Lipid Bilayer Stability in Biological Membranes

  • Leif Rilfors
  • Göran Lindblom
  • Åke Wieslander
  • Anders Christiansson
Part of the Biomembranes book series (B, volume 12)


One of the most important problems in biophysics today is the self-assembly of membrane components, in particular lipids and proteins. It has long been known that many membrane lipids spontaneously form a bilayer when mixed with water (Luzzati, 1968). Recently, it was also indicated that even a membrane protein may form a bilayer structure (Carlsson, 1981). The Singer and Nicolson (1972) model of a biomembrane is based on the assumption that the lipids form a bilayer matrix in which the proteins are incorporated and are able to diffuse more or less freely in two dimensions. If the function of the lipids is only to form this fluid matrix, why does a biological membrane often contain more than 100 different lipid species? Furthermore, many lipids do not spontaneously form bilayers with water. Sometimes not even the major lipid in a membrane forms a bilayer, e.g., monogalactosyldiglyceride of chloroplasts (Shipley et al., 1973; Brentel et al., 1984c). However, the membrane lipids together with the proteins form a stable, functioning membrane, with the properties necessary for a living cell, i.e., to be both a barrier and a communicator to the surroundings. It can thus be expected that the membrane lipids are not working just as a fluid matrix, as is suggested by the Singer and Nicolson model. Most probably they play an important structural role in biological membranes as will be discussed in this chapter.


Acyl Chain Hydrocarbon Chain Micellar Solution Lipid Species Polar Head Group 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abidor, I. G., Arakelyan, V. B., Chernomordik, L. V., Chizmadzhev, Y. A., Pastushenko, V. F., and Tarasevich, M. R., 1979, Electric breakdown of bilayer lipid membranes, Bioe-lectrochem. Bioenerg. 6:37.Google Scholar
  2. Abrahamsson, S., Pascher, I., Larsson, K., and Karlsson, K.-E., 1972, Molecular arrangements in glycosphingolipids, Chem. Phys. Lipids 8:152.Google Scholar
  3. Aibara, S., Kato, M., Ishinaga, M., and Kito, M., 1972, Changes in positional distribution of fatty acids in the phospholipids of Escherichia coli after shift-down in temperature, Biochim. Biophys. Acta 270:301.PubMedGoogle Scholar
  4. Ansell, G., Hawthorne, J. N., and Dawson, R. M. C, 1973, Form and Function of Phospholipids, Elsevier, Amsterdam.Google Scholar
  5. Arvidson, G., Brentel, I., Khan, A., Lindblom, G., and Fontell, K., 1984, Phase equilibria in four lysolecithin-water systems, submitted. Google Scholar
  6. Berger, B., Carty, C. E., and Ingram, L. O., 1980, Alcohol-induced changes in the phospholipid molecular species of Escherichia coli, J. Bacteriol. 142:1040.PubMedGoogle Scholar
  7. Boggs, J. M., Stamp, D. W., and Deber, C.M., 1981, Influence of ether linkage on the lamellar to hexagonal phase transition of ethanolamine phospholipids, Biochemistry 20:5728.PubMedGoogle Scholar
  8. Boni, L. T., Stewart, T. P., Alderfer, J. L., and Hui, S. W. 1981, Lipid-polyethylene glycol interactions. I. Induction of fusion between liposomes, J. Membr. Biol. 62:65.PubMedGoogle Scholar
  9. Brentel, I., Arvidson, G., and Lindblom, G., 1984a, Effect of fatty acids on the phase equilibria of lysolecithins, submitted.Google Scholar
  10. Brentel, I., Lindblom, G., Khan, A., Eriksson, P.-O., and Wieslander, Å., 1984b, Phase equilibria of glucolipids from membranes of Acholeplasma laidlawii, submitted.Google Scholar
  11. Brentel, I., Selstam, E., and Lindblom, G., 1984c, Phase diagrams of plant galactolipids forming cubic and reversed hexagonal phases, submitted.Google Scholar
  12. Browning, J. L., and Seelig, J., 1980, Bilayers of phosphatidylserine: A deuterium and phosphorus nuclear magnetic resonance study, Biochemistry 19:1262.PubMedGoogle Scholar
  13. Calhoun, W. I., and Shipley, G. G., 1979, Sphingomyelin-lecithin bilayers and their interaction with cholesterol, Biochemistry 18:1717.PubMedGoogle Scholar
  14. Carlsson, T., 1981, Law and order in wheat flour dough, Thesis, University of Lund, Lund, Sweden.Google Scholar
  15. Carnie, S., Israelachvili, J. N., and Pailthorpe, B. A., 1979, Lipid packing and transbilayer asymmetries of mixed lipid vesicles, Biochim. Biophys. Acta 554:340.PubMedGoogle Scholar
  16. Cevc, G., Watts, A., and Marsh, D., 1981, Titration of the phase transition of phosphatidylserine bilayer membranes, Biochemistry 20:4955.PubMedGoogle Scholar
  17. Chapman, D., 1975, Phase transitions and fluidity characteristics of lipids and cell membranes, Q. Rev. Biophys. 8:185.PubMedGoogle Scholar
  18. Chapman, D., Gómez-Fernández, J. C, and Goni, F. M., 1982, The interaction of intrinsic proteins and lipids in biomembranes, Trends Biochem. Sci. 7:67.Google Scholar
  19. Christiansson, A., and Wieslander, Å., 1978, Membrane lipid metabolism in Acholeplasma laidlawii A EF22, Eur. J. Biochem. 85:65.PubMedGoogle Scholar
  20. Christiansson, A., and Wieslander, Å., 1980, Control of membrane polar lipid composition in Acholeplasma laidlawii A by the extent of saturated fatty acid synthesis, Biochim. Biophys. Acta 595:189.PubMedGoogle Scholar
  21. Christiansson, A., Gutman, H., Wieslander, Å., and Lindblom, G., 1981, Effects of anesthetics on water permeability and lipid metabolism in Acholeplasma laidlawii membranes, Biochim. Biophys. Acta 645:24.PubMedGoogle Scholar
  22. Christiansson, A., Eriksson, L. E. G., Westman, J., and Wieslander, Å., 1984, Involvement of surface potential and ionic size in lipid regulation by Acholeplasma laidlawii membranes, submitted.Google Scholar
  23. Corda, D., Pasternak, C, and Shinitzky, M., 1982, Increase in lipid microviscosity of unila-mellar vesicles upon the creation of transmembrane potential, J. Membr. Biol. 65:235.PubMedGoogle Scholar
  24. Cowley, A. C., Fuller, N. L., Rand, R. P., and Parsegian, V. A., 1978, Measurement of repulsive forces between charged phospholipid bilayers, Biochemistry 17:3163.PubMedGoogle Scholar
  25. Crowley, J. M., 1973, Electrical breakdown of bimolecular lipid membranes as an electromechanical instability, Biophys. J. 13:711.PubMedGoogle Scholar
  26. Cullen, J., Phillips, M. C, and Shipley, G. G., 1971, The effects of temperature on the composition and physical properties of lipids of Pseudomonas fluorescens, Biochem. J. 125:733.PubMedGoogle Scholar
  27. Cullis, P. R., and de Kruijff, B., 1978, The polymorphic phase behaviour of phosphatidyle-thanolamines of natural and synthetic origin, Biochim. Biophys. Acta 513:31.PubMedGoogle Scholar
  28. Cullis, P. R., and Hope, M. J., 1980, The bilayer stabilizing role of sphingomyelin in the presence of cholesterol, Biochim. Biophys. Acta 597:533.PubMedGoogle Scholar
  29. Cullis, P. R., Verkleij, A. J., and Ververgaert, P. H. J. T., 1978a, Polymorphic phase behaviour of cardiolipin as detected by 31P NMR and freeze-fracture techniques, Biochim. Biophys. Acta 513:11.PubMedGoogle Scholar
  30. Cullis, P. R., van Dijck, P. W. M., de Kruijff, B., and de Gier, J., 1978b, Effects of cholesterol on the properties of equimolar mixtures of synthetic phosphatidylethanolamine and phos-phatidylcholine, Biochim. Biophys. Acta 513:21.PubMedGoogle Scholar
  31. Cullis, P. R., de Kruijff, B., Hope, M. J., Verkleij, A. J., Nayar, R., Farren, S. B., Tilcock, C., Madden, T. D., and Bally, M. B., 1982, Structural properties of lipids and their functional roles in biological membranes, in: Membrane Fluidity in Biology, Vol. 2 (R. C. Aloie, ed.), Academic Press, New York.Google Scholar
  32. Cunningham, C. C, and Sinthusek, G., 1979, Ionic charge on phospholipids and their interaction with mitochondrial adenosine triphosphatase, Biochim. Biophys. Acta 550:150.PubMedGoogle Scholar
  33. Curatolo, W., Small, D. M., and Shipley, G. G., 1977, Phase behaviour and structural characteristics of hydrated bovine brain gangliosides, Biochim. Biophys. Acta 468:11.PubMedGoogle Scholar
  34. Daniels, C. J., Bole, D. G., Quay, S. C, and Oxender, D. L., 1981, Role for membrane potential in the secretion of protein into the periplasm of Escherichia coli, Proc. Natl. Acad. Sci. USA 78:5396.PubMedGoogle Scholar
  35. Deese, A. J., Dratz, E. A., Dahlquist, F. W., and Paddy, M. R., 1981, Interaction of rhodopsin with two unsaturated phosphatidylcholines: A deuterium NMR study, Biochemistry 20:6420.PubMedGoogle Scholar
  36. de Kruijff, B., and Cullis, P. R., 1980, Cytochrome c specifically induces non-bilayer structures in cardiolipin-containing model membranes, Biochim. Biophys. Acta 602:477.PubMedGoogle Scholar
  37. de Kruijff, B., Verkleij, A. J., van Echteld, C. J. A., Gerritsen, W. J., Mombers, C., Noordam, P. C., and de Gier, J., 1979, The occurrence of lipidic particles in lipid bilayers as seen by 31P NMR and freeze-fracture electron-microscopy, Biochim. Biophys. Acta 555:200.PubMedGoogle Scholar
  38. Düzgünes, N., Wilschut, J., Fraley, R., and Papahadjopoulos, D., 1981, Studies on the mechanism of membrane fusion, Biochim. Biophys. Acta 642:182.PubMedGoogle Scholar
  39. Ekwall, P., 1975, Composition, properties and structures of liquid crystalline phases in systems of amphiphilic compounds, Adv. Liq. Cryst. 1:1.Google Scholar
  40. Enequist, H. G., Hirst, T. R., Harayama, S., Hardy, S. J. S., and Randall, L. L., 1981, Energy is required for maturation of exported proteins in Escherichia coli, Eur. J. Biochem. 116:227.PubMedGoogle Scholar
  41. Engelman, D. M., and Steitz, T. A., 1981, The spontaneous insertion of proteins into and across membranes: The helical hairpin hypothesis, Cell 23:411.PubMedGoogle Scholar
  42. Eriksson, P.-O., Khan, A., and Lindblom, G., 1982, Nuclear magnetic resonance studies of molecular motion and structure of cubic liquid crystalline phases, J. Phys. Chem. 86:387.Google Scholar
  43. Eriksson, P.-O., Arvidson, G., and Lindblom, G., 1983a, NMR studies of cholate-lecithin mixed micelles, Israel J. Chem., in press.Google Scholar
  44. Eriksson, P.-O., Johansson, L. B.-Å, and Lindblom, G., 1983b, NMR and polarized luminescence studies of cubic phases and model membranes, Proc. Int. Symp. on Surfactants in Solution, Lund.Google Scholar
  45. Eriksson, P.-O., Arvidson, G., and Lindblom, G., 1984, Molecular organization in phases of lecithin-cholate-water as studied by NMR, Hepatology, in press.Google Scholar
  46. Esko, J. D., and Raetz, C. R. H., 1980, Mutants of Chinese hamster ovary cells with altered membrane phospholipid composition, J. Biol. Chem. 255:4474.PubMedGoogle Scholar
  47. Farren, S. B., and Cullis, P. R., 1980, Polymorphism of phosphatidylglycerol-phosphatidyle-thanolamine model membrane systems: A 31P NMR study, Biochem. Biophys. Res. Commun. 97:182.PubMedGoogle Scholar
  48. Fernández, M. S., and Calderön, E., 1980, Formation of micelles and membrane action of the local anesthetic tetracaine hydrochloride, Biochim. Biophys. Acta 597:83.PubMedGoogle Scholar
  49. Fontell, K., 1981, Liquid crystallinity in lipid-water systems, Mol. Cryst. Liq. Cryst. 63:59.Google Scholar
  50. Freundt, E. A., and Edward, D. G., 1979, in The Mycoplasmas, Vol. 1 (M. F. Barile and S. Razin, eds.), pp. 1–42, Academic Press, New York.Google Scholar
  51. Fry, M., and Green, D. E., 1980, Cardiolipin requirement by cytochrome oxidase and the catalytic role of phospholipid, Biochem. Biophys. Res. Commun. 93:1238.PubMedGoogle Scholar
  52. Gallay, J., and de Kruijff, B., 1982, Correlation between molecular shape and hexagonal HII phase promoting ability of sterols, FEBS Lett. 143:133.PubMedGoogle Scholar
  53. Gaily, H. U., Pluschke, G., Overath, P., and Seelig, J., 1980, Structure of Escherichia coli membranes, Biochemistry 19:1638.Google Scholar
  54. Gasser, S. M., Ohashi, A., Daum, G., Böhni, P. C., Gibson, J., Reid, G. A., Yonetani, T., and Schatz, G., 1982, Imported mitochondrial proteins cytochrome b2 and cytochrome c1 are processed in two steps, Proc. Natl. Acad. Sci. USA 79:267.PubMedGoogle Scholar
  55. Ghosh, R., and Seelig, J., 1982, The interaction of cholesterol with bilayers of phosphatidy-lethanolamine, Biochim. Biophys. Acta 691:151.Google Scholar
  56. Grinius, L., 1980, Nucleic acid transport driven by ion gradient across cell membrane, FEBS Lett. 113:1.PubMedGoogle Scholar
  57. Gulik-Krzywicki, T., Rivas, E., and Luzzati, V., 1967, Structure et polymorphisme des lipides, J. Mol. Biol. 27:303.PubMedGoogle Scholar
  58. Gulik-Krzywicki, T., Shechter, E., Luzzati, V., and Faure, M., 1969, Interactions of proteins and lipids, Nature (London) 223:1116.Google Scholar
  59. Gulik-Krzywicki, T., Aggerbeck, L. P., and Larsson, K., 1983, The use of freeze-fracture and freeze-etching electron microscopy for phase analysis and structure determination of lipid systems, Proc. Int. Symp. on Surfactants in Solution, Lund.Google Scholar
  60. Gurr, M. I., and James, A. T., 1980, Lipid Biochemistry: An Introduction, 3rd ed., Chapman & Hall, London.Google Scholar
  61. Gutman, H., Arvidson, G., Fontell, K., and Lindblom, G., 1983, 31P and 2H NMR studies of phase equilibria in the three component system: Monoolein-dioleoylphosphatidylcholine-water, Proc. Int. Symp. on Surfactants in Solution, Lund.Google Scholar
  62. Harlos, K., and Eibl, H., 1980, Influence of calcium on phosphatidylethanolamine, Biochim. Biophys.Acta 601:113.PubMedGoogle Scholar
  63. Harlos, K., and Eibl, H., 1981, Hexagonal phases in phospholipids with saturated chains, Biochemistry 20:2888.PubMedGoogle Scholar
  64. Hiemenz, P. C, 1977, Principles of Colloid and Surface Chemistry, Dekker, New York.Google Scholar
  65. Hirata, F., and Axelrod, J., 1980, Phospholipid methylation and biological signal transmission, Science 209:1082.PubMedGoogle Scholar
  66. Hope, M. J., and Cullis, P. R., 1979, The lipid bilayer stability of inner monolayer lipids from the human erythrocyte, FEBS Lett. 107:323.PubMedGoogle Scholar
  67. Hope, M. J., and Cullis, P. R., 1980, Effects of divalent cations and pH on phosphatidylserine model membranes: A 31P NMR study, Biochem. Biophys. Res. Commun. 92:846.PubMedGoogle Scholar
  68. Hope, M. J., and Cullis, P. R., 1981, The role of nonbilayer lipid structures in the fusion of human erythrocyte induced by lipid fusogenes, Biochim. Biophys. Acta 640:82.PubMedGoogle Scholar
  69. Hornby, A. P., and Cullis, P. R., 1981, Influence of local and neutral anesthetics on the polymorphic phase preference of egg yolk phosphatidylethanolamine, Biochim. Biophys. Acta 647:285.PubMedGoogle Scholar
  70. Hubbard, S. C, and Brody, S., 1975, Glycerophospholipid variation in choline and inositol auxotrophs of Neurospora crassa, J. Biol. Chem. 250:7173.PubMedGoogle Scholar
  71. Hui, S. W., Stewart, T. P., and Yeagle, P. L., 1980, Temperature-dependent morphological and phase behaviour of sphingomyelin, Biochim. Biophys. Acta 601:271.PubMedGoogle Scholar
  72. Ingelman-Sundberg, M., Haaparanta, T., and Rydström, J., 1981, Membrane charge as effector of cytochrome P-450LM2 catalyzed reactions in reconstituted liposomes, Biochemistry 20:4100-4106.PubMedGoogle Scholar
  73. Ingram, L. O., 1976, Adaptation of membrane lipids to alcohols, J. Bacteriol. 125:670.PubMedGoogle Scholar
  74. Israelachvili, J. N., 1977, Refinement of the fluid-mosaic model of membrane structure, Biochim. Biophys. Acta 469:221.PubMedGoogle Scholar
  75. Israelachvili, J. N., Mitchell, D. J., and Ninham, B. W., 1976, Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers, J. Chem. Soc. Faraday Trans. II 72:1525.Google Scholar
  76. Israelachvili, J. N., Mitchell, D. J., and Ninham, B. W., 1977, Theory of self-assembly of lipid bilayers and vesicles, Biochim. Biophys. Acta 470:185.PubMedGoogle Scholar
  77. Israelachvili, J. N., Marčelja, S., and Horn, R. G., 1980, Physical principles of membrane organization. Q. Rev. Biophys. 13:121.PubMedGoogle Scholar
  78. Jain, M. K., van Echteld, C. J. A., Ramirez, F., de Gier, J., de Haas, G. H., and van Deenen, L. L. M., 1980, Association of lysophosphatidylcholine with fatty acids in aqueous phase to form bilayers, Nature (London) 284:486.Google Scholar
  79. Janiak, M. J., Small, D. M., and Shipley, G. G., 1979, Temperature and compositional dependence of the structure of hydrated dimyristoyllecithin, J. Biol. Chem. 254:6068.PubMedGoogle Scholar
  80. Johansson, L. B.-Å., and Lindblom, G., 1980, Orientation and mobility of molecules in membranes studied by polarized light spectroscopy, Q. Rev. Biophys. 13:63.PubMedGoogle Scholar
  81. Johansson, L. B.-Å., and Lindblom, G., 1981, Studies of chromophores in model membranes by polarized light-absorption spectroscopy, Biophys. J. 36:735.PubMedGoogle Scholar
  82. Kachar, B., and Reese, T. S., 1982, Evidence for the lipidic nature of tight junction strands, Nature (London) 296:464.Google Scholar
  83. Khan, A., Rilfors, L., Wieslander, Å., and Lindblom, G., 1981, The effect of cholesterol on the phase structure of glucolipids from Acholeplasma laidlawii membranes, Eur. J. Biochem. 116:215.PubMedGoogle Scholar
  84. Killian, J. A., de Kruijff, B., van Echteld, C. J. A., Verkleij, A. J., Leunissen-Bijvelt, J., and de Gier, J., 1983, Mixtures of gramicidin and lysophosphatidylcholine form lamellar structures, Biochim. Biophys. Acta 728:141.PubMedGoogle Scholar
  85. Kitagawa, T., Inoue, K., and Nojima, S., 1976, Properties of liposomal membranes containing lysolecithin, J. Biochem. 79:1123.PubMedGoogle Scholar
  86. Kito, M., Aibara, S., Kato, M., and Hata, T., 1972, Differences in fatty acid composition among phosphatidylethanolamine, phosphatidylglycerol and cardiolipin of Escherichia coli Biochim. Biophys. Acta 260:475.Google Scholar
  87. Kreil, G., 1981, Transfer of proteins across membranes, Ann. Rev. Biochem. 50:317.PubMedGoogle Scholar
  88. Kushwaha, S. C., Kates, M., Sprott, G. D., and Smith, I. C. P., 1981, Novel polar lipids from the metanogen Methanospirillum hungatei, Biochim. Biophys. Acta 664:156.PubMedGoogle Scholar
  89. Labedan, B., and Letellier, L., 1981, Membrane potential changes during the first steps of coliphage infection, Proc. Natl. Acad. Sci. USA 78:215.PubMedGoogle Scholar
  90. Larsson, K., and Puang-Ngern, S., 1979, The aqueous system of monogalactosyl diglycerides and digalactosyl diglycerides, in: Advances in the Biochemistry and Physiology of Plant Lipids (L.-Å. Appelqvist and C. Liljenberg, eds.), pp. 27–33, Elsevier, Amsterdam.Google Scholar
  91. Lindblom, G., Larsson, K., Johansson, L. B.-Å., Fontell, K., and Forsén, S., 1979, The cubic phase of monoglyceride-water systems, J. Am. Chem. Soc. 101:5465.Google Scholar
  92. Lindblom, G., Johansson, L. B.-Å, and Arvidson, G., 1981, Effect of cholesterol in membranes, Biochemistry 20:2204.PubMedGoogle Scholar
  93. Lindblom, G., Wieslander, Å., and Rilfors, L., 1984, Guest molecules as packing moderators in biological membranes, submitted.Google Scholar
  94. Loomis, C. R., Shipley, G. G., and Small, D. M., 1979, The phase behaviour of hydrated cholesterol, J. Lipid Res. 20:525.PubMedGoogle Scholar
  95. Lucy, J. A., 1970, The fusion of biological membranes, Nature (London) 227:814.Google Scholar
  96. Lutton, E. S., 1965, Phase of behavior of aqueous systems of monoglyerides, J. Am. Oil. Chem. Soc. 42:1068.PubMedGoogle Scholar
  97. Luzzati, V., 1968, X-ray diffraction studies of lipid-water systems, in: Biological Membranes (D. Chapman, ed.), pp. 71–123, Academic Press, New York.Google Scholar
  98. Luzzati, V., and Husson, F., 1962, The structure of the liquid-crystalline phases of lipid-water systems, J. Cell Biol. 12:207.PubMedGoogle Scholar
  99. Luzzati, V., Reiss-Husson, F., Rivas, E., and Gulik-Krzywicki, T., 1966, Structure and polymorphism in lipid-water systems, and their possible biological implications, Annals of the New York Academy of Sciences 137:409.PubMedGoogle Scholar
  100. Luzzati, V., Gulik-Krzywicki, T., Rivas, E., Reiss-Husson, F., and Rand, R. P., 1968, X-ray studies of model systems: Structure of the lipid-water phases in correlation with the chemical composition of the lipids, J. Gen. Physiol. 51:37S.PubMedGoogle Scholar
  101. Madden, T. D., and Cullis, P. R., 1982, Stabilization of bilayer structure for unsaturated phos-phatidylethanolamines by detergents, Biochim. Biophys. Acta 684:149.PubMedGoogle Scholar
  102. Mantsch, H. H., Martin, A., and Cameron, D. G., 1981, Characterization by infrared spectroscopy of the bilayer to nonbilayer phase transition of phosphatidylethanolamines, Biochemistry 20:3138.PubMedGoogle Scholar
  103. Means, A. R., and Dedman, J. R., 1980, Calmodulin-An intracellular calcium receptor, Nature (London) 285:73.Google Scholar
  104. Mitchell, D. J., and Ninham, B. W., 1981, Micelles, vesicles and microemulsions, J. Chem. Soc. Faraday Trans. II 77:601Google Scholar
  105. Nalȩcz, M. J., Zborowski, J., Famulski, K. S., and Wojtczak, L., 1980, Effect of phospholipid composition on the surface potential of liposomes and the activity of enzymes incorporated into liposomes, Eur. J. Biochem. 112:75.PubMedGoogle Scholar
  106. Nayar, R., Schmid, S. L., Hope, M. J., and Cullis, P. R., 1982, Structural preferences of phosphatidylinositol and phosphatidylinositol-phosphatidylethanolamine model membranes, Biochim. Biophys. Acta 688:169.PubMedGoogle Scholar
  107. Nesmeyanova, M. A., 1982, On the possible participation of acid phospholipids in the trans-location of secreted proteins through the bacterial cytoplasmic membrane, FEBS Lett. 142:189.PubMedGoogle Scholar
  108. Nicholls, D. G., 1982, Bioenergetics, Academic Press, New York.Google Scholar
  109. Ohkuma, S., and Poole, B., 1978, Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents, Proc. Natl. Acad. Sci. USA 75:3327.PubMedGoogle Scholar
  110. Ohno, Y., Yano, I., and Masui, M., 1979, Effect of NaCl concentration and temperature on the phospholipid and fatty acid compositions of a moderately halophilic bacterium, Pseudomonas halosaccharolytica, J. Biochem. (Tokyo) 85:413.Google Scholar
  111. Oldfield, E., 1982, NMR of protein-lipid interactions in model and biological membranes, in: Membranes and Transport (A. N. Martonosi, ed.), Vol. 1, pp. 115–123, Plenum Press, New York.Google Scholar
  112. Op den Kamp, J. A. F., 1979, Lipid asymmetry in membranes, Annu. Rev. Biochem. 48:47.PubMedGoogle Scholar
  113. Padan, E., Zilbertstein, D., and Schuldiner, S., 1981, pH homeostasis in bacteria, Biochim. Biophys. Acta 650:151.PubMedGoogle Scholar
  114. Paddy, M. R., Dahlquist, F. W., Davis, J. H., and Bloom, M., 1981, Dynamical and temperature-dependent effects of lipid-protein interactions, Biochemistry 20:3152.PubMedGoogle Scholar
  115. Pasquali-Ronchetti, I., Spisni, A., Casali, E. Masotti, L., and Urry, D. W., 1983, Gramicidin A induces lysolecithin to form bilayers, Bioscience Reports 3:127.PubMedGoogle Scholar
  116. Patton, S., 1970, Correlative relationship of cholesterol and sphingomyelin in cell membranes, J. Theor. Biol. 29:489.PubMedGoogle Scholar
  117. Portis, A., Newton, C., Pangborn, W., and Papahadjopoulos, D., 1979, Studies on the mechanism of membrane fusion, Biochemistry 18:780.PubMedGoogle Scholar
  118. Raetz, C. R. H., 1978, Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli, Microbiol. Rev. 42:614.PubMedGoogle Scholar
  119. Raetz, C. R. H., Kantor, G. D., Nishijima, M., and Newman, K. F., 1979, Cardiolipin accumulation in the inner and outer membranes of Escherichia coli mutants defective in phos-phatidylserine synthetase, J. Bacteriol. 139:544.PubMedGoogle Scholar
  120. Rand, R. P., and Sengupta, S., 1972, Cardiolipin forms hexagonal structures with divalent cations, Biochim. Biophys. Acta 255:484.PubMedGoogle Scholar
  121. Rand, R. P., Tinker, D. O., and Fast, P. G., 1971, Polymorphism of phosphatidylethanolamines from two natural sources, Chem. Phys. Lipids 6:333.PubMedGoogle Scholar
  122. Reiss-Husson, F., 1967, Structure des phases liquide-cristallines des différents phospholipides, monoglycérides, sphingolipides, anhydres ou en présence d’eau, J. Mol. Biol. 25:363.PubMedGoogle Scholar
  123. Rilfors, L., 1982, Regulation and physical properties of bacterial membrane lipids, Thesis, University of Lund, Lund.Google Scholar
  124. Rilfors, L., 1984, Membrane lipid composition in Acholeplasma laidlawii A grown on iso and anteiso branched-chain saturated fatty acids, submitted.Google Scholar
  125. Rilfors, L., Wieslander, Å., and StÅhl, S., 1978, Lipid and protein composition of membranes of Bacillus megaterium variants in the temperature range 5 to 70°C, J. Bacteriol. 135:1043.PubMedGoogle Scholar
  126. Rilfors, L., Khan, A., Brentel, I., Wieslander, Å., and Lindblom, G., 1982, Cubic liquid crystalline phase with phosphatidylethanolamine from Bacillus megaterium containing branched acyl chains, FEBS Lett. 149:293.Google Scholar
  127. Rivas, E., and Luzzati, V., 1969, Polymorphisme des lipides polaires et des galacto-lipides de chloroplastes de mais, en présence d’eau, J. Mol. Biol. 41:261.PubMedGoogle Scholar
  128. Ruocco, M. J., Atkinson, D., Small, D. M., Skarjune, R. P., Oldfield, E., and Shipley, G. G., 1981, X-ray diffraction and calorimetric study of anhydrous and hydrated N-palmitoyl-galactosylsphingosine (cerebroside), Biochemistry 20:5957.PubMedGoogle Scholar
  129. Sandermann, H., Jr., 1978, Regulation of membrane enzymes by lipids, Biochim. Biophys. Acta 515:209.PubMedGoogle Scholar
  130. Santos, E., and Kaback, H. R., 1981, Involvement of the proton electrochemical gradient in genetic transformation in Escherichia coli, Biochem. Biophys. Res. Commun. 99:1153.PubMedGoogle Scholar
  131. Sato, N., and Murata, N., 1980, Temperature shift-induced responses in lipids in the blue-green alga, Anabaena variabilis, Biochim. Biophys. Acta 619:353.PubMedGoogle Scholar
  132. Schleyer, M., Schmidt, B., and Neupert, W., 1982, Requirement of a membrane potential for the post-translocational transfer of proteins into mitochondria, Eur. J. Biochem. 125:109.PubMedGoogle Scholar
  133. Seddon, J. M., Cevc, G., and Marsh, D., 1983, Calorimetric studies of the gel-fluid (Lβ-Lα) and lamellar-inverted hexagonal (Lα-HII) phase transitions in dialkyl-and diacylphosphatidylethanolamines, Biochemistry 22:1280.PubMedGoogle Scholar
  134. Sen, A., Williams, W. P., and Quinn, P., 1981, The structure and thermotropic properties of pure 1,2-diacylgalactoglycerols in aqueous systems, Biochim. Biophys. Acta 663:380.PubMedGoogle Scholar
  135. Shipley, G. G., Green, J. P., and Nichols, B. N., 1973, The phase behaviour of monogalactosyl, digalactosyl, and sulphoquinosyl diglycerides, Biochim. Biophys. Acta 311:531.PubMedGoogle Scholar
  136. Shipley, G. G., Avecilla, L. S., and Small, D. M., 1974, Phase behaviour and structure of aqueous dispersions of sphingomyelin, J. Lipid Res. 15:124.PubMedGoogle Scholar
  137. Silvius, J. R., and McElhaney, R. N., 1978, Lipid compositional manipulation in Acholeplasma laidlawii B, Can. J. Biochem. 56:462.PubMedGoogle Scholar
  138. Silvius, J. R., Mak, N., and McElhaney, R. N., 1980, Lipid and protein composition and thermotropic lipid phase transitions in fatty acid-homogenous membranes of Acholeplasma laidlawii B, Biochim. Biophys. Acta 597:199.PubMedGoogle Scholar
  139. Singer, S. J., and Nicolson, G. L., 1972, The fluid mosaic model of the structure of cell membranes, Science 175:720.PubMedGoogle Scholar
  140. Small, D. M., 1967, Phase equilibria and structure of dry and hydrated egg lecithin, J. Lipid Res. 8:551.PubMedGoogle Scholar
  141. Small, D. M., Bourges, M., and Dervichian, D. G., 1966, Biophysics of lipidic associations. I. The ternary systems lecithin-bile salt-water, Biochim. Biophys. Acta, 125:563.PubMedGoogle Scholar
  142. Stier, A., Finch, S. A. E., and Bösterling, B., 1978, Non-lamellar structure in rabbit liver microsomal membranes, FEBS Lett. 91:109.PubMedGoogle Scholar
  143. Stulen, G., 1981, Electric field effects of lipid membrane structure, Biochim. Biophys. Acta 640:621.PubMedGoogle Scholar
  144. Sugar, I. P., 1979, A theory of the electric field-induced phase transitions of phospholipid bilayers, Biochim. Biophys. Acta 556:72.PubMedGoogle Scholar
  145. Tanford, C, 1980, The Hydrophobic Effect, 2nd ed., Wiley, New York.Google Scholar
  146. Taraschi, T. F., de Kruijff, B., Verkleij, A., and van Echteid, C. J. A., 1982, Effect of gly-cophorin on lipid polymorphism, Biochim. Biophys. Acta 685:153.PubMedGoogle Scholar
  147. Tartar, H. V., 1955, A theory of the structure of micelles of normal paraffin chain salts in aqueous solution, J. Phys. Chem. 59:1195.Google Scholar
  148. Teissie, J., and Tsong, T. Y., 1981, Electric field induced transient pores in phospholipid bilayer vesicles, Biochemistry 20:1548.PubMedGoogle Scholar
  149. Tiddy, G., 1980, Surfactant-water liquid crystal phases, Phys. Rep. 57:1.Google Scholar
  150. Tilcock, C. P. S., and Cullis, P. R. 1981, The polymorphic phase behaviour of mixed phos-phatidylserine-phosphatidylethanolamine model systems ad detected by 31P NMR, Biochim. Biophys. Acta 641:189.PubMedGoogle Scholar
  151. Tilcock, C. P. S., and Cullis, P. R., 1982, The polymorphic phase behaviour and miscibility properties of synthetic phosphatidylethanolamines, Biochim. Biophys. Acta 684:212.Google Scholar
  152. Ulmius, J., Wennerström, H., Lindblom, G., and Arvidson, G., 1977, Deuteron nuclear magnetic resonance studies of phase equilibria in a lecithin-water system, Biochemistry 16:5742.PubMedGoogle Scholar
  153. Ulmius, J., Lindblom, G., Wennerström, H., Johansson, L. B.-Å., Fontell, K., Söderman, O., and Arvidson, G., 1982, Molecular organization in the liquid-crystalline phases of lecithin-sodium cholate-water systems studied by nuclear magnetic resonance, Biochemistry 21:1553.PubMedGoogle Scholar
  154. van der Steen, A. T. M., de Jong, W. A. C., de Kruijff, B., and van Deenen, L. L. M., 1981, Lipid dependence of glycophorin-induced transbilayer movement of lysophosphatidylcho-line in large unilamellar vesicles, Biochim. Biophys. Acta 647:63.Google Scholar
  155. van Echteid, C. J. A., van Stigt, R., de Kruijff, B., Leunissen-Bijvelt, J., Verkleij, A. J., and de Gier, J., 1981a, Gramicidin promotes formation of the hexagonal HII phase in aqueous dispersions of phosphatidylethanolamine and phosphatidylcholine, Biochim. Biophys. Acta 648:287.Google Scholar
  156. van Echteld, C. J. A., de Kruijff, B., Mandersloot, J. G., and de Gier, J., 1981b, Effects of lysophosphatidylcholines on phosphatidylcholine and phosphatidylcholine/cholesterol liposome systems as revealed by 31P NMR, electron microscopy and permeability studies, Biochim. Biophys. Acta 649:211.PubMedGoogle Scholar
  157. van Meer, G., de Kruijff, B., Op den Kamp, J. A. F., and van Deenen, L. L. M., 1980, Preservation of the bilayer structure in human erythrocytes and erythrocyte ghosts after phospholipase treatment, Biochim. Biophys. Acta 596:1.PubMedGoogle Scholar
  158. van Nieuwenhoven, M. H., Hellingwerf, K. J., Venema, G., and Konings, W. N., 1982, Role of proton motive force in genetic transformation of Bacillus subtilis, J. Bacteriol. 151:771.PubMedGoogle Scholar
  159. van Venetië, R., and Verkleij, A. J., 1981, Analysis of the hexagonal II phase and its relations to lipidic particles and the lamellar phase, Biochim. Biophys. Acta 645:262.PubMedGoogle Scholar
  160. Verkleij, A. J., and de Gier, J., 1981, Freeze fracture studies on aqueous dispersions of membrane lipids, in: Liposomes: From Physical Structure to Therapeutic Applications (Knight, C. G. ed.), pp. 83–103, Elsevier, Amsterdam.Google Scholar
  161. Verkleij, A. J., de Maagd, R., Leunissen-Bijvelt, J., and de Kruijff, B., 1982, Divalent cations and chlorpromazine can induce non-bilayer structures in phosphatidic acid-containing model membranes, Biochim. Biophys. Acta 684:255.PubMedGoogle Scholar
  162. Vincent, M., and Gallay, J., 1983, Steroid-lipid interactions in sonicated dipalmitoyl phospha-tidyl choline vesicles, Biochem. Biophys. Res. Commun. 113:799.PubMedGoogle Scholar
  163. von Heijne, G., 1980, Trans-membrane translocation of proteins, Eur. J. Biochem. 103:431.Google Scholar
  164. Waksman, A., Hubert, P., Crémel, G., Rendon, A., and Burgun, C., 1980, Translocation of proteins through biological membranes, Biochim. Biophys. Acta 604:249.Google Scholar
  165. Watanabe, T., Fukushima, H., Kasai, R., and Nozawa, Y., 1981, Studies on thermal adaptation in Tetrahymena membrane lipids, Biochim. Biophys. Acta 665:66.PubMedGoogle Scholar
  166. Wennerström, H., 1979, The relation between micelle size and shape and the stability of liquid crystalline phases in surfactant systems, J. Colloid Interface Sci. 68:589.Google Scholar
  167. Wennerström, H., and Lindman, B., 1979, Micelles: Physical chemistry of surfactant association, Phys. Rep. 52:1.Google Scholar
  168. Wickner, W., 1980, Assembly of proteins into membranes, Science 210:864.Google Scholar
  169. White, S. H., King, G. I., and Cain, J. E., 1981, Location of hexane in lipid bilayers determined by neutron diffraction, Nature (London) 290:161.Google Scholar
  170. Wieslander, Å., Ulmius, J., Lindblom, G., and Fontell, K., 1978, Water binding and phase structures for different Acholeplasma laidlawii membrane lipids studied by deuteron nuclear magnetic resonance and X-ray diffraction, Biochim. Biophys. Acta 512:241.PubMedGoogle Scholar
  171. Wieslander, Å., Christiansson, A., Rilfors, L., and Lindblom, G., 1980, Lipid bilayer stability in membranes, Biochemistry 19:3650.PubMedGoogle Scholar
  172. Wieslander, Å., Rilfors, L., Johansson, L. B.-Å., and Lindblom, G., 1981a, Reversed cubic phase with glucolipids from Acholeplasma laidlawii, Biochemistry 20:730.PubMedGoogle Scholar
  173. Wieslander, Å., Christiansson, A., Rilfors, L., Khan, A., Johansson, L. B.-Å., and Lindblom, G., 1981b, Lipid phase structure governs the regulation of lipid composition in membranes of Acholeplasma laidlawii, FEBS Lett. 124:273.Google Scholar
  174. Zimmermann, U., 1982, Electric field-mediated fusion and related electrical phenomena, Biochim. Biophys. Acta, 694:227.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Leif Rilfors
    • 1
  • Göran Lindblom
    • 1
  • Åke Wieslander
    • 2
  • Anders Christiansson
    • 3
  1. 1.Department of Physical ChemistryUniversity of UmeåUmeåSweden
  2. 2.Department of BiochemistryUniversity of UmeåUmeåSweden
  3. 3.Department of MicrobiologyUniversity of LundLundSweden

Personalised recommendations