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Deuterium magnetic resonance: theory and application to lipid membranes

Published online by Cambridge University Press:  17 March 2009

Joachim Seelig
Affiliation:
Department of Biophysical Chemistry, Biocenter of the University of Basel, Klingelbergstrasse 70, CH-4056 Basel, Switzerland

Extract

Proton and carbon-13 nmr spectra of unsonicated lipid bilayers and biological membranes are generally dominated by strong proton–proton and proton–carbon dipolar interactions. As a result the spectra contain a large number of overlapping resonances and are rather difficult to analyse. Nevertheless, important information on the structure and dynamic behaviour of lipid systems has been provided by these techniques (Wennerström & Lindblom, 1977).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1977

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References

REFERENCES

Abragam, A. (1961). The Principles of Nuclear Magnetism. London: Oxford University Press.Google Scholar
Abrahamsson, S. & Pascher, I. (1966). Crystal and molecular structure of L-α-glycery1phosphorylcho line. Acta crystallogr. 21, 7987.CrossRefGoogle Scholar
Arvidson, G., Lindblom, G. & Drakenberg, T. (1975). A novel approach to the study of mammalian cell membranes using deuterium nmr. FEBS Lett. 54, 249–52.CrossRefGoogle Scholar
Barnes, R. G. (1974). Deuteron quadrupole tensors in solids. In Advances in Nuclear Quadrupole Resonance, vol. I (ed. Smith, J. A. S.), pp. 335–55. London: Heyden.Google Scholar
Barnes, R. G. & Bloom, J. W. (1973). Deuteron quadrupole couplings in deuterated glycine. Molec. Phys. 25, 493–4.CrossRefGoogle Scholar
Belle, J. & Bothorel, P. (1974.). Theoretical study of spin labeled aliphatic chains in bilayers. Biochem. biophys. Res. Commun. 58, 433–6.CrossRefGoogle ScholarPubMed
Boden, N., Jackson, P., Levine, Y. K. & Ward, A. J. I. (1976). Intramolecular disorder and its relation to mesophase structure in lipid/water mixtures. Biochim. biophys. Acta 419, 395403.CrossRefGoogle ScholarPubMed
Bothorel, P., Belle, J. & Lemaire, B. (1974). Theoretical study of aliphatic chain structure in mono- and bilayers. Chem. Phys. Lipids 12, 96116.CrossRefGoogle ScholarPubMed
Brown, G. H., Doane, J. W. & Neff, V. D. (1971). A Review of the Structure and Physical Properties of Liquid Crystals. London: Butterworth.Google Scholar
Büldt, G., Zaccai, G., Seelig, J. & Gally, H. (1977). (Manuscript in preparation.)Google Scholar
Burnett, L. J. & Müller, B. H. (1971). Deuteron quadrupole coupling constants in three solid deuterated paraffin hydrocarbons: C2D6, C4D10, C6D14. J. chem. Phys. 55, 5829–31.CrossRefGoogle Scholar
Cadenhead, D. A. & Müller-Landau, F. (1975). Monolayer studies of pure nitroxide fatty acid spin-label probes. Adv. Chern. Ser. 144, 294307.CrossRefGoogle Scholar
Caspary, W. J., Millett, F., Reichbach, M. & Dailey, B. P. (1969). NMR determination of deuterium quadrupole coupling constants in nematic solutions. J. chem. Phys. 51, 623–7.CrossRefGoogle Scholar
Chan, S. I., Seiter, C. H. A. & Feigenson, G. W. (1972). Anisotropic and restricted molecular motion in lecithin bilayers. Biochem. biophys. Res. Commun. 46, 1488–92.CrossRefGoogle ScholarPubMed
Chan, S. I., Sheetz, M. P., Seiter, C. H. A., Feigenson, G. W., Hsu, M., Lau, A. & Yau, A. (1973). Nuclear magnetic resonance studies of the structure of model membrane systems: The effect of surface curvature. Ann. N.Y. Acad. Sci., U.S.A. 222, 499522.CrossRefGoogle ScholarPubMed
Charvolin, J., Manneville, P. & Deloche, B. (1973). Magnetic resonance of perdeuterated potassium laurate in oriented soap-water multilayers. Chem. Phys. Letters 23, 345–8.CrossRefGoogle Scholar
Chiba, T. (1962). Deuteron magnetic resonance study of several deuterated ammonium salts. J. chem. Phys. 36, 1122–6.CrossRefGoogle Scholar
Cohen, M. H. & Reif, F. (1957). Quadrupole effects in nuclear magnetic resonance studies of solids. Solid St. Phys. 5, 321438.CrossRefGoogle Scholar
Davis, J. H. & Jeffrey, K. R. (1977). The temperature dependence of chain disorder in potassium palmitate—water. A deuterium nmr study. Chem. Phys. Lipids (in the Press).Google Scholar
Derbyshire, W., Gorvin, T. & Warner, D. (1969). A deuteron magnetic resonance study of a single crystal of deuterated malonic acid. Molec. Phys. 17, 401–7.CrossRefGoogle Scholar
De, Titta G. T. & Craven, B. M. (1971). Conformation of O-(L-α-glyceryl-phosphoryl)-ethanolamine in the crystal structure of its monohydrate. Nature (New Biol.) 233, 118–20.Google Scholar
De, Titta G. T. & Craven, B. M. (1973). L-α-Glycerylphosphorylethanolamine monohydrate. Acta crystallogr. B 29, 1354–7.Google Scholar
Devaux, P. & McConnell, H. M. (1972). Lateral diffusion in spin-labeled phosphatidylcholine multilayers. J. Am. chem. Soc. 94, 4475–81.CrossRefGoogle ScholarPubMed
Diehl, P. (1974). A survey of recent advances in 2D and 3T-NMR. In Nuclear Magnetic Resonance Spectra of Nuclei Other than Protons (ed. Axenrod, T. and Graham, A. W.), pp. 275–85. London: Wiley.Google Scholar
Diehl, P. & Niederberger, W. (1974). Proton decoupling in deuteron magnetic resonance spectra of oriented molecules. J. Magn. Reson. 15, 391–2.Google Scholar
Egozy, Y., Loewenstein, A. & Silver, B. L. (1970). Deuterium relaxation in C6D6 dissolved in a liquid crystal. Molec. Phys. 19, 177–82.CrossRefGoogle Scholar
Emsley, J. W., Lindon, J. C. & Tabony, J. (1973 a). NMR spectra of ethanol and partially deuterated ethanols as solutes in a nematic phase. Molec. Phys. 26, 1485–98.CrossRefGoogle Scholar
Emsley, J. W., Lindon, J. C. & Tabony, J. (1973 b). Measurement of deuterium quadrupole coupling constants of CD3 groups by 1H-[2H] NMR studies of nematic solutions. Molec. Phys. 26, 1499–509.CrossRefGoogle Scholar
Finer, E. G. (1973). Interpretation of deuteron magnetic resonance spectroscopic studies of the hydration of macromolecules. J. Chem. Soc. Faraday Trans. 11 69, 1590–600.CrossRefGoogle Scholar
Finer, E. G. & Darke, A. (1974.). Phospholipid hydration studied by deuteron magnetic resonance spectroscopy. Chem. Phys. Lipids 12, 116.CrossRefGoogle Scholar
Flory, P. J. (1969). Statistical Mechanics of Chain Molecules. New York: Interscience.CrossRefGoogle Scholar
Fujiwara, F., Reeves, L. W., Tracey, A. S. & Wilson, L. A. (1974). Studies of membrane processes. III. Deuterium magnetic resonance as a tool in studies of the lipophilic region of membrane systems. J. Am. chem. Soc. 96, 5249–50.CrossRefGoogle Scholar
Fung, B. M. (1974). Nuclear quadrupole coupling constants. In Critical Evaluation of Chemical and Physical Structural Information (Lide, D. R. & Paul, M. A.), pp.436–48. Washington, D.C.: National Academy of Sciences.Google Scholar
Fung, B. M. & Wei, I. Y. (1970). Proton and deuteron magnetic resonance of phenylsilane-d3, phenylphosphine-d2, and benzenethio-d in liquid crystal solutions. J. Am. chem. Soc. 92, 1497–501.CrossRefGoogle Scholar
Gaber, B. P. & Peticolas, W. L. (1977). On the quantitative interpretation of biomembrane structure by Raman spectroscopy. Biochim. biophys. Acta 465, 260–74.CrossRefGoogle ScholarPubMed
Gaffney, B. J. & McConnell, H. M. (1974). The paramagnetic resonance spectra of spin labels in phospholipid membranes. J. Magn. Reson. 16, 128.Google Scholar
Gallot, B. & Skoulious, A. (1966). Interactions électriques dans les phases méomorphes des systemes amphiphile-eau: Rôle de la teneur en eau, de la longueur de Ia chaine paraffinique, de Ia nature du cation, et de la température. Kolloid Z. u. Z. Polymere 208, 3743.CrossRefGoogle Scholar
Gally, H. U., Niederberger, W. & Seelig, J. (1975). Conformation and motion of the choline head group in bilayers of dipalmitoyl-3-sn-phosphatidylcholine. Biochemistry, N.Y. 14, 3647–52.CrossRefGoogle ScholarPubMed
Gally, H., Seelig, A. & Seelig, J. (1976). Cholesterol induced rod-like motion of fatty acyl chains in lipid bilayers. A deuterium magnetic resonance study. Hoppe-Seyler's Z. physiol. Chem. 357, 1447–50.Google ScholarPubMed
Gray, G. W. & Winsor, P. A. (1974). Liquid Crystals and Plastic Crystals. London: Wiley.Google Scholar
Henriksson, U., Oedberg, L. & Eriksson, J. C. (1975). Quadrupole splittings in deuterium nmr spectra of the hexagonal phase in the system sodium octanoate-d15-water-carbontetrachioride. Mol. Cryst. Liquid Cryst. 30, 73–8.CrossRefGoogle Scholar
Higgs, T. P. & Mackay, A. L. (1977). Determination of the complete order parameter tensor for a lipid methylene group from 1H and 2H nmr spin labels. Chem. Phys. Lipids (in the Press).Google Scholar
Hitchcock, P. B., Mason, R., Thomas, K. M. & Shipley, G. G. (1974). Structural chemistry of 1,2-dilauroyl-DL-phosphatidylethanolamine: Molecular conformation and intermolecular packing of phospholipids. Proc. natn. Acad. Sci., U.S.A. 71, 3036–40.CrossRefGoogle Scholar
Horwitz, A. F., Horsley, W. J. & Klein, M. P. (1972). Magnetic resonance studies on membrane and model membrane systems: Proton magnetic relaxation rates in sonicated lecithin dispersions. Proc. natn. Acad. Sci., U.S.A. 69, 590–3.CrossRefGoogle ScholarPubMed
Horwitz, A. F., Klein, M. P., Michaelson, D. M. & Kohler, S. J. (1973). Magnetic resonance studies of membrane and model membrane systems. V. Comparisons of aqueous dispersions of pure and mixed phospholipids. Ann. N. Y. Acad. Sci., U.S.A. 222, 468–87.CrossRefGoogle ScholarPubMed
Hoyland, J. R. (1968). Ab initio bond orbital calculations. I. Application to methane, ethane, propane and propylene. J. Am. them. Soc. 90, 2227–32.CrossRefGoogle Scholar
Hubbell, W. L. & McConnell, H. M. (1971). Molecular motion in spin-labeled phospholipids and membranes. J. Am. chem. Soc. 93, 314–26.Google ScholarPubMed
Huntress, W. T. (1970). The study of anisotropic rotation of molecules in liquids by quadrupolar relaxation. Adv. Magn. Reson. 4, 137.CrossRefGoogle Scholar
Jacobs, R. E., Hudson, B. & Andersen, H. C. (1975). A theory of the chain melting phase transition of aqueous phospholipid dispersions. Proc. natn. Acad. Sci., U.S.A. 72, 3993–7.CrossRefGoogle ScholarPubMed
Jacobsen, J. P., Bildsoe, H. K. & Schaumburg, K. (1976). Application of density matrix formalism in nmr spectroscopy. II. The one-spin-I case in anisotropic phase. J. Magn. Reson. 23, 153–64.Google Scholar
Jacobsen, J. P. & Schaumburo, K. (1976). Spin lattice relaxation time measurements of D2O in a lyotropic phase. J. Magn. Reson. 24, 173–80.Google Scholar
Janiak, M. J., Small, D. M. & Shipley, G. G. (1976). Nature of the thermal pre-transition of synthetic phospholipids: dimyristoyl and dipalmitoyl lecithin. Biochemistry, N.Y. 15, 4575–80.CrossRefGoogle Scholar
Jost, P., Libertini, L. J., Hebert, V. C. & Griffith, O. H. (1971). Lipid spin labels in lecithin multilayers. A study of motion along fatty acid chains. J. molec. Biol. 59, 7798.CrossRefGoogle ScholarPubMed
Kowalewski, J., Lindblom, T., Vestin, R. & Drakenberg, T. (1976). Deuteron magnetic resonance of monodeuteroethene: Isotropic and anisotropic phase spectra. Molec. Phys. 31, 1669–76.CrossRefGoogle Scholar
Lee, A. G. (1975). Functional properties of biological membranes: a physical chemical approach. Prog. Biophys. molec. Biol. 29, 356.CrossRefGoogle ScholarPubMed
Lesslauer, W., Cain, J. E. & Blasie, J. K. (1972). X-ray diffraction studies of lecithin bimolecular leaflets with incorporated fluorescent probes. Proc. natn. Acad., Sci. U.S.A. 69, 1499–503.CrossRefGoogle ScholarPubMed
Lippert, J. L. & Peticolas, W. L. (1971). Laser Raman investigation of the effect of cholesterol on conformational changes in dipalmitoyl lecithin multilayers. Proc. natn. Acad. Sci., U.S.A. 68, 1572–6.CrossRefGoogle ScholarPubMed
Long, R. C. & Goldstein, J. H. (1976). DMR investigation of alkyl chain order in an oriented quaternary potassium laurate mesophase. J. Magn. Reson. 23, 519–22.Google Scholar
Luzzati, V. (1968). X-ray diffraction studies of lipid-water systems. In Biological membranes (ed. Chapman, D.), pp. 71123. New York: Academic Press.Google Scholar
Mabrey, S. & Sturtevant, J. M. (1977). Incorporation of saturated fatty acids into phosphatidylcholine bilayers. Biochim. biophys. Acta 486, 444–50.CrossRefGoogle ScholarPubMed
Mantsch, H. H., Saitô, H. & Smith, I. C. P. (1977). Deuterium magnetic resonance. Applications in chemistry, physics and biology. In Progress in nmr Spectroscopy (ed. Emsley, et al. ). London: Pergamon Press. (In the Press.)Google Scholar
Marčelja, S. (1974). Chain ordering in liquid crystals. II. Structure of bilayer membranes. Biochim. biophys. Acta 367, 165–76.CrossRefGoogle ScholarPubMed
McCammon, J. A. & Deutch, J. M. (1975). Semiempirical models for biomembrane phase transitions and phase separations. J. Atn. chem. Soc. 97, 6675–81.CrossRefGoogle ScholarPubMed
McConnell, H. M. (1976). Molecular motion in biological membranes. In Spin Labeling. Theory and Application (ed. Berliner, L. J.), pp. 525–60. New York: Academic Press.CrossRefGoogle Scholar
McConnell, H. M. & McFarland, B. G. (1972). The flexibility gradient in biological membranes. Ann. N.Y. Acad. Sci., U.S.A. 195, 207–17.CrossRefGoogle ScholarPubMed
McFarland, B. G. & McConnell, H. M. (1971). Bent fatty acid chains in lecithin bilayers. Proc. natn. Acad. Sci., U.S.A. 68, 1274–8.CrossRefGoogle ScholarPubMed
McLaughlin, A. C., Cullis, P. R., Hemminga, M. A., Houldt, D. I., Radda, G. K., Ritchie, G. A., Seeley, P. J. & Richards, R. E. (1975). Application of 31P nmr to model and biological membrane systems. FEBS Lett. 57, 213–17.CrossRefGoogle ScholarPubMed
Mely, B. & Charvolin, J. (1977). DMR comparison of lyotropic mesophases with ordered and disordered paraffinic chains. Chem. Phys. Lipids 19, 4355.CrossRefGoogle Scholar
Mely, B., Charvolin, J. & Keller, P. (1975). Disorder of lipid chains as a function of their lateral packing in lyotropic liquid crystals. Chem. Phys. Lipids 15, 161–73.CrossRefGoogle Scholar
Mendelsohn, R. (1972). Laser Raman spectroscopic study of egg lecithin and egg lecithin-cholesterol mixtures. Biochim. biophys. Acta 290, 1521.CrossRefGoogle ScholarPubMed
Metcalfe, J. C., Birdsall, N. J. M., Feeney, J., Lee, A. G., Levine, Y. K. & Partington, P. (1971). 13C NMR spectra of lecithin vesicles and erythrocyte membranes. Nature, Lond. 233, 199201.CrossRefGoogle Scholar
Metcalfe, J. C., Birdsall, N. J. M. & Lee, A. G. (1973). NMR studies of lipids in bilayers and membranes. Ann. N.Y. Acad. Sci., U.S.A. 222, 460–7.CrossRefGoogle ScholarPubMed
Michaelson, D. M., Horwitz, A. F. & Klein, M. P. (1974). Head group modulation of membrane fluidity in sonicated phospholipid dispersions. Biochemistry, N.Y. 13, 2605–15.CrossRefGoogle ScholarPubMed
Nagle, J. F. (1973). Theory of biomembrane phase transitions. J. chem. Phys. 58, 252–64.CrossRefGoogle Scholar
Niederberger, W. & Seelig, J. (1974). Deuterium-magnetische Resonanzspektroskopie an spezifisch deuterierten flüssigen Kristallen. Ber. Bunsenges. physik. Chem. 78, 947–9.CrossRefGoogle Scholar
Niederberger, W. & Seelig, J. (1976). Phosphorus-31 chemical shift anisotropy in unsonicated phospholipid bilayers. J. Am. chem. Soc. 98, 3704–6.CrossRefGoogle Scholar
Oldfield, E., Chapman, D. & Derbyshire, W. (1971). Deuteron resonance: a novel approach to the study of hydrocarbon chain mobility in membrane systems. FEBS Lett. 16, 102–4.CrossRefGoogle Scholar
Oldfield, E., Chapman, D. & Derbyshire, W. (1972). Lipid mobility in Acholeplasma membranes using deuteron magnetic resonance. Chem. Phys. Lipids 9, 6981.CrossRefGoogle ScholarPubMed
Pechhold, W. (1968). Molekulbewegung in Polymeren. Kolloid- Z. u. Z. Polymere 228, 138.CrossRefGoogle Scholar
Pines, A., Ruben, D. J., Vega, S. & Mehring, M. (1976). New approach to high-resolution nmr in solids: deuterium spin-decoupling by multiple quantum transitions. Phys. Rev. Len. 36, 110–13.CrossRefGoogle Scholar
Rand, P. R., Chapman, D. & Larsson, K. (1975). Tilted hydrocarbon chains of dipalmitoyllecithin become perpendicular to the bilayer before melting. Biophys. J. 15, 1117–24.CrossRefGoogle Scholar
Reeves, L. W. & Tracey, A. S. (1975). Studies of membrane processes. VII. Hydrocarbon chain motions and the effect of changing counter-ions. J. Am. chem. Soc. 97, 5729–35.CrossRefGoogle Scholar
Reid, R. V. & Vaida, M. L. (1972). Quadrupole moment of the deuteron. Phys. Rev. Lett. 29, 494–6.CrossRefGoogle Scholar
Rose, M. E. (1957). Elementary Theory ofAngular Momentum. New York: Wiley.Google Scholar
Rosevear, F. B. (1968). Liquid crystals: The mesomorphic phases of surfactant compositions. J. Soc. Cosmetic Chem. 1, 581–94.Google Scholar
Rowell, J. C., Phillips, W. D., Melby, L. R. & Pan, M. (1965). NMR studies of some liquid crystal systems. J. chem. Phys. 43, 3442–54.CrossRefGoogle Scholar
Saitô, H., Schreier-Muccillo, S. & Smith, I. C. P. (1973). High resolution deuterium magnetic resonance – an approach to the study of molecular organization in biological membranes and model systems. FEBS Lett. 33, 281–5.CrossRefGoogle Scholar
Saupe, A. (1964). Kernresonanzen in kristallinen Flüssigkeiten und kristallinflüssigen Lösungen. Z. Naturf. 19, 161–71.CrossRefGoogle Scholar
Schindler, H. & Serlig, J. (1973). EPR spectra of spin labels in lipid bilayers. J. chem. Phys. 59, 1841–50.CrossRefGoogle Scholar
Schindler, H. & Seelig, J. (1974). EPR spectra of spin labels in lipid bilayers. II. Rotation of steroid spin probes. J. chetn. Phys. 61, 2946–9.CrossRefGoogle Scholar
Schindler, H. & Seelig, J. (1975). Deuterium order parameters in relation to thermodynamic properties of a phospholipid bilayer. A statistical mechanical interpretation. Biochemistry, N.Y. 1, 2283–7.CrossRefGoogle Scholar
Scott, H. L. (1974). A model for phase transitions in lipid bilayers and biological membranes. J. theor. Biol. 46, 241–53.CrossRefGoogle Scholar
Seelig, J. (1970). Spin label studies of oriented liquid crystals (A model system for bilayer membranes). J. Am. chem. Soc. 92, 3881–7.CrossRefGoogle Scholar
Seelig, J. (1976). Anisotropic motion in liquid crystalline structures. In Spin Labeling: Theory and Application (ed. Berliner, L. J.), pp. 373409. New York: Academic Press.CrossRefGoogle Scholar
Seelig, J. & Gally, H. (1976). Investigation of phosphatidylethanolamine bilayers by deuterium and phosphorus-31 nuclear magnetic resonance. Biochemistry, N. Y. 15, 5199–204.CrossRefGoogle ScholarPubMed
Seelig, J., Gally, H. & Wohlgemuth, R. (1977). Orientation and flexibility of the choline head group in lecithin bilayers. Biochim. biophys. Acta 467, 109119.CrossRefGoogle Scholar
Seelig, J., Limacher, H. & Bader, P. (1972). Molecular architecture of liquid crystalline bilayers. J. Am. chem. Soc. 94, 6364–71.CrossRefGoogle Scholar
Seelig, J. & Niederberger, W. (1974 a). Deuterium labeled lipids as structural probes in liquid crystalline bilayers. J. Am. chem. Soc. 96, 2069–72.CrossRefGoogle Scholar
Seelig, J. & Niederberger, W. (1974 b). Two pictures of a lipid bilayer. A comparison between deuterium label and spin label experiments. Biochemistry, N.Y. 13, 1585–8.CrossRefGoogle ScholarPubMed
Seelig, I. & Seelig, A. (1974 a). Deuterium magnetic resonance studies of phospholipid bilayers. Biochem. biophys. Res. Commun. 57, 406–11.CrossRefGoogle ScholarPubMed
Seelig, A. & Seelig, J. (1974 b). The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry, N.Y. 13, 4839–45.CrossRefGoogle Scholar
Seelig, A. & Seelig, J. (1975). Bilayers of dipalmitoyl-3-sn-phosphatidyl- choline. Conformational differences between the fatty acyl chains. Biochim. biophys. Acta 406, 15.CrossRefGoogle Scholar
Seelig, A. & Seelig, J. (1977). Effect of a single cis-double bond on the structure of a phospholipid bilayer. Biochemistry, N.Y. 16, 4550.CrossRefGoogle ScholarPubMed
Slichter, C. P. (1963). Principles of Magnetic Resonance, pp. 160–76. New York: Harper and Row.Google Scholar
Soda, G. & Chiba, T. (1969). Deuteron magnetic resonance study of cupric sulfate pentahydrate. J. chem. Phys. 50, 439–55.CrossRefGoogle Scholar
Stockton, G. W. & Smith, I. C. P. (1976). A deuterium magnetic resonance study of the condensing effect of cholesterol on egg phosphatidyicholine bilayer membranes. I. Perdeuterated fatty acid probes. Chem. Phys. Lipids 17, 251–63.CrossRefGoogle Scholar
Stockton, G. W., Polnaszek, C. F., Leitch, L. C., Tulloch, A. P. & Smith, I. C. P. (1974). A study of mobility and order in model membranes using 2H nmr relaxation rates and quadrupole splittings of specifically deuterated lipids. Biochem. biophys. Res. Commun. 60, 844–50.CrossRefGoogle ScholarPubMed
Stockton, G. W., Polnaszek, C. F., Tulloch, A. P., Hasan, F. & Smith, I. C. P. (1976). Molecular motion and order in single-bilayer vesicles and multilamellar dispersions of egg lecithin and lecithin cholesterol mixtures. A deuterium nuclear magnetic resonance study of specifically- labelled lipids. Biochemistry, N.Y. 15, 954–66.CrossRefGoogle Scholar
Stockton, G. W., Johnson, K. G., Butler, K. W., Polnaszek, C. F., Cyr, R. & Smith, I. C. P. (1975). Molecular order in Acholeplasma laidlawii membranes as determined by deuterium magnetic resonance of biosynthetically incorporated specifically-labelled lipids. Biochim. biophys. Acta 401, 535–9.CrossRefGoogle ScholarPubMed
Sundaralingam, M. (1972). Molecular structures and conformations of the phospholipids and sphingomyelins. Ann. N.Y. Acad. Sci., U.S.A. 195, 324–55.CrossRefGoogle ScholarPubMed
Tardieu, A., Luzzati, V. & Reman, F. C. (1973). Structure and polymorphism of the hydrocarbon chains of lipids: A study of lecithin—water phases. J. molec. Biol. 75, 711–33.CrossRefGoogle ScholarPubMed
Townes, C. H. & Schawlow, A. L. (1955). Microwave Spectroscopy, pp. 130–40. New York: McGraw-Hill.Google Scholar
Träuble, H. & Sackmann, E. (1972). Studies of the crystalline-liquid crystalline phase transition of lipid model membranes. III. Structure of a steroid-lecithin system below and above the lipid phase transition. J. Am. chem. Soc. 94, 4499–510.CrossRefGoogle Scholar
Tracey, A. S. & Diehl, P. (1976). A deuterium magnetic resonance study of a lamellar lyotropic liquid crystalline phase. Can. J. Chem. 54, 2283–7.CrossRefGoogle Scholar
Vaughan, D. J. & Keough, K. M. (1974). Changes in phase transition of phosphatidylethanolamine - and phosphatidylcholine - water dispersions induced by small modifications in the head group and backbone region. FEBS Lett. 47, 158–61.CrossRefGoogle Scholar
Vega, S. & Pines, A. (1977). Operator formalism for double quantum nmr. J. them. Phys. (in the Press).CrossRefGoogle Scholar
Wennerström, H., Persson, N. O. & Lindman, B. (1974). Double quantum transitions in deuteron nmr spectra of lyotropic liquid crystals. J. Magn. Reson. 13, 348–53.Google Scholar
Wennerström, H. & Lindblom, G. (1977). Biological and model membranes studied by nuclear magnetic resonance of spin one half nuclei. Q. Rev. Biophys. 10, 6796.CrossRefGoogle ScholarPubMed
Worcester, D. L. & Franks, N. P. (1976). Neutron diffraction analysis of hydrated egg lecithin and cholesterol bilayers. J. molec. Biol. 100, 359–78.CrossRefGoogle Scholar