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Reversible electrical breakdown of lipid bilayer membranes: A charge-pulse relaxation study

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Summary

Charge-pulse experiments were performed with lipid bilayer membranes from oxidized cholesterol/n-decane at relatively high voltages (several hundred mV). The membranes show an irreversible mechanical rupture if the membrane is charged to voltages on the order of 300 mV. In the case of the mechanical rupture, the voltage across the membrane needs about 50–200 μsec to decay completely to zero. At much higher voltages, applied to the membrane by charge pulses of about 500 nsec duration, a decrease of the specific resistance of the membranes by nine orders of magnitude is observed (from 108 to 0.1 Ω cm2), which is correlated with the reversible electrical breakdown of the lipid bilayer membrane. Due to the high conductance increase (breakdown) of the bilayer it is not possible to charge the membrane to a larger value than the critical potential differenceV c. For 1m alkali ion chloridesV c was about 1 V. The temperature dependence of the electrical breakdown voltageV c is comparable to that being observed with cell membranes.V c decreases between 2 and 48°C from 1.5 to 0.6 V in the presence of 1m KCl.

Breakdown experiments were also performed with lipid bilayer membranes composed of other lipids. The fast decay of the voltage (current) in the 100-nsec range after application of a charge pulse was very similar in these experiments compared with experiments with membranes made from oxidized cholesterol. However, the membranes made from other lipids show a mechanical breakdown after the electrical breakdown, whereas with one single membrane from oxidized cholesterol more than twenty reproducible breakdown experiments could be repeated without a visible disturbance of the membrane stability.

The reversible electrical breakdown of the membrane is discussed in terms of both compression of the membrane (electromechanical model) and ion movement through the membrane induced by high electric field strength (Born energy).

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References

  1. Alvarez, O., Latorre, R. 1978. Voltage-dependent capacitance in lipid bilayers made from monolayers.Biophys. J. 21:1

    Google Scholar 

  2. Apell, H.-J., Bamberg, E., Alpes, H., Läuger, P. 1977. Formation of ion channels by a negatively charged analog of gramicidin A.J. Membrane Biol. 31:171

    Google Scholar 

  3. 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 394:323

    Google Scholar 

  4. 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 464:465

    Google Scholar 

  5. Benz, R., Gisin, B.F. 1978. Influence of membrane structure on ion transport through lipid bilayer membranes.J. Membrane Biol. 40:293

    Google Scholar 

  6. Benz, R., Janko, K. 1976. Voltage-induced capacitance relaxation of lipid bilayer membranes. Effect of membrane composition.Biochim. Biophys. Acta 455:721

    Google Scholar 

  7. Benz, R., Läuger, P. 1976. Kinetic analysis of carrier-mediated ion transport by the charge-pulse technique.J. Membrane Biol. 27:171

    Google Scholar 

  8. Benz, R., Läuger, P., Janko, K. 1976. Transport kinetics of hydrophobic ions in lipid bilayer membranes. Charge pulse relaxation studies.Biochim. Biophys. Acta 455:701

    Google Scholar 

  9. 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. 14:339

    Google Scholar 

  10. Boheim, G., Benz, R. 1978. Charge-pulse relaxation studies with lipid bilayer membranes modified by alamethicin.Biochim. Biophys. Acta 507:262

    Google Scholar 

  11. Coster, H.G.L., Zimmermann, U. 1975. The mechanism of electrical breakdown in the membranes ofValonia utricularis.J. Membrane Biol. 22:73

    Google Scholar 

  12. Coster, H.G.L., Zimmermann, U. 1975. Dielectric breakdown in the membranes ofValonia utricularis. The role of energy dissipation.Biochim. Biophys. Acta 382:410

    Google Scholar 

  13. Crowley, J.M. 1973. Electrical breakdown of bimolecular lipid membranes as an electromechanical instability.Biophys. J. 13:711

    Google Scholar 

  14. Feldberg, S.W., Kissel, G. 1975. Charge pulse studies of transport phenomena in bilayer membranes. I. Steady-state measurements of actin- and valinomycin-mediated transport in glycerol monooleate bilayers.J. Membrane Biol. 20:269

    Google Scholar 

  15. Feldberg, S.W., Nakadomari, H. 1977. Charge pulse studies of transport phenomena in bilayer membranes. II. Detailed theory of steady-state behavior and application to valinomycin-mediated potassium transport.J. Membrane Biol. 31:81

    Google Scholar 

  16. Haydon, D.A. 1970. A critique of the black film as a membrane model.In: Permeability and Function of Biological Membranes. L. Balis, A. Katchalsky, R.D. Keynes, W.R. Loewenstein, and B.A. Pethica, editors. p. 185. North-Holland, Amsterdam

    Google Scholar 

  17. Hodgkin, A.L., Huxley, A.F. 1952. Currents carried by sodium and potassium ions through the membrane of the giant axon ofLoligo.J. Physiol. (London) 116:449

    Google Scholar 

  18. Janko, K., Benz, R. 1977. Properties of lipid bilayer membranes made from lipids containing phytanic acid.Biochim. Biophys. Acta 470:8

    Google Scholar 

  19. Montal, M., Mueller, P. 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties.Proc. Nat. Acad. Sci. USA 69:3561

    Google Scholar 

  20. Neumcke, B., Walz, D., Läuger, P. 1970. Non linear effects in lipid bilayer membranes. III. The dissociation field effect.Biophys. J. 10:172

    Google Scholar 

  21. Onsager, L. 1934. Deviations from Ohm's law in week electrolyts.J. Chem. Phys. 2:599

    Google Scholar 

  22. Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane. Solution to four relevant electro-static problems.Nature (London) 221:844

    Google Scholar 

  23. Pilwat, G., Zimmermann, U., Riemann, F. 1975. Dielectric breakdown measurements of human and bovine erythrocyte membranes using benzyl-alcohol as a probe molecule.Biochim. Biophys. Acta 406:424

    Google Scholar 

  24. Requena, J., Haydon, D.A., Hladky, S.B. 1975. Lenses and the compression of black lipid membranes by an electric field.Biophys. J. 15:77

    Google Scholar 

  25. Riemann, F., Zimmermann, U., Pilwat, G. 1975. Release and uptake of haemoglobin and ions in red blood cells induced by dielectric breakdown.Biochim. Biophys. Acta 394:449

    Google Scholar 

  26. Singleton, W.S., Gray, M.S., Brown, M.L., White, J.L. 1965. Chromatographically homogeneous lecithin from egg phospholipid.J. Am. Oil Chem. Soc. 42:53

    Google Scholar 

  27. Tien, H.T., Carbone, S., Dawidowicz, E.A. 1966. Formation of “black” lipid membranes by oxydation products of cholesterol.Nature (London) 212:718

    Google Scholar 

  28. Vienken, J., Jeltsch, E., Zimmermann, U. 1978. Penetration and entrapment of large particles in erythrocytes by electrical breakdown techniques.Cytobiology.17:182

    Google Scholar 

  29. White, S.H. 1970. Thickness changes in lipid bilayer membranes.Biochim. Biophys. Acta 196:354

    Google Scholar 

  30. White, S.H. 1972. Analysis of the torus surrounding planar lipid bilayer membranes.Biophys. J. 12:432

    Google Scholar 

  31. White, S.H. 1974. Comments on “Electrical breakdown of bimolecular lipid membranes as an electromechanical instability”.Biophys. J. 14:155

    Google Scholar 

  32. Zimmermann, U. 1973. Transportprozesse durch Biomembranen. Jahresbericht der Kernforschungsanlage, Jülich GmbH

  33. Zimmermann, U. 1977. Organspezifische Applikation von Pharmaka über zelluläre Trägersysteme.Chem. Labor Betr. 28:505

    Google Scholar 

  34. Zimmermann, U. 1977. Cell turgor pressure regulation and turgor pressure-mediated transport processes.In: Integration of Activity in the Higher Plannt. D. Jennings, editor. p. 117. University Press, Cambridge

    Google Scholar 

  35. Zimmermann, U., Beckers, F., Coster, H.G.L. 1977. The effect of pressure on the electrical breakdown in the membranes ofValonia utricularis.Biochim. Biophys. Acta 464:399

    Google Scholar 

  36. Zimmermann, U., Beckers, F., Steudle, E. 1977. Turgor sensing in plant cells by the electromechanical properties of the membrane.In: Transmembrane Ionic Exchanges in Plants. M. Thellier, A. Monnier, M. Demarty, and J. Dainty, editors. No. 258, p. 155. C.N.R.S., Paris

    Google Scholar 

  37. Zimmermann, U., Pilwat, G. 1976. Organspezifische Applikation von pharmazeutisch aktiven Substanzen über zelluläre Trägersysteme.Z. Naturforsch. 31c:732

    Google Scholar 

  38. Zimmermann, U., Pilwat, G., Beckers, F., Riemann, F. 1976. Effects of external electrical fields on cell membranes.Bioelectrochem. Bioenerg. 3:58.

    Google Scholar 

  39. Zimmermann, U., Pilwat, G., Esser, B. 1978. The effect on encapsulation in red blood cells on the distribution of methotrexate in mice.J. Clin. Chem. Clin. Biochem. 16:135

    Google Scholar 

  40. Zimmermann, U., Pilwat, G., Holzapfel, C., Rosenheck, K. 1976. Electrical hemolysis of human and bovine red blood cells.J. Membrane Biol. 30:135

    Google Scholar 

  41. Zimmermann, U., Pilwat, G., Riemann, F. 1974. Dielectric breakdown in cell membranes.In: Membrane Transport in Plants. U. Zimmermann and J. Dainty, editors. p. 146. Springer-Verlag, Berlin-Heidelberg-New York

    Google Scholar 

  42. Zimmermann, U., Pilwat, G., Riemann, F. 1974. Dielectric breakdown in cell membranes.Biophys. J. 14:881

    Google Scholar 

  43. Zimmermann, U., Pilwat, G., Riemann, F. 1975. Preparation of erythrocyte ghosts by dielectric breakdown of the cell membrane.Biochim. Biophys. Acta 375:209

    Google Scholar 

  44. Zimmermann, U., Riemann, F., Pilwat, G. 1976. Enzyme loading of electrically homogeneous human red blood cell ghosts prepared by dielectric breakdown.Biochim. Biophys. Acta 436:460

    Google Scholar 

  45. Zimmermann, U., Schulz, J., Pilwat, G. 1973. Transcellular ion flow inE. coli B and electrical sizing of bacteria.Biophys. J. 13:1005

    Google Scholar 

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Benz, R., Beckers, F. & Zimmermann, U. Reversible electrical breakdown of lipid bilayer membranes: A charge-pulse relaxation study. J. Membrain Biol. 48, 181–204 (1979). https://doi.org/10.1007/BF01872858

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  • DOI: https://doi.org/10.1007/BF01872858

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