NMR methods for measuring lateral diffusion in membranes

Chemistry and Physics of Lipids

Volumn 166, Issue 1, 2013, Pages 31-44

  Macdonald, Peter M ^a   Saleem, Qasim ^a   Lai, Angel ^a   Morales, Hannah H ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bicelles; Exchange NMR; Lateral diffusion; Macroscopically oriented membranes; Pulsed field gradient NMR; Vesicles

Indexed keywords

ANISOTROPY; ARTIFICIAL MEMBRANE; DEUTERON NUCLEAR MAGNETIC RESONANCE; DIFFUSION; DIFFUSION COEFFICIENT; HYDRODYNAMICS; LATERAL MEMBRANE DIFFUSION; MAGIC ANGLE SPINNING; MAGNETICALLY ALIGNED BICELLE; MATHEMATICAL MODEL; NORMAL DISTRIBUTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; VISCOSITY;

ANIMALS; CELL MEMBRANE; DIFFUSION; HUMANS; MEMBRANES, ARTIFICIAL; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOLIPIDS;

EID: 84873811812     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2012.12.004     Document Type: Review

References (181)

1. P.-A. Albertsson The structure and function of the chloroplast photosynthetic membrane-a model for the domain organization Photosynthesis Research 46 1995 141 149
2. D. Alcor, G. Gouzer, and A. Triller Single-particle tracking methods for the study of membrane receptors dynamics European Journal of Neuroscience 30 2009 987 997
3. P.F.F. Almeida, W.L.C. Vaz, and T.E. Thompson Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis Biochemistry 31 1992 6739 6747
4. P.F.F. Almeida, W.L.C. Vaz, and T.E. Thompson Lateral diffusion and percolation in 2-phase, 2-component lipid bilayers-topology of the solid-phase domains inplane and across the lipid bilayer Biochemistry 31 1992 7198 7210
5. P.F.F. Almeida, and W.L.C. Vaz Lateral diffusion in membranes R. Lipovsky, E. Sackmann, "Handbook of Biological Physics" 1 1995 305 357
6. E.R. Andrews, A. Bradbury, and R.G. Eades NMR spectra from a crystal rotated at high speed Nature 182 1958 1659 (London)
7. B. Antalek Using pulsed gradient spin echo NMR for chemical mixture analysis: How to obtain optimum results Concepts in Magnetic Resonance 14 2002 225 258
8. B. Antalek, J.M. Hewitt, W. Windig, P.D. Yacobucci, T. Mourey, and K. Le The use of PGSE NMR and DECRA for determining polymer composition Magnetic Resonance in Chemistry 40 2002 S60 S71
9. A.E. Bennett, C.M. Rienstra, M. Auger, K.V. Lakshmi, and R.G. Griffin Heteronuclear decoupling in rotating solids Journal of Chemical Physics 103 1995 6951 6958
10. M. Bloom, E.E. Burnell, S.B.W. Roeder, and M.I. Valic Nuclear magnetic-resonance line-shapes in lyotropic liquid-crystals and related systems Journal of Chemical Physics 66 1977 3012 3020
11. M. Bloom, E.E. Burnell, M.I. Valic, and G. Weeks Nuclear magnetic resonance line shapes in lipid bi-layer model membranes Chemistry and Physics of Lipids 14 1975 107 112
12. E. Boroske, and W. Helfrich Magnetic-anisotropy of egg lecithin membranes Biophysical Journal 24 1978 863 868
13. J. Boyd, and C. Redfield Characterization of N-15 chemical shift anisotropy from orientation-dependent changes to N-15 chemical shifts in dilute bicelle solutions Journal of the American Chemical Society 121 1999 7441 7442
14. J.J. Buffy, A.J. Waring, and M. Hong Determination of peptide oligomerization in lipid bilayers using 19F spin diffusion NMR Journal of the American Chemical Society 127 2005 4477 4483
15. P.T. Callaghan, and O. Söderman Examination of the lamellar phase of aerosol OT-water using pulsed field gradient nuclear magnetic resonance Journal of Physical Chemistry 87 1983 1737 1744
16. B.A. Camley, and F.L.H. Brown Contributions to membrane-embedded-protein diffusion beyond hydrodynamic theories Physical Review E 85 2012 061921 61931
17. S. Cavagnero, H.J. Dyson, and P.E. Wright Improved low pH bicelle system for orienting macromolecules over a wide temperature range Journal of Biomolecular NMR 13 1999 387 391
18. Y. Chen, B. Yang, and K. Jacobson Transient confinement zones: a type of lipid raft? Lipids 39 2004 1115 1119
19. G. Cho, B.M. Fung, and V.B. Reddy Phospholipid bicelles with positive anisotropy of the magnetic susceptibility Journal of the American Chemical Society 123 2001 1537 1538
20. P. Cicuta, S.L. Keller, and S.L. Veatch Diffusion of liquid domains in lipid bilayer membranes Journal of Physical Chemistry B 111 2007 3328 3331
21. R.M. Cotts, M.J.R. Hoch, T. Sun, and J.T. Markert Pulsed field gradient stimulated echo methods for improved NMR diffusion measurements in heterogeneous systems Journal of Magnetic Resonance 83 1989 252 266
22. P.R. Cullis Lateral diffusion rates of phosphatidylcholine in vesicle membranes-effects of cholesterol and hydrocarbon phase-transition Federation of European Biological Societies Letters 70 1976 223 228
23. J.H. Davis The description of membrane lipid conformation, order and dynamics by 2H-NMR Biochimica et Biophysica Acta 737 1983 117 171
24. C.A. Day, and A.K. Kenworthy Tracking microdomain dynamics in cell membranes Biochimica et Biophysica Acta, Biomembranes 1788 2009 245 253
25. A.A. De Angelis, D.H. Jones, C.V. Grant, S.H. Park, M.F. Mesleh, and S.J. Opella NMR experiments on aligned samples of membrane proteins Methods in Enzymology 394 2005 350 382
26. A.A. De Angelis, A.A. Nevzorov, S.H. Park, S.C. Howell, A.A. Mrse, and S.J. Opella High-resolution NMR spectroscopy of membrane proteins in aligned bicelles Journal of the American Chemical Society 126 2004 15340 15341
27. E.R. deAzevedo, T.J. Bonagamba, and K. Schmidt-Rohr Pure-exchange solid-state NMR Journal of Magnetic Resonance 142 2000 86 96
28. E.R. deAzevedo, W.-G. Hu, T.J. Bonagamba, and K. Schmidt-Rohr Centerband-only detection of exchange: efficient analysis of dynamics in solids by NMR Journal of the American Chemical Society 121 1999 8411 8412
29. E.R. deAzevedo, W.-G. Hu, T.J. Bonagamba, and K. Schmidt-Rohr Principles of centerband-only detection of exchange in solid-state nuclear magnetic resonance, and extension to four-time centerband-only detection of exchange Journal of Chemical Physics 112 2000 8988 9001
30. E.R. deAzevedo, J.R. Tozoni, K. Schmidt-Rohr, and T.J. Bonagamba Analysis of one-dimensional pure-exchange NMR experiments for studying dynamics with broad distribution of correlation times Journal of Chemical Physics 122 2005 154506 154511
31. M.K. Doeven, J.H.A. Folgering, V. Krasnikov, E.R. Geertsma, G. van den Bogaart, and B. Poolman Distribution, lateral mobility and function of membrane proteins incorporated into giant unilamellar vesicles Biophysical Journal 88 2005 1134 1142
32. C. Dolainsky, M. Unger, M. Bloom, and T.M. Bayerl Two-dimensional exchange H-2 NMR experiments of phospholipid-bilayers on a spherical solid support Physical Review E 51 1995 4743 4750
33. P.-O. Eriksson, and G. Lindblom Lipid and water diffusion in bicontinuous cubic phases measured by NMR Biophysical Journal 64 1993 129 136
34. D.B. Fenske, and H.C. Jarrell P-31 2-dimensional solid-state exchange NMR-application to model membranes and biological systems Biophysical Journal 59 1991 55 69
35. D.B. Fenske, M. Letellier, R. Roy, I.C.P. Smith, and H.C. Jarrell Effect of calcium on the dynamic behaviour of sialylglycerolipids and phospholipids in mixed model membranes-A H-2 and P-31 study Biochemistry 30 1991 10542 10550
36. B.M. Fung, A.K. Khitrin, and K. Ermolaev An improved broadband decoupling sequence for liquid crystals and solids Journal of Magnetic Resonance 142 2000 97 101
37. H.C. Gaede, and K. Gawrisch Lateral diffusion rates of lipid, water, and a hydrophobic drug in a multilamellar liposome Biophysical Journal 85 2003 1734 1740
38. H.C. Gaede, W.-M. Yau, and K. Gawrisch Electrostatic contributions to indole-lipid interactions Journal of Physical Chemistry B 109 2005 13014 13023
39. Y. Gambin, N.S. Gov, M. Genest, R.S. Hodges, and W. Urbach Lateral mobility of proteins in liquid membranes revisited Proceedings of the National Academy of Science of the United States of America 103 2006 2098 2102
40. Y. Gambin, M. Reffay, E. Siercki, F. Homble, R.S. Hodges, N.S. Gov, N. Taulier, and W. Urback Variation of the lateral mobility of transmembrane peptides with hydrophobic mismatch Journal of Physical Chemistry B 114 2010 3559 3566
41. V. Gérardy-Montouillout, C. Malveau, P. Tekely, Z. Olender, and Z. Luz ODESSA, a new 1D NMR exchange experiment for chemically equivalent nuclei in rotating solids Journal of Magnetic Resonance, Series A 123 1996 7 15
42. M. Glaser Lipid domains in biological membranes Current Opinion in Structural Biology 3 1993 475 481
43. K.J. Glover, J.A. Whiles, M.J. Wood, G. Melacini, E.A. Komives, and R.R. Vold Conformational dimorphism and transmembrane orientation of prion protein residues 110-136 in bicelles Biochemistry 40 2001 13137 13142
44. G. Guigas, and M. Weiss Size-dependent diffusion of membrane inclusions Biophysical Journal 91 2006 2393 2398
45. E.L. Hahn Spin echoes Physical Review 80 1950 580 594
46. H.-T. He, and D. Marguet Detecting nanodomains in living cell membrane by fluorescence correlation spectroscopy Annual Review of Physical Chemistry 62 2011 417 436
47. K.P. Howard, and S.J. Opella High-resolution solid-state NMR spectra of integral membrane proteins reconstituted into magnetically oriented phospholipid bilayers Journal of Magnetic Resonance B 112 1996 91 94
48. K. Jacobson, F. Zhang, and T.T. Tsay Fluorescence recovery after photobleaching techniques to measure translational mobility in microscopic samples Scanning Microscopy 5 1991 357 362
49. J. Jeener, B.H. Meier, P. Bachmann, and R.R. Ernst Investigation of exchange processes by 2-dimensional NMR-spectroscopy Journal of Chemical Physics 71 1979 4546 4553
50. T.M. Jovin, and W.L.C. Vaz Rotational and translational diffusion in membranes measured by flourescence and phosphorescence methods Methods in Enzymology 172 1989 471 513
51. M. Kadkhodaie, O. Rivas, M. Tan, A. Mohebbi, and A.J. Shaka Broadband homonuclear cross polarization using flip-flop spectroscopy Journal of Magnetic Resonance 91 1991 437 443
52. N. Kahya, and P. Schwille Fluorescence correlation studies of lipid domains in model membranes (Review) Molecular Membrane Biology 23 2006 29 39
53. N. Kaji, M. Tokeshi, and Y. Baba Single-molecule measurements with a single quantum dot Chemical Record 7 2007 295 304
54. J. Kärger NMR self-diffusion studies in heterogeneous systems Advances in Colloid and Interface Science 23 1985 129 148
55. J. Kärger, H. Pfeifer, and W. Heink Principles and applications of self-diffusion measurements by nuclear magnetic resonance Advances in Magnetic Resonance 1988 Academic Press, Inc. pp. 1-89
56. J. Katsaras, T.A. Harroun, J. Pencer, and M.-P. Nieh "Bicellar" lipid mixtures as used in biochemical and biophysical studies Naturwissenschaften 92 2005 355 366
57. H.J. Kim, S.C. Howell, W.D. Van Horn, Y.H. Jeon, and C.R. Sanders Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins Progress in Nuclear Magnetic Resonance Spectroscopy 55 2009 335 360
58. C. Kim, J. Spano, E.-K. Park, and S. Wi Evidence of pores and thinned lipid bilayers induced in oriented lipid membranes interacting with the antimicrobial peptides, magainin-2 and aurein-3.3 Biochimica et Biophysica Acta, Biomembranes 1788 2009 1482 1496
59. T. Kimura, K. Cheng, K.C. Rice, and K. Gawrisch Location, structure, and dynamics of the synthetic cannabinoid ligand CP-55,940 in lipid bilayers Biophysical Journal 96 2009 4916 4924
60. V. King, M. Parker, and K.P. Howard Pegylation of magnetically oriented lipid bilayers Journal of Magnetic Resonance 142 2000 177 182
61. N. Klonis, M. Rug, I. Harper, M. Wickham, A. Cowman, and L. Tilley Fluorescence photobleaching analysis for the study of cellular dynamics European Biophysical Journal 31 2002 36 51
62. T. Köchy, and T.M. Bayerl Lateral diffusion-coefficients of phospholipids in spherical bilayers on a solid support measured by H-2-nuclear-magnetic-resonance relaxation Physical Review E 47 1993 2109 2116
63. D. Kolin, and P. Wiseman Advances in image correlation spectroscopy: measuring number densities, aggregation states, and dynamics of fluorescently labeled macromolecules in cells Cell Biochemistry and Biophysics 49 2007 141 164
64. J. Kriegsmann, I. Gregor, I. von der Hocht, J. Klare, M. Engelhard, J. Enderlein, and J. Fitter Translational diffusion and interaction of a photoreceptor and its cognate transducer observed in giant unilamellar vesicles by using dual-focus FCS ChemBioChem 10 2009 1823 1829
65. 2O multilayers by pulsed NMR Chemistry and Physics of Lipids 25 1979 135 139
66. A. Kusumi, H. Ike, C. Nakada, K. Murase, and T. Fujiwara Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules Seminars in Immunology 17 2005 3 21
67. A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R.S. Kasai, J. Kondo, and T. Fujiwara Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules Annual Review of Biophysics and Biomolecular Structure 34 2005 351 378
68. D.W. Larsen, J.G. Boylan, and B. Cole Axially-symmetrical P-31 NMR line-shapes with selective excitation in the presence of lateral diffusion on a curved surface Journal of Physical Chemistry 91 1987 5631 5634
69. D.D. Lasic, and D. Needham The "Stealth" liposome: a prototypical biomaterial Chemical Reviews 95 1995 2601 2628
70. L.L. Latour, P.P. Mitra, R.L. Kleinberg, and C.H. Sotak Time-dependent diffusion-coefficient of fluids in porous-media as a probe of surface-to-volume ratio Journal of Magnetic Resonance Series A 101 1993 342 346
71. B.S. Lee, S.A. Mabry, A. Jonas, and J. Jonas C High-pressure proton NMR study of lateral self-diffusion of phosphatidylcholines in sonicated unilamellar vesicles Chemistry and Physics of Lipids 78 1995 103 117
72. C.C. Lee, and N.O. Petersen The lateral diffusion of selectively aggregated peptides in giant unilamellar vesicles Biophysical Journal 84 2003 1756 1764
73. V. Levi, and E. Gratton Exploring dynamics in living cells by tracking single particles Cell Biochemistry and Biophysics 48 2007 1 15
74. G. Lindblom, and G. Gröbner NMR on lipid membranes and their proteins Current Opinion in Colloid and Interface Science 11 2006 24 29
75. G. Lindblom, and G. Orädd NMR-studies of translational diffusion in lyotropc liquid-crystals and lipid membranes Progress in Nuclear Magnetic Resonance Spectroscopy 26 1994 483 515
76. G. Lindblom, and G. Orädd Order and disorder in a liquid crystalline bilayer: pulsed field gradient NMR studies of lateral phase separation Journal of Dispersion Science and Technology 28 2007 55 61
77. G. Lindblom, and G. Orädd Lipid lateral diffusion and membrane heterogeneity Biochimica et Biophysica Acta, Biomembranes 1788 2009 234 244
78. G. Lindblom, and L. Rilfors Cubic phases and isotropic structures formed by membrane lipids-possible biological relevance Biochimica et Biophysica Acta 988 1989 221 256
79. G. Lindblom, and H. Wennerström Amphiphile diffusion in model membrane systems studied by pulsed NMR Biophysical Chemistry 6 1977 167 171
80. G. Lindblom, H. Wennerström, and G. Arvidson Translation diffusion in model membranes studied by nuclear magnetic resonance International Journal of Quantum Chemistry 12 1977 153 158
81. P.H.M. Lommerse, H.P. Spaink, and T. Schmidt In vivo plasma membrane organization: results of biophysical approaches Biochimica et Biophysica Acta, Biomembranes 1664 2004 119 131
82. E. London, and G.W. Feigenson Phosphorus NMR analysis of phospholipids in detergents Journal of Lipid Research 20 1979 408 412
83. C. Loudet, S. Manet, S. Gineste, R. Oda, M.-F. Achard, and E.J. Dufourc Biphenyl bicelle disks align perpendicular to magnetic fields on large temperature scales: a study combining synthesis, solid-state NMR, TEM, and SAXS Biophysical Journal 92 2007 3949 3959
84. I.J. Lowe Free induction decays in rotating solids Physical Review Letters 2 1959 285 287
85. V. Luzzati, A. Tardieu, T. Gulik-Krzywicki, E. Rivas, and F. Reiss-Husson Structure of the cubic phases of lipid-water systems Nature 220 1968 485 488 (London)
86. Z. Luz, P. Tekely, and D. Reichert Slow exchange involving equivalent sites in solids by one-dimensional MAS NMR techniques Progress in Nuclear Magnetic Resonance Spectroscopy 41 2002 83 113
87. W.E. Maas, F.H. Laukien, and D.G. Cory Gradient, high resolution, magic angle sample spinning NMR Journal of the American Chemical Society 118 1996 13085 13086
88. P.M. Macdonald, and R. Soong Diffusion NMR and bicelle morphology Canadian Journal of Chemistry 89 2011 1021 1035
89. R. Macháň, and M. Hof Recent developments in fluorescence correlation spectroscopy for diffusion measurements in planar lipid membranes International Journal of Molecular Science 11 2010 427 457
90. P.A.B. Marasinghe, J.J. Buffy, K. Schmidt-Rohr, and M. Hong Membrane curvature change induced by an antimicrobial peptide detected by 31P exchange NMR Journal of Physical Chemistry B 109 2005 22036 22044
91. I. Marcotte, and M. Auger Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins Concepts in Magnetic Resonance 24A 2005 17 37
92. I. Marcotte, E.J. Dufourc, M. Ouellet, and M. Auger Interaction of the neuropeptide Met-enkephalin with zwitterionic and negatively charged bicelles as viewed by P-31 and H-2 solid-state NMR Biophysical Journal 85 2003 328 339
93. D. Marsh, R. Bartucci, and L. Sportelli Lipid membranes with grafted polymers: physicochemical aspects Biochimica et Biophysica Acta, Biomembranes 1615 2003 33 59
94. P.P. Mitra, and P.N. Sen Effects of microgeometry and surface relaxation on NMR pulsed-field-gradient experiments-simple pore geometries Physical Review B 45 1992 143 156
95. P.P. Mitra, P.B. Sen, L.M. Schwartz, and P. Ledoussal Diffusion propagator as a probe of the structure of porous-media Physical Review Letters 68 1992 3555 3558
96. P.P. Mitra, P.B. Sen, and L.M. Schwatrz Short-time behavior of the diffusion-coefficient as a geometrical probe of porous-media Physical Review B 47 1993 8565 8574
97. K.I. Momot, and P.W. Kuchel Convection-compensating diffusion experiments with phase-sensitive double-quantum filtering Journal of Magnetic Resonance 174 2005 229 236
98. C.W. Mullineaux FRAP analysis of photosynthetic membranes Journal of Experimental Botany 55 2004 1207 1211
99. A. Naji, A.J. Levine, and P.A. Pincus Corrections to the Saffman-Delbrück mobility for membrane bound proteins Biophysical Journal 93 2007 L49 L51
100. A.A. Nevzorov, M.F. Mesleh, and S.J. Opella Structure determination of aligned samples of membrane proteins by NMR spectroscopy Magnetic Resonance in Chemistry 42 2004 162 171
101. W. Niederberger, and J. Seelig Phosphorus-31 chemical-shift anisotropy in unsonicated phospholipid bilayers Journal of the American Chemical Society 98 1976 3704 3706
102. M.-P. Nieh, V.A. Raghunathan, G. Pabst, T. Harroun, K.J. Nagashima, H. Morales, K. Katsaras, and P.M. Macdonald Temperature driven annealing of perforations in bicellar model membranes Langmuir 27 2011 4838 4847
103. 1H-NMR: evidence for reversed micelles in the cubic phase Biophysical Journal 68 1995 1856 1863
104. G. Orädd, and G. Lindblom Lateral diffusion studied by pulsed field gradient NMR on oriented lipid membranes Magnetic Resonance in Chemistry 42 2004 123 131
105. G. Orädd, and G. Lindblom Pfg NMR studies of lateral diffusion in oriented lipid bilayers Spectroscopy 19 2005 191 198
106. D.M. Owen, D. Williamson, C. Rentero, and K. Gaus Quantitative microscopy: protein dynamics and membrane organization Traffic 10 2009 962 971
107. A. Pampel, J. Kärger, and D. Michel Lateral diffusion of a transmembrane peptide in lipid bilayers studied by pulsed field gradient NMR in combination with magic angle spinning Chemical Physics Letters 379 1993 555 561
108. K.D. Park, and Y.J. Lee Slice-selected LED and BPPLED: application of slice selection to DOSY Magnetic Resonance in Chemistry 44 2006 887 891
109. R. Peters, and R.J. Cherry Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbruck equations Proceedings of the National Academy of Science of the United States of America 70 1982 4317 4321
110. F. Picard, M.-J. Paquet, E. Dufourc, and M. Auger Measurement of the lateral diffusion of dipalmitoylphosphatidylcholine adsorbed on silica beads in the absence and presence of melittin: a P-31 two-dimensional exchange solid-state NMR study Biophysical Journal 74 1998 857 868
111. F. Picard, M.-J. Paquet, J. Levesque, A. Bélanger, and M. Auger P-31 NMR first spectral moment study of the partial magnetic orientation of phospholipid membranes Biophysical Journal 77 1999 888 902
112. F. Pinaud, S. Clarke, A. Sittner, and M. Dahan Probing cellular events, one quantum dot at a time Nature Methods 7 2010 275 285
113. S.F. Poget, and M.E. Girvin Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better Biochimica et Biophysica Acta, Biomembranes 1768 2007 3098 3106
114. 1H MAS NMR Biophysical Journal 87 2004 1741 1751
115. I.V. Polozov, L. Bezrukov, K. Gawrisch, and J. Zimmerberg Progressive ordering with decreasing temperature of the phospholipids of influenza virus Nature Chemical Biology 4 2008 248 255
116. W.S. Price Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part 1. Basic theory Concepts in Magnetic Resonance 9 1997 299 336
117. W.S. Price Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part II. Experimental aspects Concepts in Magnetic Resonance 10 1998 197 237
118. W.S. Price, F. Elwinger, C. Vigouroux, and P. Stilbs PGSE-Watergate, a new tool for NMR diffusion-based studies of ligand-macromolecule binding Magnetic Resonance in Chemistry 40 2002 391 395
119. R.S. Prosser, H. Bryant, R.G. Bryant, and R.R. Vold Lanthanide chelates as bilayer alignment tools in NMR studies of membrane-associated peptides Journal of Magnetic Resonance 141 1999 256 260
120. R.S. Prosser, F. Evanics, J.L. Kitevski, and M.S. Al-Abdul-Wahid Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins Biochemistry 45 2006 8453 8465
121. R.S. Prosser, S.A. Hunt, J.A. DiNatale, and R.R. Vold Magnetically aligned membrane model systems with positive order parameter: switching the sign of S-zz with paramagnetic ions Journal of the American Chemical Society 118 1996 269 270
122. R.S. Prosser, J.S. Hwang, and R.R. Vold Magnetically aligned phospholipid bilayers with positive ordering: a new model membrane system Biophysical Journal 74 1998 2405 2418
123. R.S. Prosser, and I.V. Shiyanovskaya Lanthanide ion assisted magnetic alignment of model membranes and macromolecules Concepts in Magnetic Resonance 13 2001 19 31
124. R.S. Prosser, V.B. Volkov, and I.V. Shiyanovskaya Novel chelate-induced magnetic alignment of biological membranes Biophysical Journal 75 1998 2163 2169
125. G. Rayan, J.-E. Guet, N. Taulier, F. Pincet, and W. Urbach Recent applications of fluorescence recovery after photobleaching (FRAP) to membrane bio-macromolecules Sensors 10 2010 5927 5948
126. P. Ram, and J.H. Prestegard Magnetic field induced ordering of bile salt/phospholipid micelles: new media for NMR structural investigations Biochimica et Biophysica Acta, Biomembranes 940 1988 289 294
127. S. Ramadurai, A. Holt, C. Krasnikov, G. can den Bogaart, J.A. Killian, and B. Poolman Lateral diffusion of membrane proteins Journal of the American Chemical Society 131 2009 12650 12656
128. S. Ramadurai, A. Holt, L.V. Schäfer, V.V. Krasnikov, D.T.S. Rijkers, S.J. Marrink, J.A. Killian, and B. Poolman Influence of hydrophobic mismatch and amino acid composition on the lateral diffusion of transmembrane peptides Biophysical Journal 99 2010 1447 1454
129. S. Ramadurai, R. Duurkens, V. Krashikov, and B. Poolman Lateral diffusion of membrane proteins: consequences of hydrophobic mismatch and lipid composition Biophysical Journal 99 2010 1482 1489
130. D. Reichert, O. Pascui, T.J. Bonagamba, E.R. deAzevedo, and A. Schmidt Scaling-down the CSA recoupling in S-CODEX 1D-MAS exchange experiments International Journal of Molecular Science 380 2003 583 588
131. D. Reichert, H. Zimmermann, P. Tekely, R. Poupko, and Z. Luz Time-reverse ODESSA. A 1D exchange experiment for rotating solids with several groups of equivalent nuclei Journal of Magnetic Resonance 125 1997 245 258
132. E.A.J. Reits, and J.J. Neefjes From fixed to FRAP: measuring protein mobility and activity in living cells Nature Cell Biology 3 2001 E145 E147
133. L. Rilfors, P.-O. Eriksson, G. Arvidson, and G. Lindblom Relationship between three-dimensional arrays of "lipidic particles" and bicontinuous cubic lipid phases Biochemistry 25 1986 7702 7711
134. K. Ritchie, R. Iino, T. Fujiwara, K. Murase, and A. Kusumi The fence and picket structure of the plasma membrane of live cells as revealed by single molecule techniques (Review) Molecular Membrane Biology 20 2003 13 18
135. P.G. Saffman, and M. Delbrück Brownian motion in biological membranes Proceedings of the National Academy of Sciences of the United States of America 73 1975 3111 3113
136. P.G. Saffman Brownian motion in thin sheets of viscous fluid Journal of Fluid Mechanics 73 1976 593 602
137. 31P CODEX NMR Chemistry and Physics of Lipids 165 2012 721 730
138. 13C NMR of unlabeled phosphatidylcholine bilayers: spectral assignments and measurement of carbon-phosphorus dipolar couplings and 13C chemical shift anisotropies Biophysical Journal 64 1993 171 181
139. C.R. Sanders, B.J. Hare, K.P. Howard, and J.H. Prestegard Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules Progress in Nuclear Magnetic Resonance Spectroscopy 26 1994 421 444
140. C.R. Sanders, A.K. Hoffmann, D.N. Gray, M.H. Keyes, and C.D. Ellis French swimwear for membrane proteins ChemBioChem 5 2004 423 426
141. C.R. Sanders, and G.C. Landis Facile acquisition and assignment of oriented sample NMR-spectra for bilayer surface-associated proteins Journal of the American Chemical Society 116 1994 6470 6471
142. C.R. Sanders, and G.C. Landis Reconstitution of membrane-proteins into lipid-rich bilayered mixed micelles for NMR-studies Biochemistry 34 1995 4030 4040
143. C.R. Sanders, and K. Oxenoid Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins Biochimica et Biophysica Acta 1508 2000 129 145
144. C.R. Sanders, and J.H. Prestegard Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO Biophysical Journal 58 1990 447 460
145. C.R. Sanders, J.E. Schaff, and J.H. Prestegard Orientation behavior of phosphatidylcholine bilayers in the presence of aromatic amphiphiles and a magnetic-field Biophysical Journal 64 1993 1069 1080
146. C.R. Sanders, and J.P. Schwonek Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR Biochemistry 31 1992 8898 8905
147. C.R. Sanders, and F. Sönnichsen Solution NMR of membrane proteins: practice and challenges Magnetic Resonance in Chemistry 44 2006 S24 S40
148. M.J. Saxton Lateral diffusion of lipids and proteins Current Topics in Membranes 48 1999 229 282
149. 13C NMR of polymers spinning at the magic angle Journal of the American Chemical Society 98 1976 1031 1032
150. 1H pulsed field gradient magic angle spinning NMR Biophysical Journal 89 2005 2504 2512
151. H.A. Scheidt, A. Pampel, L. Nissler, R. Gebhardt, and D. Huster Investigation of the membrane localization and distribution of flavonoids by high-resolution magic angle spinning NMR spectroscopy Biochimica et Biophysica Acta 1663 2004 97 107
152. K.V. Schenker, D. Suter, and A. Pines Broadband heteronuclear decoupling in the presence of homonuclear dipolar and quadrupolar interactions Journal of Magnetic Resonance 73 1987 99 113
153. 31P NMR spectroscopy of phospholipids; from micelles to membranes Current Analytical Chemistry 3 2007 283 301
154. A.J. Shaka, J. Keeler, and R. Freeman Evaluation of a new broadband decoupling sequence: WALTZ-16 Journal of Magnetic Resonance 53 1983 313 340
155. J. Seelig Deuterium magnetic resonance: theory and application to lipid membranes Quarterly Review of Biophysics 10 1977 353 418
156. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes Biochimica et Biophysica Acta 515 1978 105 140
157. P. Somerharju, J.A. Virtanen, and K.H. Cheng Lateral organisation of membrane lipids: the superlattice view Biochimica et Biophysica Acta, Molecular and Cell Biology of Lipids 1440 1999 32 48
158. 1H NMR Biophysical Journal 88 2005 255 268
159. R. Soong, and P.M. Macdonald Influence of the long-chain/short-chain amphiphile ratio on lateral diffusion of PEG-lipid in magnetically aligned lipid bilayers as measured via pulsed-field-gradient NMR Biophysical Journal 89 2005 1850 1860
160. R. Soong, and P.M. Macdonald PEG molecular weight and lateral diffusion of PEG-ylated lipids in magnetically aligned bicelles Biochimica et Biophysica Acta, Biomembranes 1768 2007 1805 1814
161. R. Soong, D. Majonis, and P.M. Macdonald Size of bicelle defects probed via diffusion nuclear magnetic resonance of PEG Biophysical Journal 97 2009 796 805
162. N. Sotirhos, B. Herslof, and L. Kenne Quantitative analysis of phospholipids by 31P-NMR Journal of Lipid Research 27 1986 386 392
163. F. Stallmach, and P. Galvosas Spin echo NMR diffusion studies Annual Reports on NMR Spectroscopy 61 2007 51 131
164. E.O. Stejskal, and J.E. Tanner Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient Journal of Chemical Physics 42 1965 288
165. P. Stilbs Fourier transform pulsed-gradient spin-echo studies of molecular diffusion Progress in Nuclear Magnetic Resonance Spectroscopy 19 1987 1 45
166. J. Struppe, E.A. Komives, S.S. Taylor, and R.R. Vold H-2 NMR studies of a myristoylated peptide in neutral and acidic phospholipid bicelles Biochemistry 37 1998 15523 15527
167. 13C PGSE NMR experiment with heteronuclear dipolar decoupling to measure diffusion in liquid crystals and solids Journal of Magnetic Resonance 142 2000 102 110
168. C. Tan, B.M. Fung, and G. Cho Phospholipid bicelles that align with their normals parallel to the magnetic field Journal of the American Chemical Society 124 2002 11827 11832
169. J.E. Tanner Use of the stimulated echo in NMR diffusion studies Journal of Chemical Physics 52 1970 2523 2526
170. N. Tjandra, and A. Bax Direct measurement of distance and angles in biomolecules by NMR in a dilute liquid crystalline medium Science 278 1997 1111 1114
171. J.-F. Tocanne, L. Dupou-Cézanne, and A. Lopez Lateral diffusion of lipids in model and natural membranes Progress in Lipid Research 33 1994 203 237
172. J.W. Traer, K.J. Soo, M. Vijayakumar, and G.R. Goward Elucidating the time scale and geometry of phosphate and phosphonate rotation in solid acid electrolytes using multinuclear NMR Journal of Physical Chemistry C 115 2011 6064 6072
173. M.N. Triba, D.E. Warshawski, and P.F. Devauz Reinvestigation by phosphorus NMR of lipid distribution in bicelles Biophysical Journal 88 2005 1887 1901
174. A. Triller, and D. Choquet New concepts in synaptic biology derived from single-molecule imaging Neuron 59 2008 359 374
175. W.L.C. Vaz, R.M. Clegg, and D. Hallmann Translational diffusion of lipids in liquid crystalline phase phosphatidylcholine multibilayers. A comparison of experiment with theory Biochemistry 24 1985 781 786
176. W.L.C. Vaz, and E. Melo Fluorescence spectroscopic studies on phase heterogeneity in lipid bilayer membranes Journal of Fluorescence 11 2001 255 271
177. R.R. Vold, A.J. Deese, and R.S. Prosser Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides Journal of Biomolecular NMR 9 1997 329 335
178. J.A. Whiles, R. Brasseur, K.J. Glover, G. Melacini, E.A. Komives, and R.R. Vold Orientation and effects of mastoparan X on phospholipid bicelles Biophysical Journal 80 2001 280 293
179. J.A. Whiles, R. Deems, R.R. Vold, and E.A. Dennis Bicelles in structure-function studies of membrane-associated proteins Bioinorganic Chemistry 30 2002 431 442
180. S. Wi, and C. Kim Pore structure, thinning effect, and lateral diffusive dynamics of oriented lipid membranes interacting with antimicrobial peptide Protegrin-1: 31P and 2H solid-state NMR study Journal of Physical Chemistry B 112 2008 11402 11414
181. Y. Yang, M. Schuster, B. Blümich, and H.W. Spiess Dynamic magic-angle spinning nmr spectroscopy: exchange-induced sidebands Chemical Physics Letters 139 1987 239 243