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Relationship between fluidity and ionic permeability of bilayers from natural mixtures of phospholipids

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Summary

Proton and calcium permeability coefficients of large unilamellar vesicles made from natural complex mixtures of phospholipids were measured in various conditions and related to membrane fluidity. Permeability coefficients at neutral pH and 25°C were in the range of 104 cm sec1 and 2.5×1011 cm sec1 for protons and calcium, respectively. With the exception of two cases. (H+)>104 m and (Ca2+)>103 m, fluidity increases correspond to permeability increases. Theoretical analysis shows that, for both ions, the measured values of permeability coefficients imply that the permeation process is controlled by the productD 1 D 2 of the diffusion coefficient from the medium into the membrane (D 1) by the diffusion coefficient in the membrane (D 2). Further analysis ofD 1 values deduced from combined use of permeability and fluidity data shows that the solubilization should occur in a medium of dielectric constant of about 12, suggesting the involvement of the hydration water of membranes. High proton concentrations, although having virtually no effect on fluidity, trigger the appearance of (i) lateral heterogeneity in membranes, as seen by31P NMR, and (ii) large permeability increases. It is proposed that the main effect of fluidity and/or lateral heterogeneity on permeability may bevia the membrane hydration control. We conclude that the current assumption that permeability is controlled by fluidity should be regarded with caution, at least in the case of ions and natural mixtures of phospholipids.

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References

  • Albert, A.D., Sen, A., Yeagle, P.L. 1984. The effect of calcium on the bilayer stability of lipids from bovine rod outer disk membranes.Biochim. Biophys. Acta 771:28–34

    Google Scholar 

  • Asheroft, R.G., Coster, H.G.L., Smith, J.R. 1981. The molecular organisation of bimolecular lipid membranes. The dielectric structure of hydrophilic/hydrophobic interface.Biochim. Biophys. Acta 643:191–204

    Google Scholar 

  • Azumi, T., Mc Glynn, S.P. 1962. Polarization of the luminescence of phenanthrene.J. Chem. Phys. 37:2413–2420

    Google Scholar 

  • Bergelson, L.D. 1980. Lipid Biochemical Preparations. pp. 187–204. Elsevier, Amsterdam

    Google Scholar 

  • Blok, M.C., Van Der Neut-Kok, E.C.M., Van Deenen, L.L.M., De Gier, J. 1975. The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes.Biochim. Biophys. Acta 406:187–196

    Google Scholar 

  • Blume, A. 1983. Apparent molar heat capacities of phospholipids in aqueous dispersion. Effect of chain length and head group structure.Biochemistry 22:5436–5442

    Google Scholar 

  • Carruthers, A., Melchior, D.L. 1983. Studies on the relationship between water permeability and bilayer physical state.Biochemistry 22:5797–5807

    Google Scholar 

  • Deamer, D., Bangham, A.D. 1976. Large volume liposomes by an ether vaporization method.Biochim. Biophys. Acta 443:629–634

    Google Scholar 

  • Deamer, D., Nichols, J.W. 1983. Proton-hydroxyde permeability of liposomes.Proc. Natl. Acad. Sci. USA 80:165–168

    Google Scholar 

  • Farren, S.B., Hope, M.J., Cullis, P.R. 1983. Polymorphic phase preference of phosphatidic acid: A31P and2H NMR study.Biochem. Biophys. Res. Commun. 111:675–682

    Google Scholar 

  • Gerritsen, W.J., De Kruijff, B., Verkleij, A.J., De Gier, J., Van Deenen, L.L.M. 1980. Ca2+-induced isotropic motion and phosphatidylcholine flip-flop in phosphatidylcholine-cardiolipin bilayers.Biochim. Biophys. Acta 598:554–560

    Google Scholar 

  • Ghorbal, M.H., Salsac, L., Grignon, C. 1978. Action du calcium sur l'exorption du potassium en milieu acide par des racines excisées de plantes calcicoles ou calcifuges.Physiol. Vég. 16:491–503

    Google Scholar 

  • Gibrat, R., Grignon, C. 1982. Effect of pH on the surface charge density of plant membranes. Comparison of microsomes and liposomes.Biochim. Biophys. Acta 692:462–468

    Google Scholar 

  • Gounaris, K., Sen, A., Brain, A.P.R., Quinn, P.J., Williams, P. 1983. The formation of non-bilayer structures in total polar lipid extracts of chloroplast membranes.Biochim. Biophys. Acta 728:129–139

    Google Scholar 

  • Gutknecht, J. 1984. Proton/hydroxyde conductance through lipid bilayer membranes.J. Membrane Biol. 82:105–112

    Google Scholar 

  • Heyn, M.P. 1979. Determination of lipid order parameters and rotational correlation times from fluorescence depolarization experiments.FEBS Lett. 108:359–364

    Google Scholar 

  • Hope, M.J., Culis, P.R. 1980. Effects of divalent cations and pH on phosphatidylserine model membranes: A31P NMR study.Biochem. Biophys. Res. Commun. 92:846–852

    Google Scholar 

  • Hyono, A., Hendriks, Th., Daemen, F.J.M., Bonting, S.L. 1975. Movement of calcium through artificial lipid membranes and the effects of ionophores.Biochim. Biophys. Acta 389:34–46

    Google Scholar 

  • Jähnig, F. 1979. Structural order of lipids and proteins in membranes: Evaluation of fluorescence anisotropy data.Proc. Natl. Acad. Sci. USA 76:6361–6365

    Google Scholar 

  • Kates, M. 1972. Techniques of lipidology.In: Laboratory Techniques in Biochemistry and Molecular Biology. T.S. Work and E. Work, editors. pp. 354–392. North-Holland/American Elsevier, Amsterdam and New York

    Google Scholar 

  • Nichols, J.W., Deamer, D.W. 1980. Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acidbase titration technique.Proc. Natl. Acad. Sci. USA 77:2038–2042

    Google Scholar 

  • Nichols, J.W., Hill, M.W., Bangham, A.D., Deamer, D.W. 1980. Measurement of the net proton-hydroxyl permeability of large unilamellar liposomes with the fluorescent probe 9-aminoacridine.Biochim. Biophys. Acta 596:393–403

    Google Scholar 

  • Noordam, P.C., Van Echteld, C.J.A., De Kruijff, B., Verkleij, A.J., De Gier, J. 1980. Barrier characteristics of membrane model systems containing unsaturated phosphatidylethanolamines.Chem. Phys. Lipids 27:221–232

    Google Scholar 

  • Papahadjopoulos, D., Jacobson, K., Nir, S., Isaac, T. 1973. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol.Biochim. Biophys. Acta 311:330–348

    Google Scholar 

  • Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: Solutions to four relevant electrostatic problems.Nature (London) 221:844–846

    Google Scholar 

  • Pottel, H., Van Der Meer, W., Herreman, W. 1983. Correlation between the order parameter and the steady-state fluorescence anisotropy of 1,6-diphenyl-1,3,5-hexatriene and an evaluation of membrane fluidity.Biochim. Biophys. Acta 730:181–186

    Google Scholar 

  • Rojas, E. 1981. Ion permeability.In: Membrane Transport S.L. Bonting and J.J.H.H.M. de Pont, editors. pp. 61–106. Elsevier/North-Holland Biomedical, Amsterdam

    Google Scholar 

  • Rossignol, M. 1984. Relations entre la structure et la perméabilité des membranes phospholipidiques: Effets du calcium et des protons sur les phospholipides de racines. Ph.D. Thesis, Montpellier. p. 270.

  • Rossignol, M., Grignon, N., Grignon, C. 1982b. Effect of temperature and ions on the microviscosity of bilayers from natural phospholipid mixtures.Biochimie 64:263–270

    Google Scholar 

  • Rossignol, M., Thomas, P., Grignon, C. 1982a. Proton permeability of liposomes from natural phospholipid mixtures.Biochim. Biophys. Acta 684:195–199

    Google Scholar 

  • Seddon, J.M., Cevc, G., Marsh, D. 1983a. Calorimetric studies of the gel (Lβ-Lα) and lamellar-inverted hexagonal (Lα-H11) phase transitions in dialkyl- and diacylphosphatidylethanolamines.Biochemistry 22:1280–1289

    Google Scholar 

  • Seddon, J.M., Kaye, R.D., Marsh, D. 1983b. Induction of the lamellar-inverted hexagonal phase transition in cardiolipin by protons and monovalent cations.Biochim. Biophys. Acta 734:347–352

    Google Scholar 

  • Shinitzky, M., Barenholz, Y. 1974. Dynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing dicetylphosphate.J. Biol. Chem. 249:2652–2657

    Google Scholar 

  • Shinitzky, M., Barenholz, Y. 1978. Fluidity parameters of lipid region determined by fluorescence polarization.Biochim. Biophys. Acta 515:367–394

    Google Scholar 

  • Shinitzky, M., Yuli, I. 1982. Lipid fluidity at the submacroscopic level: Determination by fluorescence polarization.Chem. Phys. Lipids 30:261–282

    Google Scholar 

  • Simon, S.A., McIntosh, T., Latorre, R. 1982. Influence of cholesterol on water penetration into bilayers.Science 216:65–67

    Google Scholar 

  • Szoka, F., Jr., Papahadjopoulos, D. 1978. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation.Proc. Natl. Acad. Sci. USA 75:4194–4198

    Google Scholar 

  • Van Blitterswijk, W.J., Van Hoeven, R.P., Van Der Meer, B.W. 1981. Lipid structural order parameters (reciprocal of fluidity) in biomembranes derived from steady-state fluorescence polarization measurements.Biochim. Biophys. Acta 644:323–332

    Google Scholar 

  • Vanderkooi, J.M., Martonosi, A. 1971. Sarcoplasmic reticulum. XVI. The permeability of phosphatidyl choline vesicles for calcium.Arch. Biochem. Biophys. 147:632–646

    Google Scholar 

  • Van Venetie, R., Verkleij, A.J. 1981. Analysis of the hexagonal II phase and its relations to lipidic particles and the lamellar phase. A freeze-fracture study.Biochim. Biophys. Acta 645:262–269

    Google Scholar 

  • Verkleij, A.J., De Gier, J. 1981. Freeze fracture studies on aqueous dispersions of membrane lipids.In: Liposomes: From Physical Structure to Therapeutic Applications. C.G. Knight, editor. pp. 83–103. Elsevier/North-Holland Biomedical, Amsterdam

    Google Scholar 

  • Zwolinsky, B.J., Eyring, H., Reese, C.E. 1949. Diffusion and membrane permeability.J. Phys. Coll. Chem. 53:1426–1453

    Google Scholar 

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Rossignol, M., Uso, T. & Thomas, P. Relationship between fluidity and ionic permeability of bilayers from natural mixtures of phospholipids. J. Membrain Biol. 87, 269–275 (1985). https://doi.org/10.1007/BF01871227

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  • DOI: https://doi.org/10.1007/BF01871227

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