Skip to main content
SpringerLink
Log in
Book cover

Lipid Bilayers pp 207–231Cite as

Solid State NMR Approaches to the Study of Membrane Proteins in Magnetically Aligned Model Membranes

  • Chapter

  • 324 Accesses

Part of the book series: Biological Physics Series ((BIOMEDICAL))

Abstract

A vast number of pharmacophores and 20–30% of all proteins are membrane associated [1]. Thus an understanding of the three-dimensional structure and disposition of these macromolecules in the membrane is essential to interpreting their function, which might involve drug-receptor interactions, ion or small molecule transport, membrane signaling, or a myriad of other processes known to take place in (or on) membranes. However, of more than 7000 experimentally determined structures residing in the Brookhaven protein database, less than 1% correspond to membrane proteins. This disproportionate representation reflects the difficulties associated with applying conventional protein-structure determination techniques (x-ray diffraction and high resolution solution nuclear magnetic resonance (NMR)) to membrane proteins.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. D. Boyd, C. Schierle, J. Beckwith: How many membrane proteins are there? Protein Sci. 7, 201–205 (1998)

    Article  Google Scholar 

  2. K. Thornton, D. G. Gorenstein: Structure of glucagon-like peptide (7–36) amide in a dodecylphosphocholine micelle as determined by 2D NMR, Biochemistry 33, 3532–3539 (1994)

    Article  Google Scholar 

  3. G. D. Henry, B. D. Sykes: Methods to study membrane-protein structure in solution, Method. Enzymol. 239, 515–535 (1994)

    Google Scholar 

  4. C. H. Papavoine, J. M. Aelen, R. N. Konings, C. W. Hilbers, F. J. Van de Ven: NMR studies of the major coat protein of bacteriophage M13. Structural information of gVIIIp in dodecylphosphocholine micelles, Eur. J. Biochem. 232, 490–500 (1995)

    Article  Google Scholar 

  5. J. Jarvet, J. Zdunek, P. Damberg, A. Graslund: Three-dimensional structure and position of porcine motilin in sodium dodecyl sulfate micelles determined by 1H NMR, Biochemistry 36, 8153–8163 (1997)

    Article  Google Scholar 

  6. M. E. Girvin, V. K. Rastogi, F. Abildgaard, J. L. Markley, R. H. Fillingame: Solution structure of the transmembrane H+-transporting subunit c of the FIFO ATP synthase, Biochemistry 37, 8817–8824 (1998)

    Article  Google Scholar 

  7. K. Pervushin, R. Riek, G. Wider, K. Wiithrich: Attenuated T-2 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. U.S.A. 94, 12366–12371 (1997)

    Article  ADS  Google Scholar 

  8. M. Salzmann, K. Pervushin, G. Wider, H. Senn, K. Wuthrich: TROSY in triple-resonance experiments: New perspectives for sequential NMR assignment of large proteins, Proc. Natl. Acad. Sci. U.S.A. 95, 13585–13590 (1998)

    Article  ADS  Google Scholar 

  9. A. J. Wand, M. R. Ehrhardt, P. F. Flynn: High-resolution NMR of encapsulated proteins dissolved in low-viscosity fluids, Proc. Natl. Acad. Sci. U.S.A. 96, 6571–6571 (1999)

    Google Scholar 

  10. S. Gaemers, C. J. Elsevier, A. Bax: NMR of biomolecules in low viscosity, liquid C02, Chem. Phys. Lett. 301, 138–144 (1999)

    Article  ADS  Google Scholar 

  11. O. Vinogradova, P. Badola, L. Czerski, F. D. Sonnichsen, C. R. Sanders II: Es-cherichia coli diacylglycerol kinase: a case study in the application of solution NMR methods to an integral membrane protein, Biophys. J. 72, 2688–2701 (1997)

    Article  Google Scholar 

  12. A. S. Moffat: X-ray crystallography — Opening the door to more membrane protein structures, Science 277, 1607–1608 (1997)

    Article  Google Scholar 

  13. C. Ostermeier, H. Michel: Crystallization of membrane proteins, Curr. Opin. Struct. Biol. 7, 697–701 (1997)

    Article  Google Scholar 

  14. H. Sakai, T.Tsukihara: Structures of membrane proteins determined at atomic resolution, J. Biochem. (Tokyo) 124, 1051–1059 (1998)

    Article  Google Scholar 

  15. R. Garavito: Membrane protein structures: The known world expands, Curr. Opin. Biotechnol. 9, 344–349 (1998)

    Article  Google Scholar 

  16. E. M. Landau, J. P. Rosenbusch: Lipidic cubic phases: A novel concept for the crystallization of membrane proteins, Proc. Natl. Acad. Sci. U.S.A. 93, 14532–14535 (1996)

    Article  ADS  Google Scholar 

  17. R. Gennis: Biomembranes: Molecular Structure and Function (Springer Ver-lag, New York, 1989)

    Google Scholar 

  18. J. B. Heymann, D. J. Muller, K. Mitsuoka, A. Engel: Electron and atomic force microscopy of membrane proteins, Curr. Opin. Struct. Biol. 7, 543–549 (1997)

    Article  Google Scholar 

  19. C. Tribet, R. Audebert, J. L. Popot: Stabilization of hydrophobic colloidal dispersions in water with amphiphilic polymers: Application to integral membrane proteins, Langmuir 13, 5570–5576 (1997)

    Article  Google Scholar 

  20. L. M. McDowells, J. Schaefer: High-resolution NMR of biological solids, Curr. Opin. Struct. Biol. 6, 624–629 (1996)

    Article  Google Scholar 

  21. F. Adebodun, J. Chung, B. Montez, E. Oldfield, X. Shan: Spectroscopic studies of lipids and biological membranes — Carbon-13 and proton magic-angle sample-spinning nuclear magnetic resonance study of glycolipid water systems, Biochemistry 31, 4502–4509 (1992)

    Article  Google Scholar 

  22. J. H. Davis, M. Auger, R. S. Hodges: High resolution 1H nuclear magnetic resonance of a transmembrane peptide, Biophys. J. 69, 1917–1932 (1995)

    Article  Google Scholar 

  23. F. Moll, T. A. Cross: Optimizing and characterizing alignment of oriented lipid bilayers containing gramicidin D, Biophys. J. 57, 351–362 (1990)

    Article  Google Scholar 

  24. R. S. Prosser, S. A. Hunt, R. R. Void: Improving sensitivity in mechanically oriented phospholipid bilayers using ultrathin glass plates — a deuterium solid-state NMR study, J. Magn. Reson. 109, 109–111 (1995)

    Article  Google Scholar 

  25. J. Seelig, F. Borle, T. A. Cross: Magnetic ordering of phospholipid membranes, Biochim. Biophys. Acta 814, 195–198 (1985)

    Article  Google Scholar 

  26. F. Scholz, E. Boroske, W. Helfrich: Magnetic anisotropy of lecithin membranes. A new anisotropy susceptometer, Biophys. J. 45, 589–592 (1984)

    Article  Google Scholar 

  27. P. Ram, J. H. Prestegard: Magnetic field-induced ordering of bile salt/phospholipid micelles: New media for NMR structural investigations, Biochim. Biophys. Acta 940, 289–294 (1988)

    Article  Google Scholar 

  28. C. R. Sanders, J. P. Schwonek: Characterization of magnetically orientable bilayers in mixtures of dihexanoyl phosphatidylcholine and dimyristoyl phosphatidylcholine by solid-state NMR, Biochemistry 31, 8898–8905 (1992)

    Article  Google Scholar 

  29. R. R. Void, R. S. Prosser: Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J. Magn. Res. B 113, 267–271 (1996)

    Article  Google Scholar 

  30. C. R. Sanders, B. J. Hare, K. P. Howard, J. H. Prestegard: Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules, Prog. NMR Spec. 26, 421–444 (1994)

    Article  Google Scholar 

  31. J. Struppe, E. A. Komives, S. S. Taylor, and R. R. Void: 2H NMR studies of a myristoylated peptide in neutral and acidic phospholipid bicelles, Biochem-istry 37, 15523–15527 (1998)

    Article  Google Scholar 

  32. K. J. Crowell, P. M. Macdonald: Surface charge response of the phosphatidylcholine head group in bilayered micelles from phosphorus and deuterium nuclear magnetic resonance, Biochim. Biophys. Acta 1416, 21–30 (1999)

    Article  Google Scholar 

  33. C. R. Sanders, G. C. Landis: Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies, Biochemistry 34, 4030–4040 (1995)

    Article  Google Scholar 

  34. C. R. Sanders: Solid state 13C NMR of unlabeled phosphatidylcholine bi-layers: spectral assignments and measurement of carbon-phosphorus dipolar couplings and 13C chemical shift anisotropics, Biophys. J. 64, 171–181 (1993)

    Article  Google Scholar 

  35. C. R. Sanders: unpublished data

    Google Scholar 

  36. R. R. Void, R. S. Prosser, A. J. Deese: Isotropic solutions of phospholipid bi-celles: a new membrane mimetic for high resolution NMR studies of polypeptides, J. Biomol. NMR 9, 329–335 (1997)

    Article  Google Scholar 

  37. N. Tjandra, A. Bax: Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium, Science 278, 1111–1114 (1997)

    Article  ADS  Google Scholar 

  38. J. Chung, J. H. Prestegard: Characterization of field-ordered aqueous liquid-crystals by NMR diffusion measurements, J. Phys. Chem. 97, 9837–9843 (1993)

    Article  Google Scholar 

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

    Article  Google Scholar 

  40. R. S. Prosser, S. A. Hunt, J. A. DiNatale, R. R. Void: Magnetically aligned membrane model systems with positive order parameter — switching the sign of S-ZZ with paramagnetic ions, J. Am. Chem. Soc. 118, 269–270 (1996)

    Article  Google Scholar 

  41. R. S. Prosser, J. S. Hwang, R. R. Void: Magnetically aligned phospholipid bilayers with positive ordering: A new model membrane system, Biophys. J. 74, 2405–2418 (1998)

    Article  Google Scholar 

  42. R. S. Prosser, V. B. Volkov, I. V. Shiyanovskaya: Solid-state NMR studies of magnetically aligned phospholipid membranes: Taming lanthanides for membrane protein studies, Biochem. Cell Biol. 76, 443–451 (1998)

    Google Scholar 

  43. R. S. Prosser: unpublished data

    Google Scholar 

  44. K. P. Howard, S. J. Opella: High-resolution solid-state NMR spectra of integral membrane proteins reconstituted into magnetically oriented phospholipid bilayers, J. Magn. Reson. B 112, 91–94 (1996)

    Article  Google Scholar 

  45. B. J. Hare, J. H. Prestegard, D. M. Engelman: Small angle x-ray scattering studies of magnetically oriented lipid bilayers, Biophys. J. 69, 1891–1896 (1995)

    Article  Google Scholar 

  46. J. Katsaras, R. L. Donaberger, I. P. Swainson, D. C. Tennant, R. R. Void, R. S. Prosser: Rarely observed phase transitions in a novel lyotropic liquid crystal system, Phys. Rev. Lett. 78, 899–902 (1997)

    Article  ADS  Google Scholar 

  47. I. Shiyanovskaya, O. Lavrentovich, R. S. Prosser: unpublished data

    Google Scholar 

  48. R. S. Prosser, H. Bryant, R. G. Bryant, R. R. Void: Lanthanide chelates as bilayer alignment tools in NMR studies of membrane-associated peptides, J. Magn. Reson. 141, 256–260 (1999)

    Article  ADS  Google Scholar 

  49. W. Hiibner, A. Blume: 2H NMR Spectroscopy of oriented phospholipid bilayers in the gel phase, J. Phys. Chem. 94, 7726–7730 (1990)

    Article  Google Scholar 

  50. R. Bayer, G. W. Feigenson: Reconstitution of M13 bacteriophage coat protein. A new strategy to analyze configuration of the protein in the membrane, Biochim. Biophys. Acta 815, 369–379 (1985)

    Article  Google Scholar 

  51. M. Seigneuret, J. M. Neumann, J. L. Rigaud: Detergent delipidation and solubilization strategies for high resolution NMR of the membrane-protein bacteriorhodopsin, J. Biol. Chem. 266, 10066–10069 (1991)

    Google Scholar 

  52. V. Miguel, D. Balbi, C. Castillo, R. Villegas: Reconstitution of sodium-channels in large liposomes formed by the addition of acidic phospholipids and freeze-thaw sonication, J. Membrane Biol. 129, 37–47 (1992)

    Article  Google Scholar 

  53. R. Stahn, H. Schafer, M. Kunze, J. Malur, A. Ladhoff, U. Lachmann: Quantitative reconstitution of isolated influenza hemagglutinin into liposomes by the detergent method and the immunogenicity of hemagglutinin liposomes, Acta. Virol. 36, 129–144 (1992)

    Google Scholar 

  54. M. N. Jones: Surfactants in membrane solubilisation, Int. J. Pharm. 177, 137–159 (1999)

    Article  Google Scholar 

  55. L. Rilfors, A. Niemi, S. Haraldsson, K. Edwards, A. S. Andersson, W. Dowhan: Reconstituted phosphatidylserine synthase from Escherichia coli is activated by anionic phospholipids and micelle-forming amphiphiles, Biochim. Biophys. Acta 1438, 281–294 (1999)

    Article  Google Scholar 

  56. F. W. Lau, J. U. Bowie: A method for assessing the stability of a membrane protein, Biochemistry 36, 5884–5892 (1997)

    Article  Google Scholar 

  57. P. Badola, C. R. Sanders: Escherichia coli diacylglycerol kinase is an evolution-arily optimized membrane enzyme and catalyzes direct phosphoryl transfer, J. Biol. Chem. 272, 24176–24182 (1997)

    Article  Google Scholar 

  58. R. J. Cherry: Membrane protein dynamics: rotational dynamics, in The Structure of Biological Membranes, ed. P. Yeagle (CRC Press, Ann Arbor, 1992) pp. 507–537

    Google Scholar 

  59. L. Czerski, C. R. Sanders II: unpublished data

    Google Scholar 

  60. C. R. Sanders, II, J. P. Schwonek: Simulation of NMR data from oriented membrane proteins: Practical information for experimental design, Biophys. J. 65, 1460–1469 (1993)

    Article  Google Scholar 

  61. A. Saupe: Recent results in the field of liquid crystals, Angew. Chem., Int. Ed. Engl. 7, 97 (1968)

    Article  Google Scholar 

  62. P. Diehl, C. L. Khetrapal: NMR: Basic Principles and Progress (Springer Verlag, New York, 1969)

    Google Scholar 

  63. J. W. Emsley, J. C. Lindon: NMR Spectroscopy Using Liquid Crystal Solvents (Pergamon Press, Oxford, 1975)

    Google Scholar 

  64. F. Separovic, R. Pax, B. Cornell: NMR order parameter analysis of a peptide plane aligned in a lyotropic liquid-crystal, Mol. Phys. 78, 357–369 (1993)

    Article  ADS  Google Scholar 

  65. J. A. Losonczi, J. H. Prestegard: Nuclear magnetic resonance characterization of the myristoylated, N-terminal fragment of ADP-ribosylation factor 1 in a magnetically oriented membrane array, Biochemistry 37, 706–716 (1998)

    Article  Google Scholar 

  66. J. A. Losonczi, M. Andrec, M. W. F. Fischer, J. H. Prestegard: Order matrix analysis of residual dipolar couplings using singular value decomposition, J. Magn. Reson. 138, 334–342 (1999)

    Article  ADS  Google Scholar 

  67. F. Rinaldi, M. F. Lin, M. J. Shapiro, M. Petersheim: Delta-opiate DPDPE in magnetically oriented phospholipid micelles: Binding and arrangement of aromatic pharmacophores, Biophys. J. 73, 3337–3348 (1997)

    Article  Google Scholar 

  68. R. R. Ketchem, W. Hu, T. A. Cross: High-resolution conformation of grami-cidin-A in a lipid bilayer by solid-state NMR, Science 261, 1457–1460 (1993)

    Article  ADS  Google Scholar 

  69. R. R. Ketchem, B. Roux, T. A. Cross: High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR derived orientational constraints, Structure 5, 1655–1669 (1997)

    Article  Google Scholar 

  70. F. M. Marassi, S. J. Opella: NMR structural studies of membrane proteins, Curr. Opin. Struc. Biol. 8, 640–648 (1998)

    Article  Google Scholar 

  71. A. Ramamoorthy, F. M. Marassi, M. Zasloff, S. J. Opella: 3-Dimensional solid-state NMR-spectroscopy of a peptide oriented in membrane bilayers, J. Biomol. NMR 6, 329–334 (1995)

    Article  Google Scholar 

  72. A. Ramamoorthy, C. H. Wu, S. J. Opella: 3-Dimensional solid-state NMR experiment that correlates the chemical shift and dipolar frequencies of two heteronuclei, J. Magn. Reson. B 107, 88–90 (1995)

    Article  Google Scholar 

  73. A. Ramamoorthy, L. M. Gierasch, S.J. Opella: 4-dimensional solid-state NMR experiment that correlates the chemical-shift and dipolar-coupling frequencies of 2 heteronuclei with the exchange of dilute-spin magnetization, J. Magn. Reson. B 109, 112–116 (1995)

    Article  Google Scholar 

  74. A. Ramamoorthy, L. M. Gierasch, S. J. Opella: Resolved two-dimensional anisotropic-chemical-shift heteronuclear dipolar coupling powder-pattern spectra by three-dimensional solid-state NMR spectroscopy, J. Magn. Reson. B 110, 102–106 (1996)

    Article  Google Scholar 

  75. A. Ramamoorthy, L. M. Gierasch, S. J. Opella: Three-dimensional solid-state NMR correlation experiment with H-l homonuclear spin exchange, J. Magn. Reson. B 111, 81–84 (1996)

    Article  Google Scholar 

  76. B. Bechinger, M. Zasloff, S. J. Opella, Structure and dynamics of the antibiotic peptide PGLa in membranes by solution and solid-state nuclear magnetic resonance spectroscopy, Biophys. J. 74, 981–987 (1998)

    Article  Google Scholar 

  77. R. Jelinek, A. Ramamoorthy, S. J. Opella: High-resolution 3-dimensional solid-state NMR-spectroscopy of a uniformly N-15-labeled protein, J. Am. Chem. Soc. 117, 12348–12349 (1995)

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  79. W. M. Tan, R. Jelinek, S. J. Opella, P. Malik, T. D. Terry, R. N. Perham: Effects of temperature and Y21M mutation on conformational heterogeneity of the major coat protein (pVIII) of filamentous bacteriophage fd, J. Mol. Biol. 286, 787–796 (1999)

    Article  Google Scholar 

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

    Article  Google Scholar 

  81. J. S. Waugh: Uncoupling of local field spectra in nuclear magnetic resonance: determination of atomic positions in solids, Proc. Natl. Acad. Sci. USA 73, 1394–1397 (1976)

    Article  ADS  Google Scholar 

  82. K. Wuthrich: NMR of Proteins and Nucleic Acids (Wiley < Sons, New York, 1986)

    Google Scholar 

  83. W. M. Tan, Z. T. Gu, A. C. Zeri, S. J. Opella: Solid-state NMR triple-resonance backbone assignments in a protein, J. Biomol. NMR 13, 337–342 (1999)

    Article  Google Scholar 

  84. Y. Ishii, R. Tycko: Multidimensional heteronuclear correlation spectroscopy of a uniformly 15 N and 13C-labeled peptide crystal: Towards spectral resolution, assignment, and structure determination of oriented molecules in solid state NMR, J. Am. Chem. Soc. 122, 1443–1455 (2000)

    Article  Google Scholar 

  85. F. J. M. van de Ven: Multidimensional NMR in Liquids (Wiley-VCH, New York, 1986)

    Google Scholar 

  86. B. M. Fung, K. Ermolaev, Y. L. Yu: C-13 NMR of liquid crystals with different proton homonuclear dipolar decoupling methods, J. Magn. Reson. 138, 28–35 (1999)

    Article  ADS  Google Scholar 

  87. C. R. Sanders, G. C. Landis: Facile acquisition and assignment of oriented sample NMR-spectra for bilayer surface-associated proteins, J. Am. Chem. Soc. 116, 6470–6471 (1994)

    Article  Google Scholar 

  88. D. P. Burum, N. Linder, R. R. Ernst: High-power multipulse line narrowing in solid-state NMR, J. Magn, Reson. 44, 173–188 (1981)

    Google Scholar 

  89. A. Bielecki, A. C. Kolbert, M. H. Levitt: Frequency switched pulse sequences: homonuclear decoupling and dilute spin NMR in solids, Chem. Phys. Lett. 155, 341–346 (1989)

    Article  ADS  Google Scholar 

  90. M. H. Levitt, A. C. Kolbert, A. Bielecki, D. J. Ruben: High-resolution H-l-NMR in solids with frequency-switched multiple-pulse sequences, Solid State Nucl. Magn. Reson. 2, 151–163 (1993)

    Google Scholar 

  91. D. Nanz, M. Ernst, M. Hong, M. A. Ziegeweid, K. Schmidt-Rohr, A. Pines: Low-power decoupling sequences for high resolution chemical-shift and local-field NMR-spectra of liquid-crystals, J. Magn. Reson. 113, 169–176 (1995)

    Article  Google Scholar 

  92. M. Hong, A. Pines, S. Caldarelli: Measurement and assignment of long-range C-H dipolar couplings in liquid crystals by two-dimensional NMR spectroscopy, J. Phys. Chem. 100, 14815–14822 (1996)

    Article  Google Scholar 

  93. S. Caldarelli, M. Hong, L. Emsley, A. Pines: Measurement of carbon-proton dipolar couplings in liquid crystals by local dipolar field NMR spectroscopy, J. Phys. Chem. 100, 18696–18701 (1996)

    Article  Google Scholar 

  94. J. Courtieu, J. P. Bayle, B. M. Fung: Variable-angle sample-spinning NMR in liquid-crystals, Prog. Nucl. Mag. Res. Sp. 26, 141–169 (1994)

    Article  Google Scholar 

  95. F. Tian, J. A. Losonczi, M. W. F. Fischer, J. H. Prestegard: Sign determination of dipolar couplings in field-oriented bicelles by variable angle sample spinning (VASS), J. Biomol. NMR 15, 145–150 (1999)

    Article  Google Scholar 

  96. M. Zhou, V. Frydman, L. Frydman: Order determinations in liquid crystals by dynamic director NMR spectroscopy, J. Am. Chem. Soc. 120, 2178–2179 (1998)

    Article  Google Scholar 

  97. A. Kimura, N. Kuni, H. Fujiwara: Conformation and orientation of Met-enkephalin analogues in a lyotropic liquid crystal studied by the magic angle and near-magic angle spinning 2-D methodology in NMR: Relationships between activities and membrane-associated structures, J. Am. Chem. Soc. 119, 4719–4725 (1997)

    Article  Google Scholar 

Download references

Authors
  1. R. Scott Prosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles R. Sanders II
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2001 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Prosser, R.S., Sanders, C.R. (2001). Solid State NMR Approaches to the Study of Membrane Proteins in Magnetically Aligned Model Membranes. In: Lipid Bilayers. Biological Physics Series. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04496-4_10

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-04496-4_10

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-08702-8

  • Online ISBN: 978-3-662-04496-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation