson., 143, 411 –416.
   Google Scholar
• Pervushin, K. V., Orekhov, V. Y., Popov, A. I., Musina, L. Y. and Arseniev, A. S., 1994, Three-dimensional structure (1-71)bacter- ioopsin solubilized in methanol/chloroform and SDS micelles determined by 15N-1H heteronuclear NMR spectroscopy. Eur. J. Biochem., 219, 571 –583.
   PubMedGoogle Scholar
• Pervushin, K., Riek, R., Wider, G. and Wu¨ thrich, K., 1997, Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl Acad. Sci. USA, 94, 12366 –12371.
   Google Scholar
• Rienstra, C. M., Tucker-Kellogg, L., Jaroniec, C. P., Hohwy, M., Reif, B., McMahon, M. T., Tidor, B., Lozano-Perez, T. and Griffin, R. G., 2002, De novo determination of peptide structure with solid- state magic-angle spinning NMR spectroscopy. Proc. Natl Acad. Sci. USA, 99, 10260–10265.
   Google Scholar
• Russell, R. B. and Eggleston, D. S., 2000, New roles for structures in biology and drug discovery. Nat. Struct. Biol., 7, 928 –930.
   Google Scholar
• Scheuring, S., Mu¨ ller, D. J., Stahlberg, H., Engel, H. A. and Engel, A., 2002, Sampling the conformational space of membrane protein surfaces with the AFM. Eur. Biophys. J., 31, 172 –178.
   Google Scholar
• Schiller, P. and Mo¨ gel, H.-J., 2000, Indirect interaction of colloidal molecules adsorbed on solft surfaces. Phys. Chem. Chem. Phys., 2, 4563 –4568.
   Google Scholar
• Siminovitch, D., Untidt, T. and Nielsen, N. C., 2004, Exact effective Hamiltonian theory. II. Polynomial expansion of matrix functions and entangled unitary exponential operators. J. Chem. Phys., 120, 51 –68.
   Google Scholar
• Smith, S. O. and Bormann, B. J., 1995, Determination of helix-helix interactions in membranes by rotational resonance NMR. Proc. Natl Acad. Sci USA, 92, 488 –491.
   Google Scholar
• Sorgen, P. L., Cahill, S. M., Krueger-Koplin, R. D., Schenck, C. C. and Girvin, M. E., 2002, Structure of the Rhodobacter sphaer- oides light-harvesting 1 b subunit in detergent micelles. Biochem- istry, 41, 31 -41.
   Google Scholar
• Straus, S. K., Scott, W. R. P. and Watts, A., 2003, Assessing the effects of time and spatial averaging in 15N chemical shift/15N-1H dipolar correlation solid state NMR experiments. J. Biomol. NMR, 26, 283 –295.
   Google Scholar
• Subramaniam, S. and Henderson, R., 2000, Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature, 406, 653 –657.
   PubMed Web of Science ®Google Scholar
• Tamm, L. K., Abildgaard, F., Arora, A., Blad, H. and Buschweller, J. H., 2003, Structure, dynamics and function of the outer mem- brane protein A (OmpA) and influenza hemagglutinin fusion domain in detergent micelles by solution NMR. FEBS Lett., 555, 139 –143.
   PubMed Web of Science ®Google Scholar
• Toyshima, C. and Nomura, H., 2002, Structural changes in the calcium pump accompanying the dissociation of calcium. Nature, 418, 605 –611.
   Google Scholar
• Toyshima, C., Nakasako, M., Nomura, H. and Ogawa, H., 2000, Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature, 405, 647 -655.
   Google Scholar
• Tycko, R., 2000, Solid-state NMR as a probe of amyloid fibril structure. Curr. Opin. Chem. Biol., 4, 500 –506.
   Google Scholar
• Untidt, T. S. and Nielsen, N. C., 2002, A closed solution to the Baker- Campbell-Hausforff problem: exact effective Hamiltonian theory for analysis of nuclear magnetic resonance experiments. Phys. Rev. E, 65, 021108-1 –021108-17.
   Google Scholar
• Valentine, K. G., Liu, S. F., Marassi, F. M., Veglia, G., Opella, S. J.,
   Google Scholar
• Ding, F. X., Wang, S. H., Becker, J. M. and Naider, F., 2001, Structure and topology of a peptide segment of the 6th transmembrane domain of the Saccharomyces cerevisae alpha-factor receptor in phospholipids bilayers. Biopolymer, 59, 243 –256.
   Google Scholar
• van Beek, J. D., Hess, S., Vollrath, F. and Meier, B. H., 2002, The molecular structure of spider dragline silk: folding and orientation of the protein backbone. Proc. Natl Acad. Sci. USA, 99, 10266 – 10271.Venter et al ., 2001, The sequence of the humane genome, Science,291, 1304 –1351.
   Google Scholar
• Vosegaard, T. and Nielsen, N. C., 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.
   Google Scholar
• Vosegaard, T. and Nielsen, N. C., 2004, Improved pulse sequences for pure exchange solid-state NMR spectroscopy. Magn. Reson. Chem., 42, 285 –290.
   Google Scholar
• Vosegaard, T., Malmendal, A. and Nielsen, N. C., 2002, The flexibility of SIMPSON and SIMMOL for numerical simulations in solid- and liquid-state NMR spectroscopy. Chem. Month., 133, 1555 -1574.
   Google Scholar
• Wang, J., Balazs, Y. S. and Thompson, L. K., 1997, Solid-state REDOR NMR distance measurements at the ligand site of a bacterial chemotaxis membrane receptor. Biochemistry, 36, 1699 -1703.
   PubMed Web of Science ®Google Scholar
• Wang, J., Denny, J., Tian, C., Kim, S., Mo, Y., Kovacs, F., Song, Z.,
   Google Scholar
• Nishimura, K., Gan, Z., Fu, R., Quine, J. R. and Cross, T. A., 2000, Imaging membrane protein helical wheels. J. Magn. Reson., 144, 162 –167.
   Google Scholar
• Wang, J., Kim, S., Kovacs, F. and Cross, T. A., 2001, Structure of the transmembrane region of the M2 protein H(+) channel. Prot. Sci., 10, 2241–2250.
   PubMed Web of Science ®Google Scholar
• White, S. H. and Wimley, W. C., 1999, Membrane protein folding and stability: physical principles. Ann. Rev. Biophys. Biomol. Struct., 28, 319 –365.
   PubMedGoogle Scholar
• Wu, C. H., Ramamoorthy, A. and Opella, S. J., 1994, High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. A, 109, 270 –272.
   Google Scholar
• Wu¨ thrich, K., 1998, The second decade *into the third millennium. Nat. Struct. Biol., 5, 492 -495.
   Google Scholar
• Yang, J., Gabrys, C. M. and Weliky, D. P., 2001, Solid-state nuclear magnetic resonance evidence for an extended b strand confor- mation of the membrane bound HIV-1 fusion peptide. Biochem- istry, 40, 8126 -8137.
   Google Scholar
• Zeri, A. C., Mesleh, M. F., Nevzorov, A. A. and Opella, S. J., 2003, Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy. Proc. Natl Acad. Sci. USA, 100, 6458 –6463.Received 16 January 2004; and in revised form 8 March 2004.
   Google Scholar