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Lipid conformation in model membranes and biological membranes

Published online by Cambridge University Press:  17 March 2009

Joachim Seelig  and
Anna Seelig
Joachim Seelig
Affiliation:
Department of Biophysical Chemistry, Biocenter of the University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland
Anna Seelig
Affiliation:
Department of Biophysical Chemistry, Biocenter of the University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland
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Extract

Protein molecules in solution or in protein crystals are characterized by rather well-defined structures in which α-helical regions, β-pleated sheets, etc., are the key features. Likewise, the double helix of nucleic acids has almost become the trademark of molecular biology as such. By contrast, the structural analysis of lipids has progressed at a relatively slow pace. The early X-ray diffraction studies by V. Luzzati and others firmly established the fact that the lipids in biological membranes are predominantly organized in bilayer structures (Luzzati, 1968). V. Luzzati was also the first to emphasize the liquid-like conformation of the hydrocarbon chains, similar to that of a liquid paraffin, yet with the average orientation of the chains perpendicular to the lipid–water interface. This liquid–crystalline bilayer is generally observed in lipid–water systems at sufficiently high temperature and water content, as well as in intact biological membranes under physiological conditions (Luzzati & Husson, 1962; Luzzati, 1968; Tardieu, Luzzati & Reman, 1973; Engelman, 1971; Shipley, 1973). In combination with thermodynamic and other spectroscopic observations these investigations culminated in the formulation of the fluid mosaic model of biological membranes (cf. Singer, 1971). However, within the limits of this model the exact nature of lipid conformation and dynamics was immaterial, the lipids were simply pictured as circles with two squiggly lines representing the polar head group and the fatty acyl chains, respectively. No attempt was made to incorporate the well-established chemical structure into this picture. Similarly, membrane proteins were visualized as smooth rotational ellipsoids disregarding the possibility that protruding amino acid side-chains and irregularities of the backbone folding may create a rather rugged protein surface.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 13 , Issue 1 , February 1980 , pp. 19 - 61
Copyright
Copyright © Cambridge University Press 1980

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References

Achlama, A. & Zur, Y. (1979). The electric field gradient tensor of the olefinic deuterons of potassium hydrogen maleate. J. Magn. Reson. 36, 249–258.Google Scholar
Bloom, M. (1979). Squishy proteins in fluid membranes. Can. J. Phys. 57, 2227–2230.CrossRefGoogle Scholar
Brown, M. F. & Seelig, J. (1977). Ion induced changes in the head-group conformation of lecithin bilayers. Nature, Lond. 269, 721–723.CrossRefGoogle Scholar
Brown, M. F., & Seelig, J. (1978). Influence of cholesterol on the polar region of phosphatidylcholine and phosphatidylethanolamine bilayers. Biochemistry, N.Y. 17, 381–384.CrossRefGoogle ScholarPubMed
Brown, M. F., Seelig, J. & Häberlen, U. (1979). Structural dynamics in phospholipid bilayers from deuterium spin lattice relaxation time measurements. J. Chem. Phys. 70, 5045–5053.CrossRefGoogle Scholar
Browning, J. L. & Seelig, J. (1980). Bilayers of phosphatidylserine: a deuterium and phosphorus NMR study. Biochemistry, N.Y. 19, 1262–1270.CrossRefGoogle Scholar
Büldt, G. & Seelig, J. (1980). The conformation of phosphatidylethanolamine in the gel phase as seen by neutron diffraction. Biochemistry, N, Y. in press.CrossRefGoogle Scholar
Büldt, G., Gally, H. U., Seelig, A., Seelig, J. & Zaccai, G. (1978). Neutron diffraction studies on selectively deuterated phospholipid bilayers. Nature, Lond. 271, 182–184.CrossRefGoogle ScholarPubMed
Büldt, G., Gally, H. U., Seelig, J. & Zaccai, G. (1979). Neutron diffraction studies on phosphatidylcholine model membranes. I. Head-group conformation. J. molec. Biol. 134, 673–691.CrossRefGoogle ScholarPubMed
Burnett, L. J. & Muller, B. H. (1971). Deuteron quadrupole coupling constants in three solid deuterated paraffin hydrocarbons: C2D6, C4D10, C6D14. J. Chem. Phys. 55, 5829–5831.CrossRefGoogle Scholar
Cain, J., Santillan, G. & Blasie, J. K. (1972). Molecular motion in membranes as indicated by X-ray diffraction. In Membrane Research (ed. Fox, F.), pp. 3–14. New York, N.Y.: Academic Press.Google Scholar
Chapman, D. (1975). Phase transitions and fluidity characteristics of lipids and cell membranes. Q. Rev. Biophys. 8, 185–235.CrossRefGoogle ScholarPubMed
Chapman, D., Cornell, B. A., Eliasz, A. W. & Perry, A. (1977). Interactions of helical polypeptide segments which span the hydrocarbon region of lipid bilayers. J. molec. Biol. 113, 517–538.CrossRefGoogle ScholarPubMed
Chapman, D., Gomez-Fernandez, J. C. & Goni, F. M. (1979). Intrinsic protein–lipid interactions. FEBS Lett. 98, 211–223.CrossRefGoogle ScholarPubMed
Cherry, R. J. (1979). Rotational and lateral diffusion of membrane proteins. Biochim. biophys. Acta 559, 289–327.CrossRefGoogle ScholarPubMed
Cherry, R. J., Mueller, U. & Schneider, G. (1977). Rotational diffusion of bacteriorhodopsin in lipid membranes. FEBS Lett. 80, 465–468.CrossRefGoogle ScholarPubMed
Cullis, P. R. & De Kruijff, B. (1976). 31P nmr studies of unsonicated aqueous dispersions of neutral and acidic phospholipids. Effects of phase transitions, pH and divalent cations on the motion of the phosphate region of the polar head group. Biochim. biophys. Ada 436, 523–540.CrossRefGoogle Scholar
Cullis, P. R. & De Kruijff, B. (1978). The polymorphic phase behaviour of phosphatidylethanolamines of natural and synthetic origin. Biochim. biophys. Acta 513, 31–42.CrossRefGoogle ScholarPubMed
Cullis, P. R. & De Kruijff, B. (1979). Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. biophys. Acta 559, 399–420.CrossRefGoogle ScholarPubMed
Curatolo, W., Sakura, J. D., Small, D. M. & Shipley, G. G. (1977). Protein–lipid interactions: recombinants of the proteolipid apoprotein of myelin with dimyristoyl lecithin. Biochemistry, N.Y. 16, 2313–2319.CrossRefGoogle Scholar
Davis, J. H. (1979). Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys. J. 27, 339–358.CrossRefGoogle ScholarPubMed
Davis, J. H., Jeffrey, K. R. & Bloom, M. (1978). Spin-lattice relaxation as a function of chain position in perdeuterated potassium palmitate. J. Magn. Res. 29, 191–199.Google Scholar
Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I. & Higgs, T. P. (1976). Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42, 390–394.CrossRefGoogle Scholar
Davis, J. H., Nichol, C. P., Weeks, G. & Bloom, M. (1979). Study of the cytoplasmic and outer membranes of Escherichia coli by deuterium magnetic resonance. Biochemistry, N.Y. 18, 2103–2112.CrossRefGoogle ScholarPubMed
Davoust, J., Bienvenue, A., Fellmann, P. & Deveaux, P. F. (1980). Boundary lipids and protein mobility in rhodopsin-phosphatidylcholine vesicles. Effect of lipid phase transition. Biochim. biophys. Acta 596, 28–42.CrossRefGoogle Scholar
Dix, J. A., Kivelson, D. & Diamond, J. M. (1978). Molecular motion of small nonelectrolyte molecules in lecithin bilayers. J. Membrane Biol. 40, 315–342.CrossRefGoogle ScholarPubMed
Engelman, D. M. (1971). Lipid bilayer structure in the membrane of Mycoplasma laidlawii. J. molec. Biol. 58, 153–165.CrossRefGoogle ScholarPubMed
Flory, P. J. (1969). Statistical Mechanics of Chain Molecules. New York, N.Y.: Interscience.CrossRefGoogle Scholar
Furthmayr, H. (1977). Structural analysis of a membrane glycoprotein: Glycophorin A. J. Supramol. Struct. 7, 121–134.CrossRefGoogle ScholarPubMed
Gaber, B. P. & Peticolas, W. L. (1977). On the quantitative interpretation of biomembrane structure by Raman spectroscopy. Biochim. biophys. Acta 465, 260–274.CrossRefGoogle ScholarPubMed
Gally, H. U., Niederberger, W. & Seelig, J. (1975). Conformation and motion of the choline head group in bilayers of dipalmitoyl-3-sn-phosphatidyicholine. Biochemistry, N.Y. 14, 3647–3652.CrossRefGoogle Scholar
Gally, H. U., 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, 1447–1450.Google ScholarPubMed
Gally, H. U., Pluschke, G., Overath, P. & Seelig, J. (1979). Structure of Escherichia coli membranes. Phospholipid conformation in model membranes and cells as studied by deuterium magnetic resonance. Biochemistry, N.Y. 18, 5605–5610.CrossRefGoogle ScholarPubMed
Gally, H. U., Pluschke, G., Overath, P. & Seelig, J. (1980). Structure of Escherichia coli membranes. Fatty acyl chain order parameters of inner and outer membrane and derived liposomes. Biochemistry, N.Y. 19, 1638–1643.CrossRefGoogle ScholarPubMed
Gomez-Fernandez, J. C., Goni, F. M., Bach, D., Restall, C. & Chapman, D. (1979). Protein-lipid interactions. A study of (Ca2+, Mg2+) ATPase reconstituted with synthetic phospholipids. FEBS Lett. 98, 224–228.CrossRefGoogle ScholarPubMed
Griffin, R. G. (1976). Observation of the effect of water on the 31P nuclear magnetic resonance spectra of dipalmitoyllecithin. J. Am. Chem. Soc. 98, 851–853.CrossRefGoogle ScholarPubMed
Gruen, D. W. R. (1980). A statistical-mechanical model of the lipid bilayer above its phase transition. Biochim. biophys. Acta 595, 161–183.CrossRefGoogle ScholarPubMed
Haberkorn, R. A., Griffin, R. G., Meadows, M. D., & Oldfield, E. (1977). Deuterium nuclear magnetic resonance investigation of the dipalmitoyl lecithin-cholesterol water system. J. Am. Chem. Soc. 99, 7353–7355.CrossRefGoogle ScholarPubMed
Hare, F. & Lussan, C. (1977). Variations in microviscosity values induced by different rotational behaviour of fluorescent probes in some aliphatic environments. Biochim. biophys. Acta 467, 262–272.CrossRefGoogle ScholarPubMed
Hauser, H. & Phillips, M. C. (1979). Interactions of the polar groups of phospholipid bilayer membranes. Progr. Surf. & Membrane Sci. 13, 297–413.CrossRefGoogle Scholar
Hauser, H., Guyer, W., Pascher, I., Skrabal, P. & Sundell, S. (1980). Polar group conformation of phosphatidyicholine. Effect of solvent and aggregation. Biochemistry, N.Y. 19, 366–373.CrossRefGoogle Scholar
Herzfeld, J., Griffin, R. G. & Haberkorn, R. A. (1978). Phosphorus-31 chemical shift tensors in barium diethyl phosphate and urea-phosphoric acid: model compounds for phospholipid head-group studies. Biochemistry, N.Y. 17, 2711–2718.CrossRefGoogle ScholarPubMed
Hesketh, T. R., Smith, G. A., Houslay, M. D., McGill, K. A., Birdsall, N. J. M., Metcalfe, J. & Warren, G. B. (1976). Annular lipids determine the ATPase activity of a Calcium transport protein complexed with dipalmitoyllecithin. Biochemistry, N.Y. 15, 4145–4151.CrossRefGoogle ScholarPubMed
Heyn, M. P. (1979). Determination of lipid order parameters and rotational correlation times from fluorescence depolarization experiments. FEBS Lett. 108, 359–364.CrossRefGoogle ScholarPubMed
Hitchcock, P. B., Mason, R., Thomas, K. M. & Shipley, G. G. (1974). Structural chemistry of 1,2-dilauroyl-DL-phosphatidyl-ethanolamine: Molecular conformation and intermolecular packing of phospholipids. Proc. natn. Acad. Sci. U.S.A. 71, 3036–3040.CrossRefGoogle ScholarPubMed
Jacobs, R. & Oldfield, E. (1979). Deuterium nuclear magnetic resonance investigation of dimyristoyllecithin-dipalmitoyllecithin and dimyristoyllecithin-cholesterol mixtures. Biochemistry, N.Y. 18, 3280–3285.CrossRefGoogle ScholarPubMed
Jähnig, F. (1979). Structural order of lipids and proteins in membranes. Evaluation of fluorescence anisotropy data. Proc. natn. Acad. Sci. U.S.A. 76, 6361–6365.CrossRefGoogle ScholarPubMed
Jost, P. C. & Griffith, O. H. (1980). The lipid-protein interface in biological membranes. Ann. NY. Acad. Sci. (in the Press).CrossRefGoogle Scholar
Jost, P. C., Griffith, O. H., Capaldi, R. A. & Vanderkooi, G. (1973). Evidence for boundary lipids in membranes. Proc. natn. Acad. Sci. U.S.A. 70, 480–484.CrossRefGoogle ScholarPubMed
Kang, S. Y., Gutowsky, H. S. & Oldfield, E. (1979). Spectroscopic studies of specifically deuterium labelled membrane systems. Nuclear magnetic resonance investigation of protein–lipid interactions in Escherichia coli membranes. Biochemistry, N.Y. 18, 3268–3272.CrossRefGoogle ScholarPubMed
Kang, S. Y., Gutowsky, H. S., Hshung, J. C., Jacobs, R., King, T. E., Rice, D. & Oldfield, E. (1979). Nuclear magnetic resonance investigation of the cytochrome oxidase–phospholipid interaction. A new model for boundary lipid. Biochemistry N.Y. 18, 3257–3267.CrossRefGoogle ScholarPubMed
Kohler, S. J. & Klein, M. P. (1976). 31P chemical shielding tensors of phosphorylethanolamine, lecithin and related compounds: Application to head-group motion in membranes. Biochemistry, N.Y. 15, 967–973.CrossRefGoogle ScholarPubMed
Kowalewski, J., Lindblom, T., Vestin, R. & Drakenberg, T. (1976). Deuteron magnetic resonance of monodeuteroethene: Isotropic and anisotropic phase spectra. Molec. Phys. 31, 1669–1676.CrossRefGoogle Scholar
Lee, A. G., Birdsall, N. J. M., Metcalf, J. C., Warren, G. B. & Roberts, G. C. K. (1976). A determination of the mobility gradient in lipid bilayers by 13C nuclear magnetic resonance. Proc. R. Soc. B. 193, 253–274.Google Scholar
Luzzati, V. (1968). X-ray diffraction studies of lipid–water systems. In Biological Membranes (ed. Chapman, D.), pp. 71–123. New York, N.Y.: Academic Press.Google Scholar
Luzzati, V. & Husson, F. (1962). The structure of the liquid–crystalline phases of lipid–water systems. J. Cell. Biol. 12, 207–219.CrossRefGoogle ScholarPubMed
Mabrey, S., Mateo, P. L., & Sturtevant, J. M. (1978). High-sensitivity scanning calorimetric study of mixtures of cholesterol with dimyristoyl-and dipalmitoyl phosphatidylcholines. Biochemistry, N.Y. 17, 2464–2468.CrossRefGoogle Scholar
Mantsch, H. H., Saito, H. & Smith, I. C. P. (1977). Deuterium magnetic resonance. Applications in Chemistry, physics and biology. Progr. NMR Spectroscopy 11, 211–272.CrossRefGoogle Scholar
Marčelja, S. (1974). Chain ordering in liquid crystals. II. Structure of bilayer membranes. Biochim. biophys. Acta 367, 165–176.CrossRefGoogle ScholarPubMed
Meirovitch, E. & Freed, J. H. (1979). Slow motional lineshapes for very anistropic diffusion: I = I nuclei. Chem. Phys. Lett. 64, 311–316.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, 15 161–173.CrossRefGoogle Scholar
Mombers, C., Vericleij, A. J., De Gier, J. & Van Deenen, L. L. M. (1979). The interaction of spectrin-actin and synthetic phospholipids. II. The interaction with phosphatidylserine. Biochim. biophys. Acta 551, 271–281.CrossRefGoogle ScholarPubMed
Nichol, C. P., Davis, J. H., Weeks, G. & Bloom, M. (1980). Quantitative study of the fluidity of Escherichia coli membranes using deuterium magnetic resonance. Biochemistry, N.Y. 19, 451–457.CrossRefGoogle ScholarPubMed
Niederberger, W., & Seelig, J. (1976). Phosphorus-31 chemicals shift anisotropy in unsonicated phospholipid bilayers. J. Am. Chem. Soc. 98, 3704–3706.CrossRefGoogle Scholar
Oldfield, E., Meadows, M., Rice, D. & Jacobs, R. (1978 a). Spectroscopic studies of specifically deuterium labelled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems. Biochemistry, N.Y. 17, 2727–2740.CrossRefGoogle ScholarPubMed
Oldfield, E., Gilmore, R., Glaser, M., Gutowsky, H. S., Hshung, J. C., Kang, S. Y., Tsoo, E. King, Meadows, M. & Rice, D. (1978 b). Deuterium nuclear magnetic resonance investigation of the effects of proteins and polypeptides on hydrocarbon chain order in model membrane systems. Proc. natn. Acad. Sci. U.S.A. 75, 4657–4660.CrossRefGoogle ScholarPubMed
Oldfield, E., Meadows, M. & Glaser, M. (1976). Deuterium magnetic resonance spectroscopy of isotopically labelled mammalian cells. J. biol. Chem. 251, 6147–6149.CrossRefGoogle ScholarPubMed
Pearson, R. H. & Pascher, I. (1979). The molecular structure of lecithin dihydrate. Nature, Lond. 281, 499–501.CrossRefGoogle ScholarPubMed
Phillips, M. C., Williams, R. M. & Chapman, D. (1969). On the nature of hydrocarbon chain motions in lipid liquid crystals. Chem. Phys. Lipids 3, 234–244.CrossRefGoogle Scholar
Pink, D. A. & Zuckermann, M. J. (1980). Lipid chain order in Acholeplasma laidlawii membranes. What does 2H nmr tell us? FEBS Lett. 109, 5–8.CrossRefGoogle ScholarPubMed
Rance, N., Jeffrey, K. R., Tulloch, A. P., Bulter, K. W. & Smith, I. C. P. (1980). Orientational order of unsaturated phospholipidsin the membranes of Acholeplasma laidlawii as observed by deuterium nmr. Biochim. biophys.Acta (in the Press).Google Scholar
Rand, R. P., Tinker, D. O. & Fast, P. G. (1971). Polymorphism of phosphatidylethanolamines from two natural sources. Chem. Phys. Lipids 6, 333–342.CrossRefGoogle ScholarPubMed
Rice, D. M., Meadows, M. D., Scheinman, A. O., Goni, F. M., Gomez-Fernandez, J. C., Moscarello, M. A., Chapman, D. & Oldfield, E. (1979). Protein–lipid interactions. A nuclear magnetic resonance study of sarcoplasmic reticulum Ca2+, Mg2+-ATPase, lipophilin, and proteolipid apoprotein–lecithin systems and a comparison with the effects of cholesterol. Biochemistry, N.Y. 18, 5893–5903.CrossRefGoogle Scholar
Sanderman, H. (1978). Regulation of membrane enzymes by lipids. Biochim. biophys. Acta 515, 209–237.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. 14, 2283–2287.CrossRefGoogle Scholar
Seelig, A. & Seelig, J. (1974). The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry, N.Y. 13, 4839–4845.CrossRefGoogle Scholar
Seelig, A. & Seelig, J. (1975). Bilayers of dipalmitoyl-3-sn-phosphatidylcholine. Conformational differences between the fatty acyl chains. Biochim. biophys. Acta 406, 1–5.CrossRefGoogle ScholarPubMed
Seelig, A. & Seelig, J. (1977). Effect of a single cis-double bond on the structure of a phospholipid bilayer. Biochemistry, N.Y. 16, 45–50.CrossRefGoogle ScholarPubMed
Seelig, A. & Seelig, J. (1978). Lipid–protein interaction in reconstituted cytochrome c oxidase phospholipid membranes. Hoppe-Seyler's Z. Physiol. Chem. 359, 1747–1756.CrossRefGoogle ScholarPubMed
Seelig, J. (1977). Deuterium magnetic resonance: theory and application to lipid membranes. Q. Rev. Biophys. 10, 353–418.CrossRefGoogle ScholarPubMed
Seelig, J. (1978). Phosphorus-31 nuclear magnetic resonance and the head-group structure of phospholipids in membranes. Biochim. biophys. Acta 505, 105–141.CrossRefGoogle Scholar
Seelig, J. & Browning, J. L. (1978). General features of phospholipid conformation in membranes. FEBS Lett. 92, 41–44.CrossRefGoogle Scholar
Seelig, J., Dijkman, R. & De Haas, G. H. (1980). Thermodynamic and conformational studies on 2-sn-phosphatidylcholines in monolayers and bilayers. Biochemistry, N.Y. 19, 2215–2219.CrossRefGoogle Scholar
Seelig, J. & Gally, H. U. (1976). Investigation of phosphatidylethanolamine bilayers by deuterium and phosphorus-31 nuclear magnetic resonance. Biochemistry, N.Y. 15, 5199–5204.CrossRefGoogle ScholarPubMed
Seelig, J., Gally, H. U. & Wohlgemuth, R. (1977). Orientation and flexibility of the choline head group in lecithin bilayers. Biochim. biophys. Acta 467, 109–119.CrossRefGoogle Scholar
Seelig, J. & Limacher, H. (1974). Lipid molecules in lyotropic liquid crystals with cylindrical structure. (A spin label study.) Mol. Cryst. Liquid Cryst. 25, 105–112.CrossRefGoogle Scholar
Seelig, J. & Niederberger, W. (1974). Two pictures of a lipid bilayer. A comparison between deuterium label and spin experiments. Biochemistry, N.Y., 13, 1585–1588.CrossRefGoogle ScholarPubMed
Seelig, J., Tamm, L., Fleischer, S. & Hymel, L. (1980). Deuterium and phosphorus nmr and fluorescence depolarization studies of functional reconstituted sarcoplasmic reticulum membrane vesicles. (Manuscript in preparation.)Google Scholar
Seelig, J. & Waesepe-Šarčevic, N. (1978). Molecular order in cis and trans unsaturated phospholipid bilayers. Biochemistry, N.Y. 17, 3310–3315.CrossRefGoogle ScholarPubMed
Shepherd, J. C. W. & Büldt, G. (1978). Zwitterionic dipoles as a dielectric probe for investigating head-group mobility in phospholipid membranes. Biochim. biophys. Acta 514, 83–94.CrossRefGoogle ScholarPubMed
Shipley, G. (1973). Recent X-ray diffraction studies of biological membranes and membrane components. In Biological Membranes, Vol. 2, (ed. Chapman, D. and Wallach, D. F. H.), pp. 1–89. New York, N.Y.: Academic Press.Google Scholar
Singer, S. J. (1971). The molecular organization of biological membranes. In Structure and Function of Biological Membranes (ed. Rothfield, I.), pp. 146–222. New York, N.Y.: Academic Press.Google Scholar
Skarjune, R. & Oldfield, E. (1979 a). Physical studies of cell surface and cell membrane structure. Deuterium nuclear magnetic resonance investigation of deuterium-labelled N-hexadecanoyl-galactosylceramides (cerebrosides). Biochim. biophys. Acta 556, 208–218.CrossRefGoogle ScholarPubMed
Skarjune, R. & Oldfield, E. (1979 b). Physical studies of cell surface and cell membrane structure. Determination of phospholipid head-group organization by deuterium and phosphorus nuclear magnetic resonance spectroscopy. Biochemistry, N.Y. 18, 5903–5909.CrossRefGoogle ScholarPubMed
Smith, I. C. P., Butler, K. W., Tulloch, A. P., Davis, J. H. & Bloom, M. (1979). The properties of gel state lipid membranes of Acholeplasma laidlawii as observed by deuterium nuclear magnetic resonance. FEBS Lett. 100, 57–61.CrossRefGoogle Scholar
Stockton, G. W. & Smith, I. C. P. (1976). A deuterium magnetic resonance study of the condensing effect of cholesterol on egg phosphatidylcholine bilayer membranes. I. Perdeuterated fatty acid probes. Chem. Phys. Lipids 17, 251–263.CrossRefGoogle ScholarPubMed
Stockton, G. W., Johnson, K. G., Butler, K., Tulloch, A. P., Boulanger, Y., Smith, I. C. P., Davis, J. H. & Bloom, M. (1977). Deuterium NMR study of lipid organisation in Acholeplasma laidlawii membranes. Nature 269, 268–268.CrossRefGoogle Scholar
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, 954–966.CrossRefGoogle Scholar
Stoffel, W., Zierenberg, O. & Scheefers, H. (1977). Reconstitutiou of Ca2+-ATPase of sarcoplasmic reticulum with 13C-labelled lipids. Hoppe-Seyler's Z. physiol. Chem. 358, 865–882.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, 711–733.CrossRefGoogle ScholarPubMed
Träuble, H. (1971). The movement of molecules across lipid membranes. A molecular theory. J. Membrane Biol. 4, 193–208.CrossRefGoogle ScholarPubMed
Van Deenen, L. L. M. (1965). Phospholipids and biomembranes. Prog. Chem. Fats 8, 1–127.Google Scholar
Van Zoelen, E. J. J., Van Dijck, P. W. M., De Kruijff, B., Verkleij, A. J. & Van Deenen, L. L. M. (1978). Effect of glycophorin incorporation on the physico-chemical properties of phospholipid bilayers. Biochim. biophys. Acta 514, 9–24.CrossRefGoogle ScholarPubMed
Wohlgemuth, R., Waespe-Šarčevic, N. & Seelig, J. (1980). Bilayers of phosphatidylglycerol. A deuterium and phosphorus nmr study of the head-group region. Biochemistry, N.Y. in press.Google Scholar
Worcester, D. L. (1976). Neutron beam studies of biological membranes and membrane components. In Biological Membranes, vol. 3. (ed. Chapman, D. and Wallach, D. F. H.), pp. 1–44. London: Academic Press.Google Scholar
Worcester, D. L. & Franks, N. P. (1976). Neutron diffraction analysis of hydrated egg lecithin and cholesterol bilayers. J. molec. Biol. 100, 359–378.CrossRefGoogle Scholar
Zaccai, G., Büldt, G., Seelig, A. & Seelig, J. (1979). Neutron diffraction studies on phosphatidylcholine model membranes. II. Chain conformation and segmental disorder. J. molec. Biol. 134, 693–706.CrossRefGoogle ScholarPubMed