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The Journal of Membrane Biology

, Volume 40, Issue 4, pp 293–314 | Cite as

Influence of membrane structure on ion transport through lipid bilayer membranes

  • R. Benz
  • B. F. Gisin
Article

Summary

Charge-pulse relaxation studies with the positively charged PV-K+ complex (cyclo-(d-Val-l-Pro-l-Val-d-Pro)3) and the negatively charged lipophilic ion dipicrylamine (DPA) have been performed in order to study the influence of structural properties on ion transport through lipid bilayer membranes. First, the thickness of monoolein membranes was varied over a wide range using differentn-alkanes and slovent-free membranes. The thickness (d) of the hydrocarbon core of these membranes varied between 4.9 and 2.5 nm. For both transport systems the partition coefficient β was found to be rather insensitive to variations ind. The same was valid for the translocation rate constantkMS of PV-K+, whereas a strong increase of the translocation rate constantki of DPA-with decreasingd was observed. In a further set of experimental conditions the structure of the lipids, such as number and position of the double bonds in the hydrocarbon chain and its chain length as well as the nature of the polar head group, was varied. The translocation constantkMS of PV-K+ transport was found to be much more sensitive to these variations thanki of DPA-.

Much larger variations inki andkMS were observed in membranes made from lipids with ether instead of ester linkages between glycerol backbone and hydrocarbon chain. The results are in qualitative agreement with the surface potentials of monolayers made from corresponding lipids. Increasing amounts of cholesterol in membranes of dioleoylphosphatidylcholine caused a strong decrease ofkMS (PV-K+), whereaski was found to be rather insensitive to this variation.

In monoolein membranes cholesterol causes a decrease ofkMS up to sixfold and a increase ofki up to eightfold. The partition coefficient β of DPA was insensitive to cholesterol, whereas β of PV-K+ was found to decrease about eightfold in these membranes. The influence of cholesterol onkMS is discussed on the basis of viscosity changes in the membrane and the change inki of DPA and β of PV-K+ on the basis of a possible change of the dipole potential of the membranes. The other sterols, epicholesterol and ergosterol cause no change in the kinetics of the two probes.

The different influence of membrane properties like thickness, viscosity, and dipole potential on the two transport systems is discussed under the assumption that the adsorption planes of the two probes have different positions in a membrane. Possibly because of a larger hydrophobic interaction, the adsorption plane of PV-K+ is located more towards the hydrocarbon side and that of DPA more towards the aqueous side of the dipole layer.

Keywords

Cholesterol Ergosterol Hydrocarbon Chain Lipid Bilayer Membrane 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.

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References

  1. 1.
    Anderson, O.S., Fuchs, M. 1975. Potential energy barriers to ion transport within lipid bilayers. Studies with tetraphenylborate.Biophys. J. 15:795Google Scholar
  2. 2.
    Benz, R., Cros, D. 1977. Influence of sterols on ion transport through lipid bilayer membranes.Biochim. Biophys. Acta 506:265Google Scholar
  3. 3.
    Benz, R., Fröhlich, O., Läuger, P. 1976. Influence of membrane structure on the kinetics of carrier-mediated ion transport through lipid bilayers.Biochim. Biophys. Acta 464:465Google Scholar
  4. 4.
    Benz, R., Fröhlich, O., Läuger, P., Montal, M. 1975. Electrical capacity of black lipid films and of lipid bilayers made from monolayers.Biochim. Biophys. Acta 394:323Google Scholar
  5. 5.
    Benz, R., Gisin, B.F., Ting-Beall, H.P., Tosteson, D.C., Läuger, P. 1976. Mechanism of ion transport through lipid bilayer membranes mediated by peptide cyclo-(d-Val-l-Pro-l-Val-d-Pro)3.Biochim. Biophys. Acta 455:665Google Scholar
  6. 6.
    Benz, R., Janko, K. 1976. Voltage-induced capacitance relaxation of lipid bilayer membrane. Effect of membrane composition.Biochim. Biophys. Acta 455:721Google Scholar
  7. 7.
    Benz, R., Läuger, P. 1976. Kinetic analysis of carrier-mediated ion transport by the charge-pulse technique.J. Membrane Biol. 27:171Google Scholar
  8. 8.
    Benz, R., Läuger, P. 1977. Transport kinetics of dipicrylamine through lipid bilayer membranes. Effects of membrane structure.Biochim. Biophys. Acta 468:245Google Scholar
  9. 9.
    Benz, R., Läuger, P., Janko, K. 1976. Transport kinetics of hydrophobic ions in lipid bilayer membranes. Charge pulse relaxation studies.Biochim. Biophys. Acta 455:701Google Scholar
  10. 10.
    Benz, R., Stark, G. 1975. Kinetics of macrotetrolide-induced ion transport across lipid bilayer membranes.Biochim. Biophys. Acta 282:27Google Scholar
  11. 11.
    Benz, R., Stark, G., Janko, K., Läuger, P. 1973. Valinomycin-mediated ion transport through neutral lipid membranes: Influence of hydrocarbon chain length and temperature.J. Membrane Biol. 14:339Google Scholar
  12. 12.
    Bruner, L.J. 1975. The interaction of hydrophobic ions with lipid bilayer membranes.J. Membrane Biol. 22:125Google Scholar
  13. 13.
    Bunce, A.S., Hider, R.C. 1974. The composition of black lipid membranes formed from egg-yolk lecithin, cholesterol andn-decane.Biochim. Biophys. Acta 363:423Google Scholar
  14. 14.
    Davis, D.G., Gisin, B.F., Tosteson, D.C. 1976. Conformational studies of peptide cyclo-(d-Val-d-pro-l-Val-d-Pro)3, a cation-binding analogue of valinomycin.Biochemistry 15:768Google Scholar
  15. 15.
    Demel, R.A., Bruckdorfer, K.R., von Deenen, L.L.M. 1972. The effect of sterol structure on the permeability of liposomes to glucose, glycerol and Rb+.Biochim. Biophys. Acta 255:321Google Scholar
  16. 16.
    Demel, R.A., Kruyff, B. de 1976. The influence of sterols in membranes.Biochim. Biophys. Acta 457:109Google Scholar
  17. 17.
    Gaboriaud, R. 1966. Sur le comportement des acides non chargés dans les milieux eauméthanol.C. R. Acad. Sci. Ser. C. 263:911Google Scholar
  18. 18.
    Gisin, B.F., Merrifield, R.B. 1972. Synthesis of a hydrophobic potassium binding peptide.J. Am. Chem. Soc. 94:6165Google Scholar
  19. 19.
    Hanai, T., Haydon, D.A., Taylor, J. 1965. The influence of lipid composition and of some adsorbed proteins on the capacitance of black hydrocarbon membranes.J. Theor. Biol. 9:422Google Scholar
  20. 20.
    Haydon, D.A. 1975. Functions of the lipid in bilayer ion permeability.Ann. New York Acad. Sci. 264:2Google Scholar
  21. 21.
    Haydon, D.A., Hladky, S.B. 1972. Ion transport across thin lipid membranes: A critical discussion of mechanisms in selected systems.Q. Rev. Biophys. 5:187Google Scholar
  22. 22.
    Haydon, D.A., Myers, V.B. 1973. Surface charge, surface dipoles and membrane conductance.Biochim. Biophys. Acta 307:429Google Scholar
  23. 23.
    Hladky, S.B. 1975. Tests of the carrier model for ion transport by nonactin and trinactin.Biochim. Biophys. Acta 375:327Google Scholar
  24. 24.
    Hladky, S.B., Haydon, D.A. 1972. Ion transfer across lipid membranes with presence of Gramicidin A: I. Studies of the unit conductance channel.Biochim. Biophys. Acta 274:294Google Scholar
  25. 25.
    Hladky, S.B., Haydon, D.A. 1973. Membrane conductance and surface potential.Biochim. Biophys. Acta 318:464Google Scholar
  26. 26.
    Janko, K., Benz, R. 1977. Properties of lipid bilayer membranes made from lipids containing phytanic acid.Biochim. Biophys. Acta 470:8Google Scholar
  27. 27.
    Ketterer, B., Neumcke, B., Läuger, P. 1971. Transport mechanism of hydrophobic ions through lipid bilayer membranes.J. Membrane Biol. 5:225Google Scholar
  28. 28.
    Knoll, W., Stark, G. 1975. An extended kinetic analysis of valinomycin-induced Rb-transport through monoglyceride membranes.J. Membrane Biol. 25:249Google Scholar
  29. 29.
    Laprade, R., Ciani, S.M., Eisenman, G., Szabo, G. 1975. The kinetics of carrier-mediated ion permeation.In: Membranes. A Series of Advances. G. Eisenman, editor. Vol. 3, p. 127. Marcel Dekker, New YorkGoogle Scholar
  30. 30.
    McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces.In: Curr. Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. p. 71. Academic Press, New YorkGoogle Scholar
  31. 31.
    Melnik, E., Latorre, R., Hall, J.E., Tosteson, D.C. 1977. Phloretin-induced changes in ion transport across lipid bilayer membranes.J. Gen. Physiol. 69:243Google Scholar
  32. 32.
    Pagano, R.E., Ruysschaert, J.M., Miller, J.R. 1972. The molecular composition of some lipid bilayer membranes in aqueous solution.J. Membrane Biol. 10:11Google Scholar
  33. 33.
    Paltauf, F., Hauser, H., Philips, M.C. 1971. Monolayer characteristics of some 1,2-diacyl, 1-alkyl-2-acyl and 1,2-dialkyl phospholipids at the airwater interfaces.Biochim. Biophys. Acta 249:539Google Scholar
  34. 34.
    Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: Solutions of four relevant electrostatic problems.Nature (London) 221:844Google Scholar
  35. 35.
    Sanders, H. 1967. Preparative isolation of phosphatidyl serine from brain.Biochim. Biophys. Acta 144:485Google Scholar
  36. 36.
    Singleton, W.S., Gray, M.S., Brown, M.L., White, J.L. 1965. Chromatographically homogeneous lecithin from egg phospholipids.J. Am. Oil Chem. Soc. 42:53Google Scholar
  37. 37.
    Stark, G., Ketterer, B., Benz, R., Läuger, P. 1971. The rate constants of valinomycinmediated ion transport through thin lipid bilayer membranes.Biophys. J. 11:981Google Scholar
  38. 38.
    Szabo, G. 1974. Dual mechanism for the action of cholesterol on membrane permeability.Nature (London) 257:47Google Scholar
  39. 39.
    Szabo, G. 1976. The influence of dipole potentials on the magnitude and the kinetics of ion transport in lipid bilayer membranes.In: Extreme Environment: Mechanisms of Microbiol Adaptation. M.R. Heinrich, editor. p. 321. Academic Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1978

Authors and Affiliations

  • R. Benz
    • 1
  • B. F. Gisin
    • 1
  1. 1.Fachbereich BiologieUniversität KonstanzKonstanzGermany

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