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Physical properties of lipid bilayer membranes: relevance to membrane biological functions.

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Over the last 25 years one of us (WKS) has been investigating physical properties of lipid bilayer membranes. In 1991 a group led by WKS was organized into the Laboratory of Structure and Dynamics of Biological Membranes, the effective member of which is AW. Using mainly the electron paramagnetic resonance (EPR) spin-labeling method, we obtained unexpected results, which are significant for the better understanding of the functioning of biological membranes. We have developed a new pulse EPR spin-labeling method for the detection of membrane domains and evaluation of lipid exchange rates. This review will be focused on our main results which can be summarized as follows: (1) Unsaturation of alkyl chains greatly reduces the ordering and rigidifying effects of cholesterol although the unsaturation alone gives only minor fluidizing effects, as observed by order and reorientational motion, and rather significant rigidifying effects, as observed by translational motion of probe molecules; (2) Fluid-phase model membranes and cell plasma membranes are not barriers to oxygen and nitric oxide transport; (3) Polar carotenoids can regulate membrane fluidity in a way similar to cholesterol; (4) Formation of effective hydrophobic barriers to the permeation of small polar molecules across membranes requires alkyl chain unsaturation and/or the presence of cholesterol; (5) Fluid-phase micro-immiscibility takes place in cis-unsaturated phosphatidylcholine-cholesterol membranes and induces the formation of cholesterol-rich domains; (6) In membranes containing high concentrations of transmembrane proteins a new lipid domain is formed, with lipids trapped within aggregates of proteins, in which the lipid dynamics is diminished to the level of gel-phase.
Physical description
  • Biophysics Research Institute, Medical College of Wisconsin, Milwaukee, Wisconsin, U.S.A.
  • Biophysics Department, Institute of Molecular Biology, Jagiellonian University, Kraków, Poland
  • 1. Gorter, E. & Grendel, F. (1925) On bimolecular layers of lipid on the chromacytes of blood. J. Exp. Med. 41, 439-443.
  • 2. Danielli, J.F. & Dawson, H. (1935) A contribution of the theory of permeability of thin films. J. Cell Comp. Physiol. 5, 495-508.
  • 3. Singer, S.J. & Nicolson, G.L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720-731.
  • 4. Robertson, R.N. (1983) The Lively Membranes. Cambridge University Press.
  • 5. Kusumi, A., Subczynski, W.K., Pasenkiewicz- Gierula, M., Hyde, J.S. & Merkle, H. (1986) Spin label study on phosphatidylcholine-cholesterol membranes: Effect of alkyl chain length and unsaturation in fluid phase. Biochim. Biophys. Acta 854, 307-317.
  • 6. Subczynski, W.K., Markowska, E., Gruszecki, W.I. & Sielewiesiuk, J. (1992) Effect of polar carotenoids on dimyristoylphosphatidylcholine: A spin-label study. Biochim. Biophys. Acta 1105, 97-108.
  • 7. Subczynski, W.K., Markowska, E. & Sielewiesiuk, J. (1993) Spin-label studies on phosphatidylcholine-polar carotenoid membranes: Effects of alkyl chain length and unsaturation. Biochim. Biophys. Acta 1150, 173-181.
  • 8. Subczynski, W.K., Lewis, R.N.A., McElhaney, R.N., Hodges, R.S., Hyde, J.S. & Kusumi, A. (1998) Molecular organization and dynamics of 1-palmitoyl-2-oleoyl-phosphatidylcholine bilayers containing a transmembrane alpha-helical peptide. Biochemistry 37, 3156-3164.
  • 9. Pasenkiewicz-Gierula, M., Subczynski, W.K. & Kusumi, A. (1990) Rotational diffusion of a steroid molecule in phosphatidylcholine-cholesterol membranes: Fluid phase micro- immiscibility in unsaturated phosphatidylcholine-cholesterol membranes. Biochemistry 29, 4059-4069.
  • 10. Kusumi, A., Subczynski, W.K. & Hyde, J.S. (1982) Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels. Proc. Natl. Acad. Sci. U.S.A. 79, 1854-1858.
  • 11. Subczynski, W.K., Antholine, W.E., Hyde, J.S. & Petering, D.H. (1987) Orientation and mobility of copper square planar complex in a lipid bilayer. J. Am. Chem. Soc. 109, 46-52.
  • 12. Subczynski, W.K., Hyde, J.S. & Kusumi, A. (1989) Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proc. Natl. Acad. Sci. U.S.A. 86, 4474-4478.
  • 13. Subczynski, W.K., Antholine, W.E., Hyde, J.S. & Kusumi, A. (1990) Micro-immiscibility and three-dimensional dynamic structure of phosphatidylcholine-cholesterol membranes: Translational diffusion of copper complex in the membrane. Biochemistry 29, 7936-7945.
  • 14. Subczynski, W.K., Hyde, J.S. & Kusumi, A. (1991) Effect of alkyl chain unsaturation and cholesterol intercalation on oxygen transport in membranes: A pulse ESR spin labeling study. Biochemistry 30, 8578-8590.
  • 15. Subczynski, W.K., Pasenkiewicz-Gierula, M., Antholine, W.E. & Hyde, J.S. (1999) Oriented self-association of copper (II) tetraphenylporphine in liquid-crystalline lipid bilayer membranes: An EPR study. J. Am. Chem. Soc. 121, 4054-4059.
  • 16. Pasenkiewicz-Gierula, M. & Subczynski, W.K. (1996) Structure and dynamics of lipid bilayer membranes comparison of EPR and molecular dynamics simulation results. Curr. Top. Biophys. 20, 93-98.
  • 17. Pasenkiewicz-Gierula, M., Rog, T., Kitamura, K. & Kusumi, A. (2000) Cholesterol effects on the phosphatidylcholine bilayer polar region: A molecular simulation study. Biophys. J. 78, 1376-1389.
  • 18. Subczynski, W.K. (1999) Spin-label oximetry in biological and model systems. Curr. Top. Biophys. 23, 69-77.
  • 19. Kusumi, A. & Pasenkiewicz-Gierula, M. (1988) Rotational diffusion of a steroid molecule in phosphatidylcholine membranes: Effects of alkyl chain length, unsaturation and cholesterol as studied by a spin-label method. Biochemistry 27, 4407-4415.
  • 20. Subczynski, W.K., Markowska, E. & Sielewiesiuk, J. (1991) Effect of polar carotenoids on the oxygen diffusion-concentration product in lipid bilayers. An ESR spin label study. Biochim. Biophys. Acta 1068, 68-72.
  • 21. Yin, J.J. & Subczynski, W.K. (1996) Effects of lutein and cholesterol on alkyl chain bending in lipid bilayers: A pulse electron spin resonance spin labeling study. Biophys. J. 71, 832-839.
  • 22. Yin, J.J., Feix, J.B. & Hyde, J.S. (1990) Mapping of collision frequencies for stearic acid spin labels by saturation-recovery electron paramagnetic resonance. Biophys. J. 58, 713-720.
  • 23. Jain, M.K. & Wagner, R.F. (1980) Introduction to Biological Membranes. New York, Wiley.
  • 24. Stubbs, C.D. & Smith, A.D. (1984) The modification of mammalian polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim. Biophys. Acta 779, 89-137.
  • 25. Rohmer, M., Bouvier, P. & Ourisson, G. (1979) Molecular evolution of membranes: Structural equivalents and phylogenetic precursors of sterols. Proc. Natl. Acad. Sci. U.S.A. 76, 847-851.
  • 26. Yeagle, P.L. (1993) The biophysics and cell biology of cholesterol: A hypothesis for the essential role of cholesterol in mammalian cells; in Cholesterol in Membrane Models (Finegold, L., ed.) pp. 1-12, CRC Press.
  • 27. Wisniewska, A. & Subczynski, W.K. (1998) Effect of polar carotenoids on the shape of the hydrophobic barrier of phospholipid bilayers. Biochim. Biophys. Acta 1368, 235-246.
  • 28. Gruszecki, W.I. (1999) Carotenoids in membranes; in The Photochemistry of Carotenoids (Frank, H.A., Young, A.J., Britton, G. & Cogdell, R.J., eds.) pp. 363-379, Kluwer Academy Pub.
  • 29. Anwar, M., Khan, T.H., Prebble, J. & Zagalsky, P.F. (1977) Membrane-bound carotenoid in Micrococus luteus protects naphtoquinone from photodynamic action. Nature 270, 538-540.
  • 30. Yokoyama, A., Sandman, G., Hoshino, T., Adachi, K. Sakai, M. & Shizuri, Y. (1995) Thermozeaxanthins, new carotenoid-glycoside-esters from thermophilic eubacterium Thermus thermophilus. Tetrahedron Lett. 36, 4901-4904.
  • 31. Subczynski, W.K. & Markowska, E. (1992) Effect of carotenoids on oxygen transport within and across model membranes. Curr. Top. Biophys. 16, 62-68.
  • 32. Subczynski, W.K. & Hyde, J.S. (1981) The diffusion-concentration product of oxygen in lipid bilayers using the spin-label T1 method. Biochim. Biophys. Acta 643, 283-291.
  • 33. Subczynski, W.K. & Hyde, J.S. (1983) Concentration of oxygen in lipid bilayers using a spin-label method. Biophys. J. 41, 283-286.
  • 34. Subczynski, W.K. & Hyde, J.S. (1984) Diffusion of oxygen in water and hydrocarbons using an electron spin resonance spin label technique. Biophys. J. 45, 743-748.
  • 35. Subczynski, W.K., Hopwood, L.E. & Hyde, J.S. (1992) Is the mammalian cell plasma membrane a barrier to oxygen transport? J. Gen. Physiol. 100, 69-87.
  • 36. Ligeza, A., Tikhonov, A.N., Hyde, J.S. & Subczynski, W.K. (1998) Oxygen permeability of thylakoid membranes: Electron paramagnetic resonance spin labeling study. Biochim. Biophys. Acta 1365, 453-463.
  • 37. Ashikawa, I., Yin, J.J., Subczynski, W.K., Kouyama, T., Hyde, J.S. & Kusumi, A. (1994) Molecular organization and dynamics in bacteriorhodopsin-rich reconstituted membranes: Discrimination of lipid environments by the oxygen transport parameter using a pulse ESR spin-labeling technique. Biochemistry 33, 4947-4952.
  • 38. Kawasaki, K., Yin, J.J., Subczynski, W.K., Hyde, J.S., Ohnishi, S. & Kusumi, A. (1988) Observation of lipid exchange reaction between two domains in the outer membrane of influenza virus by a pulse ESR spin labeling method. XIII International Conference on Magnetic Resonance in Biological Systems, Madison, Wisconsin, U.S.A. abstract P13-31.
  • 39. Hyde, J.S. & Subczynski, W.K. (1989) Spin label oximetry; in Biological Magnetic Resonance. Vol. 8 Spin Labeling. Theory and Applications (Berliner, L.J. & Reuben, J., eds.) pp. 399-425, Plenum, NY.
  • 40. Skulachev, V.P. (1990) Power transmission along biological membranes. J. Membr. Biol. 114, 97-112.
  • 41. Subczynski, W.K., Renk, G.E., Crouch, R.K., Hyde, J.S. & Kusumi, A. (1992) Oxygen diffusion-concentration product in rhodopsin as observed by a pulse ESR spin labeling method. Biophys. J. 63, 573-577.
  • 42. Lomnicka, M. & Subczynski, W.K. (1996) Spin-label NO-metry. Curr. Top. Biophys. 20, 76-80.
  • 43. Subczynski, W.K., Lomnicka, M. & Hyde, J.S. (1996) Permeability of nitric oxide through lipid bilayer membranes. Free Radical Res. 24, 343-349.
  • 44. Subczynski, W.K. & Hyde, J.S. (1998) Spin-label NO-metry in lipid bilayer membranes; in Nitric Oxide in Transplant Rejection and Anti-Tumor Defense (Lukiewicz, S. & Zweier, J.L., eds.) pp. 95-108, Kluwer Academy Pub.
  • 45. Kharitonov, V.G., Sundquist, A.R. & Sharma, V.S. (1994) Kinetics of nitric oxide autooxidation in aqueous solution. J. Biol. Chem. 269, 5881-5883.
  • 46. Aisaka, K., Gross, S.S., Griffith, O.W. & Levi, R. (1989) L-Arginine availability determines the duration of acetylcholine-induced systemic vasodilation in vivo. Biochem. Biophys. Res. Commun. 163, 710-717.
  • 47. Stamler, J.S., Jaraki, O., Osborne, J.A., Simons, D.I., Vita, J., Singel, D., Valeri, C.R. & Localzo, J. (1992) Nitric oxide circulates in mammalian plasma primarily as an S-nitrosoadduct of serum albumin. Proc. Natl. Acad. Sci. U.S.A. 89, 7674-7677.
  • 48. Beckman, J.S. (1996) The physiological and pathological chemistry of nitric oxide; in Nitric Oxide. Principles and Actions (Lancaster, J.R. Jr. ed.) pp.1-82, Academic Press.
  • 49. Liu, X., Miller, M.J.S., Joshi, M.S., Thomas, D.D. & Lancaster, J.R., Jr. (1998) Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranes. Proc. Natl. Acad. Sci. U.S.A. 95, 2175-2179.
  • 50. Griffith, O.H., Dehlinger, P.J. & Van, S.P. (1974) Shape of the hydrophobic barrier of phospholipid bilayers (Evidence for water penetration in biological membranes). J. Membr. Biol. 15, 159-192.
  • 51. Windle, J.J. (1981) Hyperfine coupling constants for nitroxide spin probes in water and carbon tetrachloride. J. Magn. Reson. 45, 432-439.
  • 52. Johnson, M.E. (1981) Apparent hydrogen bonding by strongly immobilized spin-labels. Biochemistry 20, 3319-3328.
  • 53. Subczynski, W.K., Wisniewska, A., Yin, J.J., Hyde, J.S. & Kusumi, A. (1994) Hydrophobic barriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol. Biochemistry 33, 7670-7681.
  • 54. Wisniewska, A. & Subczynski, W.K. (1996) Spin label study on gramicidin-phosphatidylcholine interface: Fluidity, hydrophobicity and ion penetration. Curr. Top. Biophys. 20, 86-92.
  • 55. Deamer, D.W. & Bramhall, J. (1986) Permeability of lipid bilayers to water and ionic solutes. Chem. Phys. Lipids 40, 167-188.
  • 56. Chakrabarti, A.C. & Deamer, D.W. (1992) Permeability of lipid bilayers to amino acids and phosphate. Biochim. Biophys. Acta 1111, 171-177.
  • 57. Wisniewska, A. & Subczynski, W.K. (1999) Ion penetration as an indicator of changes in the hydrophobicity of lipid bilayer membranes: Spin-probe spin-label method. Curr. Top. Biophys. 23, 79-85.
  • 58. Overton, E. (1889) Über die allgemeinen osmotischen Eigenschaften der Zelle, ihre vermutlichen Ursachen und ihre Bedeutung für die Physiologie. Vierteljahrsschr. Naturforsch. Ges Zürich. 44, 88-135.
  • 59. Diamond, J.M. & Katz, Y. (1974) Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water. J. Membr. Biol. 17, 121-154.
  • 60. Lieb, W.R. & Stein, W.D. (1986) Non- Stokesian nature of transverse diffusion within human red cell membranes. J. Membr. Biol. 92, 111-119.
  • 61. Kusumi, A., Tsuda, M., Akino, T., Ohnishi, S. & Terayama, Y. (1983) Protein-phospholipid- cholesterol interaction in the photolysis of invertebrate rhodopsin. Biochemistry 22, 1165-1170.
  • 62. Edidin, M. (1990) Molecular associations and membrane domains. Curr. Top. Membr. Trans. 36, 81-93.
  • 63. Simons, K. & Ikonen, E. (1997) Functional rafts in membranes. Nature 387, 569-572.
  • 64. Mouritsen, O.G. & Andersen, O.S. (1998) In search of a new biomembrane model. Biol. Skr. Dan. Vid. Selsk. 49. (The Royal Danish Academy of Sciences and Letters, Copenhagen).
  • 65. Kusumi, A. & Sako, Y. (1996) Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8, 566-574.
  • 66. Edidin, M. (1997) Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7, 528-532.
  • 67. Hwang, J., Gheber, L.A., Margolis, L. & Edidin, M. (1998) Domains in cell plasma membranes investigated by near-field scanning optical microscopy. Biophys. J. 74, 2184-2190.
  • 68. Pasenkiewicz-Gierula, M., Subczynski, W.K. & Kusumi, A. (1991) Influence of phospholipid unsaturation on the cholesterol distribution in membranes. Biochimie 73, 1311-1316.
  • 69. Gaidarov, I., Santini, F., Warren, R.A. & Keen, J.H. (1998) Spatial control of coated-pit dynamics in living cells. Nature Cell Biology 1, 1-7.
  • 70. Adams, C. & Nelson, W.J. (1998) Cytomechanics of cell adhesion structures. Curr. Opin. Cell Biol. 7, 457-463.
  • 71. Davis, J.H., Clare, D.M., Hodges, R.S. & Bloom, M. (1983) Interaction of a synthetic amphiphilic polypeptide and lipids in a bilayer structure. Biochemistry 22, 5298-5305.
  • 72. Morrow, M.R., Huschilt, J.C. & Davis, J.H. (1985) Simultaneous modeling of phase and calorimetric behavior in an amphiphilic peptide/phospholipid model membrane. Biochemistry 24, 5396-5406.
  • 73. Klenk, H.D. & Choppin, P.W. (1970) Plasma membrane lipids and parainfluenza virus assembly. Virology 40, 939-947.
  • 74. Blough, H.A. & Merlie, J.P (1970) The lipids of incomplete influenza virus. Virology 40, 685- 692.
  • 75. Kanaseki, T., Kawasaki, K., Murata, M., Ikeuchi, Y. & Ohnishi, S. (1997) Structural features of membrane fusion between influenza virus and liposome as revealed by quick-freezing electron microscopy. J. Cell Biol. 137, 1041-1056.
  • 76. Wilson, I.A., Skehel, J.J. & Wiley, D.C. (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289, 366-378.
  • 77. Varghese, J.N., Laver, W.G. & Colman, P.M. (1983) Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303, 35-40.
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