Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins

Biochemistry

Volumn 45, Issue 28, 2006, Pages 8453-8465

  Prosser, R Scott ^a   Evanics, Ferenc ^a   Kitevski, Julianne L ^a   Al Abdul Wahid, M Sameer ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BINDING ENERGY; BIOLOGICAL MEMBRANES; MICELLES; MICROBIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TOPOLOGY;

FAST TUMBLING BICELLES; MIMETIC MEMBRANE MODEL; MIMIC SPECIFIC MEMBRANES; POLYTOPIC TRANSMEMBRANE PROTEINS;

PROTEINS;

AMPHOPHILE; LIPID; MEMBRANE PROTEIN; PEPTIDE;

BICELLE; CARBON NUCLEAR MAGNETIC RESONANCE; DRUG BINDING; IMMERSION; MAGNETISM; MEMBRANE MODEL; MEMBRANE RECONSTITUTION; MICELLE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVIEW; SOLID STATE;

LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; SURFACE-ACTIVE AGENTS;

EID: 33746045690     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060615u     Document Type: Review

References (113)

1. Lancelot, N., Elbayed, K., and Piotto, M. (2005) Applications of variable-angle sample spinning experiments to the measurement of scaled residual dipolar couplings and N-15 CSA in soluble proteins, J. Biomol. NMR 33, 153-161.
2. Sanders, C. R., and Oxenoid, K. (2000) Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins, Biochim. Biophys. Acta 1508, 129-145.
3. Sanders, C. R., Hare, B. J., Howard, K. P., and Prestegard, J. H. (1994) Magnetically-Oriented Phospholipid Micelles as a Tool for the Study of Membrane-Associated Molecules, Prog. Nucl. Magn. Reson. Spectrosc. 26, 421-444.
4. Sanders, C. R., and Prosser, R. S. (1998) Bicelles: A model membrane system for all seasons? Structure 6, 1227-1234.
5. Marcotte, I., and Auger, M. (2005) Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins, Concepts Magn. Reson., Part A 24, 17-37.
6. De Angelis, A. A., Jones, D. H., Grant, C. V., Park, S. H., Mesleh, M. F., and Opella, S. J. (2005) NMR experiments on aligned samples of membrane proteins, in Nuclear Magnetic Resonance of Biological Macromolecules, Part C, pp 350-382, Academic Press, New York.
7. Prosser, R. S., and Shiyanovskaya, I. V. (2001) Lanthanide ion assisted magnetic alignment of model membranes and macromolecules, Concepts Magn. Reson. 13, 19-31.
8. Davis, J. H., Auger, M., and Hodges, R. S. (1995) High-resolution H-1 nuclear magnetic resonance of a transmembrane peptide, Biophys. J. 69, 1917-1932.
9. Andronesi, O. C., Becker, S., Seidel, K., Heise, H., Young, H. S., and Baldus, M. (2005) Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy, J. Am. Chem. Soc. 127, 12965-12974.
10. Huster, D. (2005) Investigations of the structure and dynamics of membrane-associated peptides by magic angle spinning NMR, Prog. Nucl. Magn. Reson. Spectrosc. 46, 79-107.
11. Everts, S., and Davis, J. H. (2000) H-1 and C-13 NMR of multilamellar dispersions of polyunsaturated (22:6) phospholipids, Biophys. J. 79, 885-897.
12. Opella, S. J., Ma, C., and Marassi, F. M. (2001) Nuclear magnetic resonance of membrane-associated peptides and proteins, in Nuclear Magnetic Resonance of Biological Macromolecules, Part B, pp 285-313, Academic Press, New York.
13. Opella, S. J., and Marassi, F. M. (2004) Structure determination of membrane proteins by NMR spectroscopy, Chem. Rev. 104, 3587-3606.
14. Cross, T. A. (1997) Solid-state nuclear magnetic resonance characterization of gramicidin channel structure, in Solid-Phase Peptide Synthesis, p 672, Academic Press, New York.
15. Prosser, R. S., Hunt, S. A., and Vold, R. R. (1995) Improving Sensitivity in Mechanically Oriented Phospholipid-Bilayers Using Ultrathin Glass Plates: A Deuterium Solid-State NMR Study, J. Magn. Reson., Ser. B 109, 109-111.
16. Katsaras, J., Harroun, T. A., Pencer, J., and Nieh, M. P. (2005) "Bicellar" lipid mixtures as used in biochemical and biophysical studies, Naturwissenschaften 92, 355-366.
17. Nieh, M. P., Glinka, C. J., Krueger, S., Prosser, R. S., and Katsaras, J. (2001) SANS study of the structural phases of magnetically alignable lanthanide-doped phospholipid mixtures, Langmuir 17, 2629-2638.
18. Nieh, M. P., Raghunathan, V. A., Glinka, C. J., Harroun, T., and Katsaras, J. (2004) Structural phase behavior of high-concentration, alignable biomimetic bicelle mixtures, Macromol. Symp. 219, 135-145.
19. Nieh, M. P., Raghunathan, V. A., Glinka, C. J., Harroun, T. A., Pabst, G., and Katsaras, J. (2004) Magnetically alignable phase of phospholipid "Bicelle" mixtures is a chiral nematic made up of wormlike micelles, Langmuir 20, 7893-7897.
20. Aussenac, F., Lavigne, B., and Dufourc, E. J. (2005) Toward bicelle stability with ether-linked phospholipids: Temperature, composition, and hydration diagrams by H-2 and P-31 solid-state NMR, Langmuir 21, 7129-7135.
21. Aussenac, F., Laguerre, M., Schmitter, J. M., and Dufourc, E. J. (2003) Detailed structure and dynamics of bicelle phospholipids using selectively deuterated and perdeuterated labels. H-2 NMR and molecular mechanics study, Langmuir 19, 10468-10479.
22. Prosser, R. S., Hunt, S. A., DiNatale, J. A., and Vold, R. R. (1996) 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.
23. Prosser, R. S., Bryant, H., Bryant, R. G., and Vold, R. R. (1999) Lanthanide chelates as bilayer alignment tools in NMR studies of membrane-associated peptides, J. Magn. Reson. 141, 256-260.
24. Prosser, R. S., Volkov, V. B., and Shiyanovskaya, I. V. (1998) Novel chelate-induced magnetic alignment of biological membranes, Biophys. J. 75, 2163-2169.
25. Howard, K. P., and Opella, S. J. (1996) High-resolution solid-state NMR spectra of integral membrane proteins reconstituted into magnetically oriented phospholipid bilayers, J. Magn. Reson., Ser. B 112, 91-94.
26. Mangels, M. L., Cardon, T. B., Harper, A. C., Howard, K. P., and Lorigan, G. A. (2000) Spectroscopic characterization of spin-labeled magnetically oriented phospholipid bilayers by EPR spectroscopy, J. Am. Chem. Soc. 122, 7052-7058.
27. Chou, J. J., Kaufman, J. D., Stahl, S. J., Wingfield, P. T., and Bax, A. (2002) Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel, J. Am. Chem. Soc. 124, 2450-2451.
28. Vold, R. R., Prosser, R. S., and Deese, A. J. (1997) Isotropic solutions of phospholipid bicelles: A new membrane mimetic for high-resolution NMR studies of polypeptides, J. Biomol. NMR 9, 329-335.
29. Moberg, P., Nilsson, S., Stahl, A., Eriksson, A. C., Glaser, E., and Maler, L. (2004) NMR solution structure of the mitochondrial F-1β presequence from Nicotiana plumbaginifolia, J. Mol. Biol. 336, 1129-1140.
30. Braunschweiler, L., and Ernst, R. R. (1983) Coherence Transfer by Isotropic Mixing: Application to Proton Correlation Spectroscopy, J. Magn. Reson. 53, 521-528.
31. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of Exchange Processes by 2-Dimensional NMR Spectroscopy, J. Chem. Phys. 71, 4546-4553.
32. Rance, M., Sorensen, O. W., Bodenhausen, G., Wagner, G., Ernst, R. R., and Wuthrich, K. (1983) Improved Spectral Resolution in Cosy H-1-Nmr Spectra of Proteins Via Double Quantum Filtering, Biochem. Biophys. Res. Commun. 117, 479-485.
33. Barany-Wallje, E., Andersson, A., Graslund, A., and Maler, L. (2004) NMR solution structure and position of transportan in neutral phospholipid bicelles, FEBS Lett. 567, 265-269.
34. Zhang, W. Y., and Smith, S. O. (2005) Mechanism of penetration of Antp(43-58) into membrane bilayers, Biochemistry 44, 10110-10118.
35. Andersson, A., and Maler, L. (2002) NMR solution structure and dynamics of motilin in Isotropic phospholipid bicellar solution, J. Biomol. NMR 24, 103-112.
36. Papadopoulos, E., Oglecka, K., Maler, L., Jarvet, J., Wright, P. E., Dyson, H. J., and Graslund, A. (2006) NMR solution structure of the peptide fragment 1-30, derived from unprocessed mouse Doppel protein, in DHPC micelles, Biochemistry 45, 159-166.
37. Lindberg, M., Jarvet, J., Langel, U., and Graslund, A. (2001) Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR, Biochemistry 40, 3141-3149.
38. Anderluh, G., Razpotnik, A., Podlesek, Z., Macek, P., Separovic, F., and Norton, R. S. (2005) Interaction of the eukaryotic pore-forming cytolysin equinatoxin II with model membranes: F-19 NMR studies, J. Mol. Biol. 347, 27-39.
39. Losonczi, J. A., Olejniczak, E. T., Betz, S. F., Harlan, J. E., Mack, J., and Fesik, S. W. (2000) NMR studies of the anti-apoptotic protein Bcl-x(L) in micelles, Biochemistry 39, 11024-11033.
40. Gomez-Fernandez, J. C., Llamas, M. A., and Aranda, F. J. (1999) The interaction of coenzyme Q with phosphatidylethanolamine membranes, Eur. J. Biochem. 259, 739-746.
41. Hilty, C., Wider, G., Fernandez, C., and Wuthrich, K. (2004) Membrane protein-lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents, ChemBioChem 5, 467-473.
42. Buck-Koehntop, B. A., Mascioni, A., Buffy, J. J., and Veglia, G. (2005) Structure, dynamics, and membrane topology of stannin: A mediator of neuronal cell apoptosis induced by trimethyltin chloride, J. Mol. Biol. 354, 652-665.
43. Metcalfe, E. E., Zamoon, J., Thomas, D. D., and Veglia, G. (2004) H-1/N-15 heteronuclear NMR spectroscopy shows four dynamic domains for phospholamban reconstituted in dodecylphosphocholine micelles, Biophys. J. 87, 1205-1214.
44. Opella, S. J., DeSilva, T. M., and Veglia, G. (2002) Structural biology of metal-binding sequences, Curr. Opin. Chem. Biol. 6, 217-223.
45. Prosser, R. S., Luchette, P. A., and Westerman, P. W. (2000) Using O-2 to probe membrane immersion depth by F-19 NMR, Proc. Natl. Acad. Sci. U.S.A. 97, 9967-9971.
46. Prosser, R. S., Luchette, P. A., Westerman, P. W., Rozek, A., and Hancock, R. E. W. (2001) Determination of membrane immersion depth with O-2: A high-pressure F-19 NMR study, Biophys. J. 80, 1406-1416.
47. Luchette, P. A., Prosser, R. S., and Sanders, C. R. (2002) Oxygen as a paramagnetic probe of membrane protein structure by cysteine mutagenesis and F-19 NMR spectroscopy, J. Am. Chem. Soc. 124, 1778-1781.
48. Evanics, F., and Prosser, R. S. (2005) Discriminating binding and positioning of amphiphiles to lipid bilayers by H-1 NMR, Anal. Chim. Acta 534, 21-29.
49. Hirose, K. (2001) A practical guide for the determination of binding constants, J. Inclusion Phenom. Macrocyclic Chem. 39, 193-209.
50. Marcotte, I., Separovic, F., Auger, M., and Gagne, S. M. (2004) A multidimensional H-1 NMR investigation of the conformation of methionine-enkephalin in fast-tumbling bicelles, Biophys. J. 86, 1587-1600.
51. Andersson, A., Almqvist, J., Hagn, F., and Maler, L. (2004) Diffusion and dynamics of penetratin in different membrane mimicking media, Biochim. Biophys. Acta 1661, 18-25.
52. Dhanasekaran, M., Palian, M. M., Alves, I., Yeomans, L., Keyari, C. M., Davis, P., Bilsky, E. J., Egleton, R. D., Yamamura, H. I., Jacobsen, N. E., Tollin, G., Hruby, V. J., Porreca, F., and Polt, R. (2005) Glycopeptides related to β-endorphin adopt helical amphipathic conformations in the presence of lipid bilayers, J. Am. Chem. Soc. 127, 5435-5448.
53. Guo, J. X., Pavlopoulos, S., Tian, X. Y., Lu, D., Nikas, S. P., Yang, D. P., and Makriyannis, A. (2003) Conformational study of lipophilic ligands in phospholipid model membrane systems by solution NMR, J. Med. Chem. 46, 4838-4846.
54. Wang, J. F., Schnell, J. R., and Chou, J. J. (2004) Amantadine partition and localization in phospholipid membrane: A solution NMR study, Biochem. Biophys. Res. Commun. 324, 212-217.
55. Nakamura, T., Takahashi, H., Takeuchi, K., Kohno, T., Wakamatsu, K., and Shimada, I. (2005) Direct determination of a membrane-peptide interface using the nuclear magnetic resonance cross-saturation method, Biophys. J. 89, 4051-4055.
56. Kohno, T., Kusunoki, H., Sato, K., and Wakamatsu, K. (1998) A new general method for the biosynthesis of stable isotope-enriched peptides using a decahistidine-tagged ubiquitin fusion system: An application to the production of mastoparan-X uniformly enriched with N-15 and N-15/C-13, J. Biomol. NMR 12, 109-121.
57. Farrow, N. A., Zhang, O. W., Szabo, A., Torchia, D. A., and Kay, L. E. (1995) Spectral Density-Function Mapping Using N-15 Relaxation Data Exclusively, J. Biomol. NMR 6, 153-162.
58. Bruschweiler, R. (2003) New approaches to the dynamic interpretation and prediction of NMR relaxation data from proteins, Curr. Opin. Struct. Biol. 13, 175-183.
59. Gardner, K. H., and Kay, L. E. (1998) The use of H-2, C-13, N-15 multidimensional NMR to study the structure and dynamics of proteins, Annu. Rev. Biophys. Biomol. Struct. 27, 357-406.
60. Kay, L. E. (2005) NMR studies of protein structure and dynamics, J. Magn. Reson. 173, 193-207.
61. Tycko, R., Blanco, F. J., and Ishii, Y. (2000) Alignment of biopolymers in strained gels: A new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR, J. Am. Chem. Soc. 122, 9340-9341.
62. Sass, H. J., Musco, G., Stahl, S. J., Wingfield, P. T., and Grzesiek, S. (2000) Solution NMR of proteins within polyacrylamide gels: Diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes, J. Biomol. NMR 18, 303-309.
63. Crowell, K. J., and Macdonald, P. M. (1999) Surface charge response of the phosphatidylcholine head group in bilayered micelles from phosphorus and deuterium nuclear magnetic resonance, Biochim. Biophys. Acta 1416, 21-30.
64. Sanders, C. R., and Schwonek, J. P. (1992) Characterization of Magnetically Orientable Bilayers in Mixtures of Dihexanoylphosphatidylcholine and Dimyristoylphosphatidylcholine by Solid-State NMR, Biochemistry 31, 8898-8905.
65. Soong, R., and Macdonald, P. M. (2005) Lateral diffusion of PEG-lipid in magnetically aligned bicelles measured using stimulated echo pulsed field gradient H-1 NMR, Biophys. J. 88, 255-268.
66. Nusair, N. A., and Lorigan, G. A. (2005) Investigating the structural and dynamic properties of n-doxylstearic acid in magnetically-aligned phospholipid bilayers by X-band EPR spectroscopy, Chem. Phys. Lipids 133, 151-164.
67. Minto, R. E., Adhikari, P. R., and Lorigan, G. A. (2004) A H-2 solid-state NMR spectroscopic investigation of biomimetic bicelles containing cholesterol and polyunsaturated phosphatidylcholine, Chem. Phys. Lipids 132, 55-64.
68. Nusair, N. A., Tiburu, E. K., Dave, P. C., and Lorigan, G. A. (2004) Investigating fatty acids inserted into magnetically aligned phospholipid bilayers using EPR and solid-state NMR spectroscopy, J. Magn. Reson. 168, 228-237.
69. Sanders, C. R., and Landis, G. C. (1994) Facile Acquisition and Assignment of Oriented Sample NMR Spectra for Bilayer Surface-Associated Proteins, J. Am. Chem. Soc. 116, 6470-6471.
70. Sanders, C. R., and Landis, G. C. (1995) Reconstitution of Membrane Proteins into Lipid-Rich Bilayered Mixed Micelles for NMR Studies, Biochemistry 34, 4030-4040.
71. Tian, F., Losonczi, J. A., Fischer, M. W. F., and Prestegard, J. H. (1999) Sign determination of dipolar couplings in field-oriented bicelles by variable angle sample spinning (VASS), J. Biomol. NMR 15, 145-150.
72. Kishore, A. I., and Prestegard, J. H. (2003) Molecular orientation and conformation of phosphatidylinositides in membrane mimetics using variable angle sample spinning (VASS) NMR, Biophys. J. 85, 3848-3857.
73. Zandomeneghi, G., Tomaselli, M., van Beek, J. D., and Meier, B. H. (2001) Manipulation of the director in bicellar mesophases by sample spinning: A new tool for NMR spectroscopy, J. Am. Chem. Soc. 123, 910-913.
74. Zandomeneghi, G., Williamson, P. T. F., Hunkeler, A., and Meier, B. H. (2003) Switched-angle spinning applied to bicelles containing phospholipid-associated peptides, J. Biomol. NMR 25, 125-132.
75. Zandomeneghi, G., Tomaselli, M., Williamson, P. T. F., and Meier, B. H. (2003) NMR of bicelles: Orientation and mosaic spread of the liquid-crystal director under sample rotation, J. Biomol. NMR 25, 113-123.
76. Losonczi, J. A., and Prestegard, J. H. (1998) 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.
77. Losonczi, J. A., Tian, F., and Prestegard, J. H. (2000) Nuclear magnetic resonance studies of the N-terminal fragment of adenosine diphosphate ribosylation factor 1 in micelles and bicelles: Influence of N-myristoylation, Biochemistry 39, 3804-3816.
78. Sizun, C., Aussenac, F., Grelard, A., and Dufourc, E. J. (2004) NMR methods for studying the structure and dynamics of oncogenic and antihistaminic peptides in biomembranes, Magn. Reson. Chem. 42, 180-186.
79. Lu, J. X., Damodaran, K., and Lorigan, G. A. (2006) Probing membrane topology by high-resolution H-1-C-13 heteronuclear dipolar solid-state NMR spectroscopy, J. Magn. Reson. 178, 283-287.
80. Nevzorov, A. A., and Opella, S. J. (2003) A "Magic Sandwich" pulse sequence with reduced offset dependence for high-resolution separated local field spectroscopy, J. Magn. Reson. 164, 182-186.
81. Kim, Y., Valentine, K., Opella, S. J., Schendel, S. L., and Cramer, W. A. (1998) Solid-state NMR studies of the membrane-bound closed state of the colicin E1channel domain in lipid bilayers, Protein Sci. 7, 342-348.
82. Tan, W. M., Gu, Z. T., Zeri, A. C., and Opella, S. J. (1999) Solid-state NMR triple-resonance backbone assignments in a protein, J. Biomol. NMR 13, 337-342.
83. Marassi, F. M., Gesell, J. J., Valente, A. P., Kim, Y., Oblatt-Montal, M., Montal, M., and Opella, S. J. (1999) Dilute spin-exchange assignment of solid-state NMR spectra of oriented proteins: Acetylcholine M2 in bilayers, J. Biomol. NMR 14, 141-148.
84. Ramamoorthy, A., Wu, C. H., and Opella, S. J. (1999) Experimental aspects of multidimensional solid-state NMR correlation spectroscopy, J. Magn. Reson. 140, 131-140.
85. Gu, Z. T. T., and Opella, S. J. (1999) Two- and three-dimensional H-1/C-13 PISEMA experiments and their application to backbone and side chain sites of amino acids and peptides, J. Magn. Reson. 140, 340-346.
86. Gorzelle, B. M., Nagy, J. K., Oxenoid, K., Lonzer, W. L., Cafiso, D. S., and Sanders, C. R. (1999) Reconstitutive refolding of diacylglycerol kinase, an integral membrane protein, Biochemistry 38, 16373-16382.
87. Park, S. H., Prytulla, S., De Angelis, A. A., Brown, J. M., Kiefer, H., and Opella, S. J. (2006) High-Resolution NMR Spectroscopy of a GPCR in Aligned Bicelles, J. Am. Chem. Soc. 128, 7402-7403.
88. Waugh, J. S. (1976) Uncoupling of Local Field Spectra in Nuclear Magnetic-Resonance: Determination of Atomic Positions in Solids, Proc. Natl. Acad. Sci. U.S.A. 73, 1394-1397.
89. Goldburg, W. I., and Lee, M. (1963) Nuclear Magnetic Resonance Line Narrowing by a Rotating Rf Field, Phys. Rev. Lett. 11, 255.
90. Wu, C. H., Ramamoorthy, A., and Opella, S. J. (1994) High-Resolution Heteronuclear Dipolar Solid-State Nmr-Spectroscopy, J. Magn. Reson., Ser. A 109, 270-272.
91. Rhim, W. K., Pines, A., and Waugh, J. S. (1970) Violation of Spin-Temperature Hypothesis, Phys. Rev. Lett. 25, 218.
92. Wang, J., Denny, J., Tian, C., Kim, S., Mo, Y., Kovacs, F., Song, Z., 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.
93. 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.
94. Marassi, F. M., Ma, C., Gesell, J. J., and Opella, S. J. (2000) Three-dimensional solid-state NMR spectroscopy is essential for resolution of resonances from in-plane residues in uniformly N-15-labeled helical membrane proteins in oriented lipid bilayers, J. Magn. Reson. 144, 156-161.
95. Wu, C. H., Ramamoorthy, A., Gierasch, L. M., and Opella, S. J. (1995) Simultaneous Characterization of the Amide H-1 Chemical Shift, H-1-N-15 Dipolar, and N-15 Chemical-Shift Interaction Tensors in a Peptide-Bond by 3-Dimensional Solid-State NMR Spectroscopy, J. Am. Chem. Soc. 117, 6148-6149.
96. 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.
97. Ramamoorthy, A., Wu, C. H., and Opella, S. J. (1995) Three-Dimensional Solid-State NMR Experiment That Correlates the Chemical-Shift and Dipolar Coupling Frequencies of 2 Heteronuclei, J. Magn. Reson., Ser. B 107, 88-90.
98. Gu, Z. T., and Opella, S. J. (1999) Three-dimensional C-13 shift/H-1-N-15 Coupling/N-15 shift solid-state NMR correlation spectroscopy, J. Magn. Reson. 138, 193-198.
99. Park, S. H., Mrse, A. A., Nevzorov, A. A., De Angelis, A. A., and Opella, S. J. (2006) Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy, J. Magn. Reson. 178, 162-165.
100. Sharpe, S., Yau, W. M., and Tycko, R. (2006) Structure and dynamics of the HIV-1 Vpu transmembrane domain revealed by solid-state NMR with magic-angle spinning, Biochemistry 45, 918-933.
101. Park, S. H., Mrse, A. A., Nevzorov, A. 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.
102. Thiriot, D. S., Nevzorov, A. A., Zagyanskiy, L., Wu, C. H., and Opella, S. J. (2004) Structure of the coat protein in Pf1 bacteriophage determined by solid-state NMR Spectroscopy, J. Mol. Biol. 341, 869-879.
103. Howell, S. C., Mesleh, M. F., and Opella, S. J. (2005) NMR structure determination of a membrane protein with two transmembrane helices in micelles: MerF of the bacterial mercury detoxification system, Biochemistry 44, 5196-5206.
104. Sanders, C. R., and Prestegard, J. H. (1990) Magnetically Orientable Phospholipid-Bilayers Containing Small Amounts of a Bile-Salt Analog, CHAPSO, Biophys. J. 58, 447-460.
105. Losonczi, J. A., and Prestegard, J. H. (1998) Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules, J. Biomol. NMR 12, 447-451.
106. Struppe, J., Whiles, J. A., and Vold, R. R. (2000) Acidic phospholipid bicelles: A versatile model membrane system, Biophys. J. 78, 281-289.
107. Marcotte, I., Dufourc, E. J., Ouellet, M., and Auger, M. (2003) Interaction of the neuropeptide Met-enkephalin with zwitterionic and negatively charged bicelles as viewed by P-31 and H-2 solid-state NMR, Biophys. J. 85, 328-339.
108. Parker, M. A., King, V., and Howard, K. P. (2001) Nuclear magnetic resonance study of doxorubicin binding to cardiolipin containing magnetically oriented phospholipid bilayers, Biochim. Biophys. Acta 1514, 206-216.
109. Aussenac, F., Lavigne, B., Dubernet, O., Raffard, G., and Dufourc, E. J. (2001) Phase diagrams of acyl chain ester- vs. ether-linked lipid bicelles: Towards the bicelle stability, Biophys. J. 80, 333A.
110. King, V., Parker, M., and Howard, K. P. (2000) Pegylation of magnetically oriented lipid bilayers, J. Magn. Reson. 142, 177-182.
111. Ulrich, A. S., and Watts, A. (1993) H-2 NMR Line Shapes of Immobilized Uniaxially Oriented Membrane-Proteins, Solid State Nucl. Magn. Reson. 2, 21-36.
112. Andersson, A., and Maler, L. (2005) Magnetic resonance investigations of lipid motion in isotropic bicelles, Langmuir 21, 7702-7709.
113. Dvinskikh, S., Durr, U., Yamamoto, K., Ramamoorthy, A. (2006) A high-resolution solid-state NMR approach for the structural studies of bicelles, J. Am. Chem. Soc., 128(19), 6326-6327