Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Organization and Dynamics of the Lipid Components of Biological Membranes

T. E. Thompson, M. B. Sankaram, C. Huang

10.1002/cphy.cp140102

Source: Supplement 31: Handbook of Physiology, Cell Physiology

Originally published: 1997

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Lipid Bilayer as A Structural and Functional Component of Biological Membranes
2 Molecular Structures of Membrane Lipids
2.1 Glycerophospholipids
2.2 Sphingolipids
2.3 Cholesterol
3 Lipid Composition of Some Mammalian Cell Membranes
4 Molecular Organization of Membrane Lipids
4.1 Lamellar Phases
4.2 Binary Phospholipid Mixtures
4.3 Nonlamellar Phases
5 Physical Properties of Bilayers
5.1 Experimental Bilayer Systems
5.2 Bilayer Thickness
5.3 Electrical Properties
5.4 Permeability to Non‐Ionic Solutes
5.5 Mechanical Properties of Bilayers
6 Lipid Dynamics in Bilayer Systems
6.1 Intramolecular Motions
6.2 Whole Molecule Motions
7 Bilayer Curvature
Figure 1. Figure 1.

Structures of common membrane lipids.
Figure 2. Figure 2.

Molecular structure of C(14):C(14)PC, based on torsional angles of x‐ray crystallographic structure B of C(14):C(14)PC dihydrate determined by Pearson and Pascher 150. A: Ball‐and‐stick model. B: Computer‐generated diagram with van der Waals spheres of atoms.
Figure 3. Figure 3.

Molecular models depicting molecular (top) and acyl chain (bottom) packing arrangement of fully hydrated C(18):C(2)PC in crystalline (A) and gel (B) phases.

Taken with kind permission from Huang et al., 1984 85
Figure 4. Figure 4.

Molecular models depicting bilayer structure of C(18):C(10)PC with mixed interdigitated packing motif. A: Ball‐and‐stick model. B: Computer‐generated diagram with van der Waals spheres of atoms.
Figure 5. Figure 5.

Two types of partially interdigitated packing motif. A: One C(14):C(14)PC molecule in one leaflet pairs with two C(14):C(14)PC molecules in the opposing leaflet B: One C(14):C(14)PC molecule pairs with another single C(14):C(14)PC molecule in the opposing leaflet.
Figure 6. Figure 6.

Representative DSC heating thermograms for aqueous dispersions of C(18):C(10)PC (left) and C(16):C(16)PC (right). The phase transition curves observed at left for C(18):C(10)PC are virtually identical in the first and second heating scans. The first DSC heating scan for C(16):C(16)PC, shown at right, has three discernible transitions; however, only two (the Lβ′→Pβ′ and Pβ′→Lα) transitions are detectable in the second heating scan. The lowest‐temperature (the Lc→Lβ′) transition observed in the first heating scan is abolished in the second heating scan.
Figure 7. Figure 7.

Representative DSC heating thermograms for aqueous dispersions of C(12):C(12)PE. Bottom: First heating scan showing Lc → Lα phase transition with Tm = 43.0 °C and ΔH = 13.6 kcal/mol, and top: second heating scan showing the Lβ → Lα phase transition with lower transition temperature and smaller peak area (Tm = 30.6 °C and ΔH = 3.7 kcal/mol).
Figure 8. Figure 8.

Phase diagrams for (A) an isomorphous system with complete miscibility in both gel (G) and liquid‐crystalline (L) phases, (B) a peritectic system showing extensive gel‐gel immiscibility region (G1 + G2), and (C) a eutectic system showing partial gel‐gel phase separation (G1 + G2) combined with liquid‐crystalline (L) phase miscibility.
Figure 9. Figure 9.

Topology of the normal, type I, and inverse, type II, hexagonal, and cubic phases, a: Normal hexagonal phase, HI b: inverted hexagonal phase, HII, c: “plumber's nightmare” bicontinuous cubic phase, and d: “double diamond” bicontinuous cubic phase.

Adapted from Tate et al., 1991 183
Figure 10. Figure 10.

Molecular organization of the four phases of dipalmitoylphosphatidylcholine as determined from low‐angle x‐ray data.

Taken with kind permission from Figure 6 on p. 487 of Small, 1986 176
Figure 11. Figure 11.

Superposition of ten consecutive time frames of single‐molecule simulation. Time interval between superimposed coordinate sets varies from 100 fs (a) to 10 ns (f), increasing by a factor of 10 between each part of figure.

Taken with kind permission from de Loof et al., 1991 53
Figure 12. Figure 12.

Cross‐section of a minimum radius vesicle.

Taken with kind permission from p. 5 of Thompson et al., 1974 187


Figure 1.

Structures of common membrane lipids.



Figure 2.

Molecular structure of C(14):C(14)PC, based on torsional angles of x‐ray crystallographic structure B of C(14):C(14)PC dihydrate determined by Pearson and Pascher 150. A: Ball‐and‐stick model. B: Computer‐generated diagram with van der Waals spheres of atoms.



Figure 3.

Molecular models depicting molecular (top) and acyl chain (bottom) packing arrangement of fully hydrated C(18):C(2)PC in crystalline (A) and gel (B) phases.

Taken with kind permission from Huang et al., 1984 85


Figure 4.

Molecular models depicting bilayer structure of C(18):C(10)PC with mixed interdigitated packing motif. A: Ball‐and‐stick model. B: Computer‐generated diagram with van der Waals spheres of atoms.



Figure 5.

Two types of partially interdigitated packing motif. A: One C(14):C(14)PC molecule in one leaflet pairs with two C(14):C(14)PC molecules in the opposing leaflet B: One C(14):C(14)PC molecule pairs with another single C(14):C(14)PC molecule in the opposing leaflet.



Figure 6.

Representative DSC heating thermograms for aqueous dispersions of C(18):C(10)PC (left) and C(16):C(16)PC (right). The phase transition curves observed at left for C(18):C(10)PC are virtually identical in the first and second heating scans. The first DSC heating scan for C(16):C(16)PC, shown at right, has three discernible transitions; however, only two (the Lβ′→Pβ′ and Pβ′→Lα) transitions are detectable in the second heating scan. The lowest‐temperature (the Lc→Lβ′) transition observed in the first heating scan is abolished in the second heating scan.



Figure 7.

Representative DSC heating thermograms for aqueous dispersions of C(12):C(12)PE. Bottom: First heating scan showing Lc → Lα phase transition with Tm = 43.0 °C and ΔH = 13.6 kcal/mol, and top: second heating scan showing the Lβ → Lα phase transition with lower transition temperature and smaller peak area (Tm = 30.6 °C and ΔH = 3.7 kcal/mol).



Figure 8.

Phase diagrams for (A) an isomorphous system with complete miscibility in both gel (G) and liquid‐crystalline (L) phases, (B) a peritectic system showing extensive gel‐gel immiscibility region (G1 + G2), and (C) a eutectic system showing partial gel‐gel phase separation (G1 + G2) combined with liquid‐crystalline (L) phase miscibility.



Figure 9.

Topology of the normal, type I, and inverse, type II, hexagonal, and cubic phases, a: Normal hexagonal phase, HI b: inverted hexagonal phase, HII, c: “plumber's nightmare” bicontinuous cubic phase, and d: “double diamond” bicontinuous cubic phase.

Adapted from Tate et al., 1991 183


Figure 10.

Molecular organization of the four phases of dipalmitoylphosphatidylcholine as determined from low‐angle x‐ray data.

Taken with kind permission from Figure 6 on p. 487 of Small, 1986 176


Figure 11.

Superposition of ten consecutive time frames of single‐molecule simulation. Time interval between superimposed coordinate sets varies from 100 fs (a) to 10 ns (f), increasing by a factor of 10 between each part of figure.

Taken with kind permission from de Loof et al., 1991 53


Figure 12.

Cross‐section of a minimum radius vesicle.

Taken with kind permission from p. 5 of Thompson et al., 1974 187
References
 1. Almeida, P.F.F., W.L.C. Vaz, and T. E. Thompson. Lateral diffusion and percolation in two‐phase, two‐component lipid bilayers. Topology of the solid‐phase domains in‐plane and across the lipid bilayer. Biochemistry 31: 7198–7210, 1992.
 2. Almeida, P.F.F., 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: 6739–6747, 1992.
 3. Andersen, O. Permeability properties of unmodified lipid bilayer membranes. In: Membrane Transport in Biology, edited by G. Giebisch, D. C. Tosteson, and H. H. Ussing, Berlin: Springer‐Verlag, 1978, p. 370–372.
 4. Andersen, O. Ion movement through gramicidin A channels. Single‐channel measurements at very high potentials. Biophys. J. 41: 119–133, 1983.
 5. McMurray, W. C. Phospholipids of subcellular organelles and membranes. In: Form and Function of Phospholipids, edited by G. B. Ansell, J. N. Hawthorne, and R. M. C. Dawson, Amsterdam: Elsevier, 1973, p. 205–223.
 6. Auger, M., D. Carrier, I. C. P. Smith, and H. C. Jarrell. Elucidation of motional modes in glycoglycerolipid bilayers. A 2H NMR relaxation and line‐shape study. J. Am. Chem. Soc. 112: 1373–1381, 1990.
 7. Auger, M., I.C.P. Smith, and H. C. Jarrell. Slow motions in lipid bilayers. Direct detection by two‐dimensional solid‐state deuterium nuclear magnetic resonance. Biophys. J. 59: 31–38, 1991.
 8. Auger, M., M.‐R. Van Calsteren, I.C.P. Smith, and H. C. Jarrell. Glycerolipids: common features of molecular motion in bilayers. Biochemistry 29: 5815–5821, 1990.
 9. Bangham, A. D. and D. A. Haydon. Ultrastructure of membranes: biomolecular organization. Br. Med. Bull. 24: 124–126, 1968.
 10. Bangham, A. D., M. W. Hill, and N.G.A. Miller. Preparation and use of liposomes as models of biological membranes. In: Methods in Membrane Biology, Volume 1, edited by E. D. Korn, New York: Plenum Press, 1974, p. 1–68.
 11. Bangham, A. D., M. M. Standish, and J. C. Watkins. Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13: 238–252, 1965.
 12. Bangham, A. D., M. M. Standish, and G. Weissman. The action of steroids and streptolysin S on the permeability of phospholipid structures to cations. J. Mol. Biol. 13: 253–259, 1965.
 13. Bankaitis, V. A., J. R. Aitken, A. E. Cleves, and W. Dowhan. An essential role for a phospholipid transfer protein in yeast golgi function. Nature 347: 561–562, 1990.
 14. Barchfeld, G. L. and D. W. Deamer. The effect of general anesthetics on the proton and potassium permeability of liposomes. Biochim. Biophys. Acta 819: 161–169, 1985.
 15. Barton, P. G. and F. D. Gunstone. Hydrocarbon chain packing and molecular motion in phospholipid bilayers formed from unsaturated lecithins. J. Biol. Chem. 250: 4470–4476, 1975.
 16. Bennet, V. Spectrin, a structural mediator between diverse plasma membrane proteins and the cytoplasm. Curr. Opin. Cell Biol. 2: 51–56, 1990.
 17. Berkowitz, M. L. and K. Raghavan. Computer simulation of a water/membrane interface. Langmuir 7: 1042–1044, 1991.
 18. Blok, M. C., E.C.M. Van Der Neut‐Kok, L.L.M. Van Deenen, and J. De Gier. The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes. Biochim. Biophys. Acta 406: 187–196, 1975.
 19. Bloom, M. and E. Sternin. Transverse nuclear spin relaxation in phospholipid bilayer membranes. Biochemistry 26: 2101–2105, 1987.
 20. Bonmatin, J.‐M., I.C.P. Smith, H. C. Jarrell, and D. J. Siminovitch. Use of a comprehensive approach to molecular dynamics in ordered lipid systems: cholesterol reorientation in oriented lipid bilayers. A 2H NMR relaxation case study. J. Am. Chem. Soc. 112: 1697–1704, 1990.
 21. Boys, C. V. Soap Bubbles. Their Colors and The Forces That Mold Them, New York: Dover Publications, 1959, p. 60–61.
 22. Bresselers, G.J.M., H. L. Goderis, and P. P. Tobback. Measurement of the glucose permeation rate across phospholipid bilayers using small unilamellar vesicles. Effect of membrane composition and temperature. Biochim. Biophys. Acta 772: 374–382, 1984.
 23. Brian, A. A. and H. M. McConnell. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci. U.S.A. 81: 6159–6163, 1984.
 24. Brown, M. F. Theory of spin‐lattice relaxation in lipid bilayers and biological membranes. 2H and 14N quadrupolar relaxation. J. Chem. Phys. 77: 1576–1599, 1982.
 25. Brown, M. F. Theory of spin‐lattice relaxation in lipid bilayers and biological membranes. Dipolar relaxation. J. Chem. Phys. 80: 2808–2836, 1984.
 26. Brown, M. F., A. A. Ribeiro, and G. D. Williams. New view of lipid bilayer dynamics from 2H and 13C NMR relaxation time measurements. Proc. Natl. Acad. Sci. U.S.A. 80: 4325–4329, 1983.
 27. Brown, M. F., J. Seelig, and U. Haeberlen. Structural dynamics in phospholipid bilayers from deuterium spin‐lattice relaxation time measurements. J. Chem. Phys. 70: 5045–5053, 1979.
 28. Brown, R. E., F. A. Stephenson, T. Markello, Y. Barenholz, and T. E. Thompson. Properties of a specific glycolipid transfer protein from bovine brain. Chem. Phys. Lipids 38: 79–93, 1985.
 29. Brumbaugh, E. E. and C. Huang. Parameter estimation in binary mixtures of phospholipids. Methods Enzymol. 210: 521–539, 1992.
 30. Brunner, J., D. E. Graham, H. Hauser, and G. Semenza. Ion and sugar permeabilities of lecithin bilayers: comparison of curved and planar bilayers. J. Membr. Biol. 57: 133–141, 1980.
 31. Bultmann, T., H‐N. Lin, Z‐Q. Wang, and C. Huang. Thermotropic and mixing behavior of mixed‐chain phosphatidylcholines with molecular weights identical with L‐α‐dipalmitoylphosphatidylcholine. Biochemistry 30: 7194–7202, 1991.
 32. Büldt, G. H., J. Gally, J. Seelig, and G. Zaccai. Neutron diffraction studies on phosphatidylcholine model membranes. I. Head group conformation. J. Mol. Biol. 134: 673–691, 1979.
 33. Carnie, S., J. N. Israelachvili, and B. A. Pailthorpe. Lipid packing and transbilayer asymmetries of mixed lipid vesicles. Biochim. Biophys. Acta 554: 340–357, 1979.
 34. Carrier, D., J. B. Giziewicz, D. Moir, I.C.P. Smith, and H. C. Jarrell. Dynamics and orientation of glycolipid headgroups by 2H‐NMR: gentiobiose. Biochim. Biophys. Acta 983: 100–108, 1989.
 35. Castello, M. J. and T. Gulik‐Krzywicki. Correlated x‐ray diffraction and freeze‐fracture studies on model membrane systems. Perturbations induced by freeze‐fracture preparation procedures. Biochim. Biophys. Acta 455: 412–432, 1976.
 36. Cevc, G. Polymorphism of the bilayer membranes in the ordered phase and the molecular origin of the lipid pretransition and rippled lamellae. Biochim. Biophys. Acta 1062: 59–69, 1991.
 37. Cevc, G. and D. Marsh. Phospholipid Bilayers: Physical Principles and Models, New York: John Wiley and Sons, 1987, p. 3–12.
 38. Cevc, G. and D. Marsh. Phospholipid Bilayers: Physical Principles and Models, New York: John Wiley and Sons, 1987, p. 29–46.
 39. Cevc, G. and D. Marsh. Phospholipid Bilayers: Physical Principles and Models, New York: John Wiley and Sons, 1987, p. 19–24.
 40. Cevc, G. and D. Marsh. Phospholipid Bilayers: Physical Principles and Models, New York: John Wiley and Sors, 1987, p. 157–195.
 41. Chang, H. and R. M. Epand. The existence of a highly ordered phase in fully hydrated dilauroylphosphatidylethanolamine. Biochim. Biophys. Acta 728: 319–324, 1983.
 42. Cherry, R. J. and D. Chapman. Refractive index determination of lecithin black films. J. Mol. Biol. 30: 551–553, 1967.
 43. Cherry, R. J. and D. Chapman. Optical properties of black lecithin films. J. Mol. Biol. 40: 19–32, 1969.
 44. Chowdhry, B. Z., G. Lipka, A. W. Dalziel, and J. M. Sturtevant. Multicomponent phase transitions of diacyl phosphatidylethanolamine dispersions. Biophys. J. 45: 901–904, 1984.
 45. Clegg, R. M. and W.L.C. Vaz. Translational diffusion of proteins and lipids in artificial lipid bilayer membranes. A comparison of experiment with theory. In: Progress in Protein‐Lipid Interactions, edited by A. Watts, Amsterdam: Elsevier, 1985, p. 173–229.
 46. Clegg, S. G., and T. E. Thompson. Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine membranes with coexisting gel and liquid‐crystalline phases. Biophys. J. 68: 2333–2341, 1995.
 47. Clerq, S. G., and T. E. Thompson. A possible mechanism for vesicle formation by extensions. Biophys. J. 67: 475–477, 1995.
 48. Cullis, P. R. and B. De Kruijff. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta 559: 399–420, 1979.
 49. Curatolo, W., B. Sears, and L. J. Neuringer. A calorimetry and deuterium NMR study of mixed model membranes of 1‐palmitoyl‐2‐oleylphosphatidylcholine and saturated phosphatidylcholines. Biochim. Biophys. Acta 817: 261–270, 1985.
 50. Danielli, J. F. and H. Davson. A contribution to the theory of the permeability of thin films. J. Cell. Comp. Physiol. 5: 495–508, 1935.
 51. Davis, J. H. Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys. J. 27: 339–358, 1979.
 52. Davis, J. H. Deuterium nuclear magnetic resonance and relaxation in partially ordered systems. Adv. Magn. Res. 13: 195–222, 1989.
 53. De Loof, H., S. C. Harvey, J. P. Segrest, and R. W. Pastor. Mean field stochastic boundary molecular dynamics simulation of a phospholipid in a membrane. Biochemistry 30: 2099–2113, 1991.
 54. Devaux, P., C. J. Scandella, and H. M. McConnell. Spin‐spin interactions between spin‐labelled phospholipids. J. Magn. Res. 9: 474–485, 1973.
 55. Dowhan, W. Phospholipid‐transfer proteins. Curr. Opin. Cell Biol. 3: 621–625, 1991.
 56. Edidin, M. Molecular associations in membrane domains. Curr. Top. Membr. Transplant. 36: 81–96, 1990.
 57. Edidin, M. The variety of cell surface membrane domains. Comments Mol. Cell. Biophys. 8: 73–82, 1992.
 58. El‐Mashak, E. M. and T. Y. Tsong. Ion selectivity of temperature‐induced and electric field induced pores in dipalmitoylphosphatidylcholine vesicles. Biochemistry 24: 2884–2888, 1985.
 59. Ellena, J. F., L. S. Lepore, and D. S. Cafiso. Estimating lipid lateral diffusion in phospholipid vesicles from 13C spin‐spin relaxation. J. Phys. Chem. 97: 2952–2957, 1993.
 60. Evans, E. and D. Needham. Physical properties of surfactant bilayer membranes. J. Phys. Chem. 91: 4219–4288, 1987.
 61. Evans, E. A. Bending resistance and chemically induced moments in membrane bilayers. Biophys. J. 14: 923–931, 1974.
 62. Evans, E. A. and R. M. Hochmuth. Mechanochemical properties of membranes. In: Current Topics in Membranes and Transport, edited by F. Bonner and A. Kleinzeller, New York: Academic Press, 1978, p. 1–64.
 63. Evans, E. A. and R. Skalak. Mechanics and thermodynamics of biomembranes. Crit. Rev. Bio Eng. 3: 294–299, 1979.
 64. Fajer, P., A. Watts, and D. Marsh. Saturation transfer, continuous wave saturation, and saturation recovery electron spin resonance studies of chain‐spin labeled phosphatidylcholines in the low temperature phases of dipalmitoyl phosphatidylcholine bilayers. Effects of rotational dynamics and spin‐spin interactions. Biophys. J. 61: 879–891, 1992.
 65. Fettiplace, R., L.M.G. Gordon, S. B. Hladky, J. Requena, H. P. Zingsheim, and D. A. Haydon. Techniques in the formation and examination of black lipid bilayer membranes. In: Methods in Membrane Biology, Volume 4, edited by E. D. Korn, New York: Plenum Press, 1975, p. 1–75.
 66. Finkelstein, A. Water and nonelectrolyte permeability of lipid bilayer membranes. J. Gen. Physiol. 68: 127–135, 1976.
 67. Florio, E., H. C. Jarrell, D. B. Fenske, K. R. Barber, and C.W.M. Grant. Glycosphingolipid interdigitation in phospholipid bilayers examined by deuterium NMR and EPR. Biochim. Biophys. Acta 1025: 157–163, 1990.
 68. Fricke, H. The electric capacity of suspensions with special reference to blood. J. Gen. Physiol. 9: 137–152, 1925.
 69. Fromherz, P. and D. Ruppel. Lipid vesicle formation: the transition from open discs to closed shells. FEBS Lett. 179: 155–159, 1985.
 70. Füldner, H. H. Characterization of a third phase transition in multilamellar dipalmitoyllecithin liposomes. Biochemistry 20: 5707–5710, 1981.
 71. Grell, E. Membrane Spectroscopy, Berlin: Springer‐Verlag, 1981, 498 p.
 72. Gruner, S. M. Intrinsic curvature hypothesis for biomembrane lipid composition. Proc. Natl. Acad. Sci. U.S.A. 82: 3665–3669, 1985.
 73. Guidotti, G. Membrane proteins: structure, arrangement and disposition in membranes. In: Physiology of Membrane Disorders, edited by T. E. Andreoli, J. F. Hoffman, D. D. Fanestil, and S. G. Schultz, New York: Plenum Press, 1986, p. 45–55.
 74. Hauser, H., O. Oldani, and M. C. Philips. Mechanism of ion escape from phosphatidylcholine and phosphatidylserine single bilayer vesicle. Biochemistry 12: 4507–4517, 1973.
 75. Henn, F. A., G. L. Decker, J. W. Greenawalt, and T. E. Thompson. The properties of lipid bilayer membranes separating two aqueous phases: Electron microscope studies. J. Mol. Biol. 24: 51–58, 1967.
 76. Henn, F. A. and T. E. Thompson. Properties of lipid bilayer membranes separating two aqueous phases. J. Mol. Biol. 31: 227–235, 1968.
 77. Henn, F. A. and T. E. Thompson. Synthetic lipid bilayer membranes. Annu. Rev. Biochem. 38: 241–262, 1969.
 78. Hope, M. J., M. B. Baley, G. Webb, and P. R. Cullis. Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta 812: 55–65, 1985.
 79. Huang, C. Studies on phosphatidylcholine vesicles: formation and physical characteristics. Biochemistry 8: 344–352, 1969.
 80. Huang, C. Roles of carbonyl oxygens at the bilayer interface in phospholipid‐sterol interaction. Nature 259: 242–244, 1976.
 81. Huang, C. A structural model for the cholesterol‐phosphatidylcholine complexes in bilayer membranes. Lipids 12: 348–356, 1977.
 82. Huang, C. Mixed‐chain phospholipids and interdigitated bilayer systems. Klin. Wochenschrift 68: 149–165, 1990.
 83. Huang, C., S. Li, Z‐Q. Wang, and H‐N. Lin. Dependence of the bilayer transition temperatures on the structural parameters of phosphatidylcholines. Lipids 28: 365–370, 1993.
 84. Huang, C. and J. T. Mason. Geometric packing constraints in egg phospahtidylcholine vesicles. Proc. Natl. Acad. Sci. U.S.A. 75: 308–310, 1978.
 85. Huang, C., J. T. Mason, F. A. Stephenson, and I. W. Levin. Raman and 31P NMR spectroscopic identification of a highly ordered lamellar phase in aqueous dispersions of 1‐stearoyl‐2‐acetyl‐sn‐glycero‐3‐phosphorylcholine. J. Phys. Chem. 88: 6454–6458, 1984.
 86. Huang, C., J. T. Mason, F. A. Stephenson, and I. W. Levin. Polymorphic phase behavior of platelet‐activating factor. Biophys. J. 49: 587–595, 1986.
 87. Huang, C. and T. E. Thompson. Properties of lipid bilayer membranes separating two aqueous phases: determination of membrane thickness. J. Mol. Biol. 13: 183–193, 1965.
 88. Huang, C. and T. E. Thompson. Thickness of bilayer membranes. J. Mol. Biol. 16: 576, 1966.
 89. Huang, C., Z‐Q. Wang, H‐N. Lin, and E. E. Brumbaugh. Calorimetric studies of fully hydrated phosphatidylcholines with highly asymmetric acyl chains. Biochim. Biophys. Acta 1145: 298–310, 1993.
 90. Hubbell, W. L. Transbilayer coupling mechanism for the formation of lipid asymmetry in biological membranes. Application to the photoreceptor disc membranes. Biophys. J. 57: 99–108, 1990.
 91. Hui, S. W. and C. Huang. X‐ray diffraction evidence for fully interdigitated bilayers of 1‐stearoyllysophosphatidylcholine. Biochemistry 25: 1330–1335, 1986.
 92. Hui, S. W., J. T. Mason, and C. Huang. Acyl chain interdigitation in saturated mixed‐chain phosphatidylcholine bilayer dispersions. Biochemistry 23: 5570–5577, 1984.
 93. Israelachvili, J. N., D. J. Mitchell, and B. W. Ninham. Theory of self‐assembly of lipid bilayers and vesicles. Biochim. Biophys. Acta 470: 185–201, 1977.
 94. Jain, M. K. The Bimolecular Lipid Membrane—A System, New York: Van Nostrad Reinhold, 1972, p. 52–84.
 95. Jain, M. K. The Bimolecular Lipid Membrane—A System. New York: Van Nostrad Reinhold, 1972, p. 112–132.
 96. Janiak, M. J., D. M. Small, and G. G. Shipley. Nature of the pretransition of synthetic phospholipids: dimyristoyl and dipalmitoyl phosphatidylcholine. Biochemistry 15: 4575–4580, 1976.
 97. Jarrell, H. C., J. B. Giziewicz, and I.C.P. Smith. Structure and dynamics of a glyceroglycolipid: A 2H NMR study of head group orientation, ordering, and effect on lipid aggregate structure. Biochemistry 25: 3950–3957, 1986.
 98. Jones, J. D. and T. E. Thompson. Spontaneous phosphatidylcholine transfer by collision between vesicles at high lipid concentration. Biochemistry 28: 129–134, 1989.
 99. Jovin, T. M. and W.L.C. Vaz. Rotational and translational diffusion in membranes measured by fluorescence and phosphorescence methods. Methods Enzymol. 172: 471–512, 1989.
 100. Kalb, E., S. Frey, and L. K. Tamm. Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers. Biochim. Biophys. Acta 1103: 307–316, 1992.
 101. Kanfer, J. N. and S. Hakomori. Sphingolipid Biochemistry. New York: Plenum Press, 1983, p. 89–135.
 102. Karplus, M. and G. A. Petsko. Molecular dynamics simulations in biology. Nature 347: 631–639, 1990.
 103. Katz, S. L., H. M. Laboda, L. R. McLean, and M. C. Phillips. Influence of molecular packing and phospholipid types on rates of cholesterol exchange. Biochemistry 27: 3416–3423, 1988.
 104. Kornberg, R. D. and H. M. McConnell. Inside‐outside transitions of phospholipids in vesicle membranes. Biochemistry 10: 1111–1120, 1971.
 105. Koynova, R. and H‐J. Hinz. Metastable behavior of saturated phosphatidylethanolamines: a densitometric study. Chem. Phys. Lipids 54: 67–72, 1990.
 106. Kwok, R. and E. Evans. Thermoelasticity of large lecithin bilayer vesicles. Biophys. J. 35: 637–652, 1981.
 107. Lasic, D. D. A molecular model for vesicle formation. Biochim. Biophys. Acta 692: 501–502, 1982.
 108. Lasic, D. D. A general model for vesicle formation. J. Theor. Biol. 124: 35–41, 1987.
 109. Lasic, D. D. The mechanism of vesicle formation. Biochem. J. 256: 1–11, 1988.
 110. Lee, A. G. Lipid phase transitions and phase diagrams. II. Mixtures involving lipids. Biochim. Biophys. Acta 472: 285–344, 1977.
 111. Lewis, B. A. and D. M. Engelman. Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166: 211–217, 1983.
 112. Lewis, R.N.A.H. and R. N. McElhaney. Structures of the subgel phases of n‐saturated diacyl phosphatidylcholine bilayers: FTIR spectroscopic studies of 13C0 and 2H labelled lipids. Biophys. J. 67: 63–77, 1992.
 113. Lewis, R.N.A.H. and R. N. McElhaney. Calorimetric and spectroscopic studies of the polymorphic phase behavior of a homologous series of n‐saturated 1, 2‐diacylphosphatidylethanolamines. Biophys. J. 64: 1081–1096, 1993.
 114. Li, S., Z‐Q. Wang, H‐N. Lin, and C. Huang. Energy‐minimized structures and packing states of a homologous series of mixedchain phosphatidylcholines: a molecular mechanics study on the diglyceride moieties. Biophys. J. 65: 1415–1428, 1993.
 115. Lichtenberg, D., E. Friere, C. F. Schmidt, Y. Barenholz, P. L. Feigner, and T. E. Thompson. The effect of surface curvature on the stability, thermodynamic behavior and osmotic activity of single lamellar dipalmitoylphosphatidylcholine vesicles. Biochemistry 20: 3462–3467, 1981.
 116. Lichtenberg, L. and Y. Barenholz. Liposomes: preparation, characterization and preservation. In: Methods of Biochemical Analysis, edited by D. Glick, 1988, p. 337–462.
 117. Lin, H‐N. and C. Huang. Eutectic phase behavior of 1‐stearoyl‐2‐caprylphosphatidylcholine and dimyristoylphosphatidylcholine mixtures. Biochim. Biophys. Acta 946: 178–184, 1988.
 118. Lindblom, G. and L. Rilfors. Cubic phases and isotropic structures formed by membrane lipids—possible biological relevance. Biochim. Biophys. Acta 988: 221–256, 1989.
 119. Lipowsky, R. The conformation of membranes. Nature 349: 475–481, 1991.
 120. Luzzati, V. X‐ray diffraction studies of lipid‐water systems. In: Biological Membranes, edited by D. Chapman, New York: Academic Press, 1968, p. 71–123.
 121. Luzzati, V. and F. Husson. The structure of the liquid crystalline phases of lipid‐water systems. J. Cell Biol. 12: 207–219, 1962.
 122. Mabrey, S. and J. M. Sturtevant. Investigation of phase transitions of lipids and lipid mixtures by high sensitivity differential scanning calorimetry. Proc. Natl. Acad. Sci. U.S.A. 73: 3862–3866, 1976.
 123. Mantsch, H. H., S. C. Hsi, K. W. Butler, and D. G. Cameron. Studies on the thermotropic behavior of aqueous phosphatidylethanolamines. Biochim. Biophys. Acta 728: 325–330, 1983.
 124. Mariani, P. The cubic phases. Curr. Opin. Struct. Biol. 1: 501–505, 1991.
 125. Mariani, P., V. Luzzati, and H. Delacroix. Cubic phases of lipid‐containing systems. Structure analysis and biological implications. J. Mol. Biol. 204: 165–189, 1988.
 126. Marsh, D. Molecular motion in phospholipid bilayers in the gel phase: long axis rotation. Biochemistry 19: 1632–1637, 1980.
 127. Marsh, D. CRC Handbook of Lipid Bilayers. Boca Raton: CRC Press, 1990, 387 p.
 128. Marsh, D. Handbook of Lipid Bilayers. Boca Raton: CRC Press, 1990, p. 87–120.
 129. Mason, J. T., C. Huang, and R. L. Biltonen. Calorimetric investigations of saturated mixed‐chain phosphatidylcholine bilayer dispersions. Biochemistry 20: 6086–6092, 1981.
 130. Mason, J. T. and F. A. Stephenson. Thermotropic properties of saturated mixed acyl phosphatidylethanolamines. Biochemistry 29: 590–598, 1990.
 131. Mattai, J., P. K. Sripada, and G. G. Shipley. Mixed‐chain phosphatidylcholine bilayers: structure and properties. Biochemistry 26: 3287–3297, 1987.
 132. Mayer, L. D., M. J. Hope, and P. Cullis. Vesicles of variable size produced by a rapid extrusion procedure. Biochim. Biophys. Acta 858: 161–168, 1986.
 133. McIntosh, T. J. and S. A. Simon. Area per molecule and distribution of water in fully hydrated dilauroyiphosphatidylethanolamine bilayers. Biochemistry 25: 4948–4952, 1986.
 134. McIntosh, T. J., S. A. Simon, J. Ellington, and N. A. Porter. New structural model for mixed‐chain phosphatidylcholine bilayers. Biochemistry 23: 4038–4044, 1984.
 135. McLean, L. R. and M. C. Phillips. Mechanism of cholesterol and phosphatidylcholine exchange or transfer between unilamellar vesicles. Biochemistry 20: 2893–2900, 1981.
 136. Melo, E.C.C., I.M.G. Lourtie, M. B. Sankaram, T. E. Thompson, and W. L. C. Vaz. Effects of domain connection and disconnection on the yields of in‐plane bimolecular reactions in membranes. Biophys. J. 63: 1506–1512, 1992.
 137. Meraldi, J.‐P. and J. Schlitter. A statistical mechanical treatment of fatty acyl chain order in phospholipid bilayers and correlation with experimental data. A. theory. Biochim. Biophys. Acta 645: 183–192, 1981.
 138. Mimms, L. T., G. Zampighi, Y. Nozaki, C. Tanford, and J. A. Reynolds. Phospholipid vesicle formation and transmembrane protein incorporation using octyl glucoside. Biochemistry 20: 833–840, 1981.
 139. Montal, M. Formation of bimolecular membranes from lipid monolayers. Methods Enzymol. 32: 545–556, 1974.
 140. Mueller, P., D. O. Rudin, H. T. Tien, and W. C. Wescott. Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 194: 979–980, 1962.
 141. Mulukutla, S. and G. G. Shipley. Structural and thermotropic properties of phosphatidylethanolamine and its N‐methyl derivatives. Biochemistry 23: 2514–2519, 1984.
 142. Nicklas, K., J. Bocker, M. Schlenkrich, J. Brickmann, and P. Bopp. Molecular dynamics studies of the interface between a model membrane and an aqueous solution. Biophys. J. 60: 261–272, 1991.
 143. Nigg, E. and R. Cherry. Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface, protein rotational diffusion measurements. Proc. Natl. Acad. Sci. U.S.A. 77: 4702–4706, 1980.
 144. Nordlund, J. R., C. F. Schmidt, S. N. Dicken, and T. E. Thompson. Transbilayer distribution of phosphatidylethanolamine in large and small unilamellar vesicles. Biochemistry 20: 3237–3241, 1981.
 145. Nozaki, Y. and C. Tanford. Proton and hydroxide ion permeability of phospholipid vesicles. Proc. Natl. Acad. Sci. U.S.A. 78: 4324–4328, 1981.
 146. Pagano, R. and T. E. Thompson. Spherical bilayer membranes. Biochim. Biophys. Acta 144: 666–669, 1967.
 147. Pagano, R. and T. E. Thompson. Spherical lipid bilayer membranes: Electrical and isotopic studies of ion permeability. J. Mol. Biol. 38: 41–57, 1968.
 148. Pascher, I., M. Lundmark, P.‐G. Nyholm, and S. Sundell. Crystal structures of membrane lipids. Biochim. Biophys. Acta 1113: 339–373, 1992.
 149. Pastor, R. W., R. M. Venable, and M. Karplus. Model for the structure of the lipid bilayer. Proc. Natl. Acad. Sci. U.S.A. 88: 892–896, 1991.
 150. Pearson, R. H. and I. Pascher. The molecular structure of lecithin hydrate. Nature 281: 499–501, 1979.
 151. Peterson, D. C. Water permeation through the lipid bilayer membrane. Test of the liquid hydrocarbon model. Biochim. Biophys. Acta 600: 666–677, 1980.
 152. Redwood, W. R., W. Takashima, H. P. Schwan, and T. E. Thompson. Dielectric studies on homogeneous phosphatidylcholine vesicles. Biochim. Biophys. Acta 255: 557–566, 1992.
 153. Reeves, J. P. and R. M. Dowben. Formation and properties of thin‐walled phospholipid vesicles. J. Cell Physiol. 73: 49–60, 1969.
 154. Requena, J. and D. A. Haydon. Lenses and the compression of black lipid membranes by an electric field. Biophys. J. 15: 77–81, 1975.
 155. Robertson, R. N. and T. E. Thompson. The function of phospholipid polar groups in membranes. FEBS Lett. 74: 16–19, 1977.
 156. Rodgers, W. and M. Glaser. Characterization of lipid domains in erythrocyte membranes. Proc. Natl. Acad. Sci. U.S.A. 88: 1364–1368, 1991.
 157. Roseman, M., B. J. Litman, and T. E. Thompson. Transbilayer exchange of phosphatidylethanolamine for phosphatidylcholine and N‐acetamidoylphosphatidylethanolamine in single‐walled bilayer vesicles. Biochemistry 14: 4826–4830, 1975.
 158. Ruocco, M. J. and G. G. Shipley. Characterization of the subtransition of hydrated dipalmitoyl phosphatidylcholine bilayers: kinetic hydration and structural study. Biochim. Biophys. Acta 691: 309–320, 1982.
 159. Ruocco, M. J. and G. G. Shipley. Characterization of the subtransition of hydrated dipalmitoyl phosphatidylcholine bilayers: X‐ray diffraction study. Biochim. Biophys. Acta 684: 59–66, 1982.
 160. Sackmann, E. Physical foundation of the molecular organization and dynamics of membranes. In: Biophysics, edited by W. Hoppe, W. Lohman, H. Marlet, and H. Ziegler, Berlin: Springer‐Verlag, 1983, p. 425–433.
 161. Sankaram, M. B. and T. E. Thompson. Deuterium magnetic resonance study of phase equilibria and membrane thickness in binary phospholipid mixed bilayers. Biochemistry 31: 8258–8268, 1992.
 162. Seddon, J. M. Structure of the inverted hexagonal (HII) phase, and non‐lamellar phase transitions of lipids. Biochim. Biophys. Acta 1031: 1–69, 1990.
 163. Seddon, J. M., G. Cevc, R. D. Kaye, and D. Marsh. X‐ray diffraction study of the polymorphism of hydrated diacyl‐ and dialkylphosphatidylethanolamines. Biochemistry 23: 2634–2644, 1984.
 164. Seddon, J. M., K. Harlos, and D. Marsh. Metastability and polymorphism in the gel and fluid bilayer phases of dilauroylphosphatidylethanolamine. Two crystalline forms in excess water. J. Biol. Chem. 258: 3850–3854, 1983.
 165. Seelig, A. and J. Seelig. The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry 13: 4839–4845, 1974.
 166. Seifert, U., K. Berndl, and R. Lipowsky. Shape transformations in vesicles: phase diagram for spontaneous curvature and bilayer‐coupling models. Phys. Rev. 44: 1182–1202, 1991.
 167. Servas, R. M., W. Harbich, and W. Helfrich. Measurement of the curvature‐elastic modules of egg lecithin bilayers. Biochim. Biophys. Acta 436: 900–903, 1976.
 168. Shah, J., P. K. Sripada, and G. G. Shipley. Structure and properties of mixed‐chain phosphatidylcholine bilayers. Biochemistry 29: 4254–4262, 1990.
 169. Shepherd, J.C.W. and G. Büldt. Zwitterionic dipoles as a dielectric probe for investigating head group mobility in phospholipid membranes. Biochim. Biophys. Acta 514: 83–94, 1978.
 170. Siegel, D. P. Inverted micellar intermediates and the transitions between lamellar, cubic and inverted hexagonal lipid phases. I. Mechanism of the Lα‐HII phase transitions. Biophys. J. 49: 1155–1170, 1986.
 171. Simon, S. A. A comment on the water permeability through planar lipid bilayers. J. Gen. Physiol. 70: 123–125, 1977.
 172. Singer, S. J. and G. L. Nicholson. The fluid mosaic model of the structure of cell membranes. Science 175: 720–731, 1972.
 173. Sisk, R. B., Z‐Q. Wang, H‐N. Lin, and C. Huang. Mixing behavior of identical molecular weight phosphatidylcholines with various chain‐length differences in two‐component lamellae. Biophys. J. 58: 777–784, 1991.
 174. Slater, J. L. and C. Huang. Lipid bilayer interdigitation. In: The Structure of Biological Membranes, edited by P. L. Yeagle, Boca Raton: CRC Press, 1992, p. 175–210.
 175. Slater, J. L., C. Huang, R. G. Adams, and I. W. Levin. Polymorphic phase behavior of lysophosphatidylethanolamine dispersions. A thermodynamic and spectroscopic characterization. Biophys. J. 56: 243–252, 1989.
 176. Small, D. M. The Physical Chemistry of Lipids. From Alkanes to Phospholipids. New York: Plenum Press, 1986, 672 p.
 177. Speyer, J. B., R. T. Weber, S. K. Das Gupta, and R. G. Griffin. Anisotropic 2H NMR spin‐lattice relaxation in Lα‐phase cerebroside bilayers. Biochemistry 28: 9569–9574, 1989.
 178. Stauffer, D. Introduction to Percolation Theory. London: Taylor and Francis, 1985, 124 p.
 179. Suurkuusk, J., B. R. Lentz, Y. Barenholz, R. L. Biltonen, and T. E. Thompson. A calorimetric and fluorescent probe study of the gel‐liquid crystalline phase transition in small, single‐walled dipalmitoylphosphatidylcholine vesicles. Biochemistry 15: 1393–1401, 1976.
 180. Sweeley, C. C. and B. Siddiqui. Chemistry of mammalian glycolipids. In: The Glycoconjugates, Volume I, edited by M. I. Horowitz and W. Pigman, New York: American Press, 1977, p. 459–540.
 181. Szoka, F. and D. Papahadjopoulos. Comparative properties and methods of preparation of lipid vesicle (liposomes). Annu. Rev. Biophys. Biomol. Chem. 9: 467–508, 1980.
 182. Tadros, T. F. and B. Vincent. Emulsion stability. In: Encyclopedia of Emulsion Technology, Volume 1, edited by P. Becher, New York: Marcel Dekker, 1983, p. 129–285.
 183. Tate, M. W., E. F. Eikenberry, D. C. Turner, E. Shyamsunder, and S. M. Gruner. Nonbilayer phases of membrane lipids. Chem. Phys. Lipids 57: 147–164, 1991.
 184. Tenchov, B. G., A. I. Boyanov, and R. D. Koynova. Lyotropic polymorphism of racemic dipalmitoylphosphatidylethanolamine. A differential scanning calorimetry study. Biochemistry 23: 3553–3558, 1984.
 185. Thompson, T. E. and F. A. Henn. Experimental phospholipid model membranes. In: Structure and Function of Membranes of Mitochondria and Chloroplasts, edited by E. Racker, New York: Van Nostrad Reinhold, 1969, p. 1–52.
 186. Thompson, T. E. and C. Huang. Composition and dynamics of lipids in biomembranes. In: Physiology of Membrane Disorders, edited by T. Andreoli, R. D. Fannestil, J. F. Hoffman, and S. G. Schulz, New York: Plenum, 1985, p. 25–44.
 187. Thompson, T. E., C. Huang, and B. J. Litman. Bilayers and biomembranes: compositional asymmetries induced by surface curvature. In: The Cell Surface in Development, edited by A. A. Moscona, New York: John Wiley and Sons, 1974, p. 1–16.
 188. Thompson, T. E., B. Lentz, and Y. Barenholz. A calorimetric and fluorescent probe study of phase transitions in phosphatidylcholine liposomes. In: Biochemistry of Membrane Transport, edited by G. Semenza and E. Carafoli, Berlin: Springer‐Verlag, 1977, p. 47–71.
 189. Thompson, T. E., M. B. Sankaram, and R. L. Biltonen. Biological membrane domains: functional significance. Comments Mol. Cell. Biophys. 8: 1–15, 1992.
 190. Thompson, T. E. and T. W. Tillack. Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu. Rev. Biophys. Biophys. Chem. 14: 361–386, 1985.
 191. Tien, H. T. Bilayer Lipid Membranes (BLM), New York: Marcel Dekker, 1974, p. 11–28.
 192. Tien, H. T. Black Lipid Membranes (BLM), New York: Marcel Dekker, 1974, p. 117–163.
 193. Tilcock, C.P.S. Lipid polymorphism. Chem. Phys. Lipids 40: 109–125, 1986.
 194. Toyoshima, Y. and T. E. Thompson. Chloride flux in bilayer membranes: The electrically silent chloride flux in semispherical bilayers. Biochemistry 14: 1518–1524, 1975.
 195. Toyoshima, Y. and T. E. Thompson. Chloride flux in bilayer membranes: chloride permeability in aqueous dispersions of single‐walled, bilayer vesicles. Biochemistry 14: 1525–1531, 1975.
 196. Trahms, L., W. D. Klabe, and L. Koroske. 1H NMR study of the three low temperature phases of DPPC‐water systems. Biophys. J. 42: 285–293, 1983.
 197. Ueno, M., C. Tanford, and J. Reynolds. Phospholipid vesicle formation using nonionic detergents with low monomer solubility. Kinetic factors determine vesicle size and permeability. Biochemistry 23: 3070–3076, 1984.
 198. Ulrich, A. S., F. Volke, and A. Watts. The dependence of phospholipid and head‐group mobility on hydration as studied by deuterium‐NMR spin‐lattice relaxation time measurements. Chem. Phys. Lipids 55: 61–66, 1990.
 199. Van Der Leeuw, Y.C.W. and G. Stulen. Proton relaxation measurements on lipid membranes oriented at the magic angle. J. Magn. Reson. Imaging, 42: 434–445, 1981.
 200. Vance, D. F. and J. E. Vance. Biochemistry of Lipids and Membranes, San Francisco: Benjamin/Cummings, 1985, p. 30.
 201. Vaz, W.L.C. Translational diffusion in phase‐separated lipid bilayer membranes. Comments Mol. Cell. Biophys. 8: 17–36, 1992.
 202. Vaz, W.L.C., E.C.C. Melo, and T. E. Thompson. Translational diffusion and fluid domain connectivity in a two‐component, two‐phase phospholipid bilayer. Biophys. J. 56: 869–876, 1989.
 203. Verkman, A. S. Water channels in cell membranes. Annu. Rep. Physiol. 54: 97–108, 1992.
 204. Ververgaert, P. H. and P. E. Elbers. Ultrastructural analysis of black lipid membranes. J. Mol. Biol. 58: 431–437, 1971.
 205. Vinson, P. K., Y. Talmon, and A. Walter. Vesicle‐micelle transition of phosphatidylcholine and octyl glucoside elucidated by cryotransmission electron microscopy Biophys. J. 56: 669–681, 1989.
 206. Walter, A. and J. W. Gutknecht. Permeability of small nonelectrolytes through lipid bilayer membranes. J. Membr. Biol. 90: 207–217, 1986.
 207. Weisz, K., G. Grobner, C. Mayer. J. Stohrer, and G. Kothe. Deuteron nuclear magnetic resonance study of the dynamic organization of phospholipid/cholesterol bilayer membranes: molecular properties and viscoelastic properties. Biochemistry 31: 1100–1112, 1992.
 208. Wiener, M. C. and S. H. White. Fluid bilayer structure determination by the combined use of x‐ray and neutron diffraction. I. Fluid bilayer models and the limits of resolution. Biophys. J. 59: 162–173, 1991.
 209. Wiener, M. C. and S. H. White. Fluid bilayer structure determination by the combined use of x‐ray and neutron diffraction. II. The composition space refinement method. Biophys. J. 59: 174–185, 1991.
 210. Wiener, M. C. and S. H. White. Fluid bilayer structure determination by combined use of x‐ray and neutron diffraction. III. The complete structure. Biophys. J. 61: 434–447, 1992.
 211. Wilkinson, D. A. and J. F. Nagle. Metastability in the phase behavior of dimyristoylphophatidylethanolamine bilayers. Biochemistry 23: 1538–1541, 1984.
 212. Williamson, P., A. Kulick, A. Zachowski, R. A. Schlegel, and P. F. Devaux. Ca2+ induces transbilayer redistribution of all major phospholipids in human erythrocytes. Biochemistry 31: 6355–6360, 1992.
 213. Wong, P.T.T. and C. Huang. Structural aspects of pressure effects on infrared spectra of mixed‐chain phosphatidylcholine assemblies in D2O. Biochemistry 28: 1259–1263, 1989.
 214. Wong, P.T.T., D. J. Siminovitch, and H. H. Mantsch. Structure and properties of model membranes: new knowledge from high‐pressure vibrational spectroscopy. Biochim. Biophys. Acta 947: 139–171, 1988.
 215. Woolley, G. A. and B. A. Wallace. Model ion channels: gramicidin and alamethicin. J. Membr. Biol. 129: 109–136, 1992.
 216. Wyatt, K. and R. Cherry. Both ankyrin and band 4.1 are required to restrict the rotational mobility of band 3 in the human erythrocyte membrane. Biochim. Biophys. Acta 1103: 327–330, 1992.
 217. Xu, H. and C. Huang. Scanning calorimetric study of fully hydrated asymmetric phosphatidylcholines with one acyl chain twice as long as the other. Biochemistry 26: 1036–1043, 1987.
 218. Xu, H., F. A. Stephenson, H‐N. Lin, and C. Huang. Phase metastability and supercooled metastable state of diundecanoyl‐phosphatidylethanolamine bilayers. Biochim. Biophys. Acta 943: 63–75, 1988.
 219. Ye, R. and A. S. Verkman. Simultaneous optical measurement of osmotic and diffusional water permeability in cells and liposomes. Biochemistry 28: 824–829, 1989.
 220. Yeh, H. C. Interpretation of phase diagrams. In: Phase Diagrams: Materials Science and Technology, edited by A. M. Alper, New York: Academic Press, 1970, p. 167–197.
 221. Zaccai, G., G. Büldt, A. Seelig, and J. Seelig. Neutron diffraction studies on phosphatidylcholine model membranes. II. Chain conformation and segmental disorder. J. Mol. Biol. 134: 693–706, 1979.
 222. Zachowski, A. and P. F. Devaux. Bilayer asymmetry and lipid transport across biomembranes. Comments Mol. Cell. Biophys. 6: 63–90, 1989.
 223. Zachowski, A., E. Favre, S. Cribier, P. Herve, and P. F. Devaux. Outside‐inside translocation of aminophospholipids in the human erythrocyte membrane is maintained by a specific enzyme. Biochemistry 25: 2585–2590, 1986.
 224. Zhu, T. and M. Caffrey. Thermodynamic, thermomechanical and structural properties of a hydrated asymmetric phosphatidylcholine. Biophys. J. 65: 939–954, 1993.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Organization and Dynamics of the Lipid Components of Biological Membranes
 

How to Cite

T. E. Thompson, M. B. Sankaram, C. Huang. Organization and Dynamics of the Lipid Components of Biological Membranes. Compr Physiol 2011, Supplement 31: Handbook of Physiology, Cell Physiology: 23-57. First published in print 1997. doi: 10.1002/cphy.cp140102