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Correlations between changes in membrane capacitance induced by changes in ionic environment and the conductance of channels incorporated into bilayer lipid membranes

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Abstract

The action of metal polycations and pH on ionic channels produced in bilayer lipid membranes (BLM) by three different toxins was studied by measuring membrane capacitance and channel conductance. Here, we show that critical concentrations of Cd2+, La3+ or Tb3+ induce complex changes in membrane capacitance. The time course of capacitance changes is similar to the time course of channel blocking by these ions at low concentration. No changes in BLM capacitance or conductance were observed in the range of pH 5.8–9.0. A pH shift from 7.4 to 3–4 or 11–12 induced large changes in BLM capacitance and channel conductance. For all studied channel-forming proteins, the initial capacitance increase preceded the conductance decrease caused by addition of polycations or by a change in pH. A close relationship between membrane lipid packing and ion channel protein is suggested.

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References

  • Almers, W., McCleskey, E.W. 1984. Ion selective conductance in calcium channels of frog muscle: calcium selectivity in a single fill pore. J. Physiol. 353:585–609

    Google Scholar 

  • Cai, M., Jordan, P.S. 1990. How does vestibule charge affect ion conduction and toxin binding in sodium channel? Biophys. J. 57:883–891

    Google Scholar 

  • Chanturiya, A.N. 1990. Detection of transient capacitance increase associated with channel formation in lipid bilayers. Biochim. Biophys. Acta 1026:248–250

    Google Scholar 

  • Chanturiya, A.N., Sokolov, Yu.V., Grebinozko, E.I., Nikolaenko, A.N., Ivanov, A.P., Lishko, V.K. 1985. Temperature dependences of α-latrotoxin interaction with bilayer lipid membranes. Doklady Acad. Sci. USSR 9:82–85 (in Russian)

    Google Scholar 

  • Chizmadziew, Yu.A., Abidor, I.G., Glazunow, I.Yu. 1985. Studies of electromechanical properties of membranes by the potentiodynamic method. Biol. membrany 2:906–918 (in Russian)

    Google Scholar 

  • Epand, R.M., Epand, R.F., Leon, B.T., Menger, F.M., Kuo, J.F. 1991. Evidence for the regulation of the activity of protein kinase C through changes in membrane properties. Biosci. Rep. 11:59–64.

    Google Scholar 

  • Evzen, A., Teising, J., Svoboda, P. 1987. Mg2+ induced changes of lipid order and conformation of (Na-K)ATP-ase. Biochim. Biophys. Acta 905:376–382

    Google Scholar 

  • Gambal, F., Menini, A., Rauch, G. 1987. Effect of calcium on the gramicidin A single channel in phospholipid membranes. Eur. Biophys. J. 14:369–374

    Google Scholar 

  • Grant, E.J., Beeler, T.J., Taylor, K.M.P., Gable, K., Rosenman, M.A. 1992. Mechanism of Maganin 2a induced permeabilization of phospholipid vesicles. Biochemistry 31:9912–9918

    Google Scholar 

  • Jacobson, K., Papahajopoulos, D. 1975. Phase transition and phase separation in phospholipid membranes induced by changes in temperature, pH and concentration of bivalent cations. Biochemistry 14:152–161

    Google Scholar 

  • Knoll, W., Appel, H-J., Eibl, H., Miller, A. 1986. Direct evidence for Ca2+ induced lateral phase separation in black membranes of lipid mixture by the analysis of gramicidin A single channels. Eur. Biophys. J. 13:187–193

    Google Scholar 

  • Kryshtal, O.A. 1976. Blocking action of cadmium ions on calcium inward current in the membrane of nerve cell. Doklady Acad. Sci. USSR 231:322–331 (in Russian)

    Google Scholar 

  • Laüger, P., Stephan, W., Frehland, E. 1980. Fluctuation of barrier structure of ionic channels. Biochim. Biophys. Acta 602:167–180

    Google Scholar 

  • Massari, S., Folena, E., Ambrosin, V., Schiavo, G., Colonna, R. 1991. pH dependent lipid packing, membrane permeability and fusion in phosphatydylcholine vesicles. Biochim. Biophys. Acta 1067: 131–138

    Google Scholar 

  • McLaughlin, A., Grathwohl, C., McLaughlin, S. 1987. The absorption of divalent cations to phospholipid bilayer membranes. Biochim. Biophys. Acta 513:338–357

    Google Scholar 

  • McLaughlin, S., Mulrine, N., Cresalfi, T., Vaio, G., McLaughlin, A. 1981. Adsorption of divalent cations to bilayer membranes containing phosphatydylserine. J. Gen. Physiol. 77:445–473

    Google Scholar 

  • McLaughlin, S.G.A., Szabo, G., Eisenman, G. 1971. Divalent ions and the surface potential of charged phospholipid membranes. J. Gen. Physiol. 58:667–687

    Google Scholar 

  • Menestrina, G. 1986. Ionic channels formed by Staphylococcus aureus alpha toxin. J. Membrane Biol. 90:177–190

    Google Scholar 

  • Mironov, S.L., Sokolov, Yu.V., Chanturiya, A.N., Lishko, V.K. 1986. Channels produced by spider venoms in bilayer lipid membranes: mechanism of ion transport and toxic action. Biochim. Biophys. Acta 862:185–198

    Google Scholar 

  • Misley, N.P., Lin, H.Y., Verkman, A.S. 1987. Lipid domain structure correlated with membrane protein function in placental microvillous vesicles. Biophys. J. 51:172a

    Google Scholar 

  • Mueller, P., Rudin, D.O., Tien, T., Westcott, W.C. 1962. Reconstitution of cell membrane in vitro and its transformation into excitable system. Nature 194:979–980

    Google Scholar 

  • Mueller, R., Finkelstein, A. 1972. The effect of surface charge on the voltage-dependent conductance induced in thin lipid membranes by monoazomycin. J. Gen. Physiol. 60:285–306

    Google Scholar 

  • Nathan, R.D., Kanal, K., Clark, R.B., Giles, W. 1988. Selective block of calcium channels by lanthanum in single bullfrog atrial cells. J. Gen. Physiol. 91:549–572

    Google Scholar 

  • Ohki, S., Duax, J. 1986. Effects of cations and polycations on the aggregation and fusion of phosphatidylserine membranes. Biochim. Biophys. Acta 861:177–186

    Google Scholar 

  • Omelchenko, A.M., Browykin, B.A. 1988. The possibility of the existence of carbon hydrogen solvent between layers of BLM. Biofizika 23:456–459 (in Russian)

    Google Scholar 

  • Osipov, V.V., Rostovtseva, T.K., Lev, A.A. 1987. Current voltage characteristics of the single gramicidin A channels in glyceryl monoleate bilayers under asymmetrical and symmetrical ANS-adsorption. In: Internat. Symp. Membrane Lipids—Metabolism and Organisation. Varna, 30

    Google Scholar 

  • Papahadjopulos, D., Vail, W.J., Newton, C. 1977. Studies of membrane fusion. III. The role of calcium induced phase separation. Biochim. Biophys. Acta 465:579–598

    Google Scholar 

  • Robello, M., Rolandi, R., Alema, S., Grasso, A. 1984. Trans-bilayer orientation and voltage dependence of α-latrotoxin induced channels. Proc. R. Soc. (London) 220:477–487

    Google Scholar 

  • Rudnev, V.S., Likhatskaya, G.N., Kozlovskaya, E.P., Monasturnaya, M.M., Elyakov, G.B. 1984. Influence of sea anemone Radianthus macrodactylus hemolysin on the conductance of lipid membranes. Biol. Membr. 1:1019–1024 (in Russian)

    Google Scholar 

  • Salikhov, Sh.I., Tashmukhamedov, M.S., Adulbekov, M.T. 1982. Purification and structure of neurotoxin from the venom of Latrodectus tredecimguttatus spider. Doklady Acad. Sci. USSR 262:485–488 (in Russian)

    Google Scholar 

  • Smith, A.D., Stubbs, C.D. 1987. Modulation of membrane protein function by bilayer lipids. Basic Res. Cardiol. 82:93–97

    Google Scholar 

  • Sokolov, Y.V., Chanturiya, A.N., Lishko, V.K. 1987. Latrotoxin-induced fusion of liposomes with bilayer phospholipid membranes. Biochim. Biophys. Acta 900:295–299

    Google Scholar 

  • Teslenko, V.I. 1985. Current-dependent blockage of membrane channels. Studio Biophysica 106:89–110

    Google Scholar 

  • Van Dijck, P.V.M., De Ckruijf, B., Verkleij, A.J., Van Deenen, L.L.M., De Gier, J. 1978. Comparative studies on the effect of pH and Ca2+ on bilayers of various negatively charged phospholipids and their mixtures with phosphatydylcholine. Biochim. Biophys. Acta 512:84–96

    Google Scholar 

  • Westman, J., Eriksson, L.E.G. 1979. The interaction of various lanthanide ions and some anions with phosphatidylcholine vesicle membranes. Biochim. Biophys. Acta 557:62–78

    Google Scholar 

  • Zimmerberg, J., Curran, M., Cohen, F.S. 1991. A lipid/protein complex hypothesis for exocytotic fusion pore formation. Ann. NY Acad. Sci. 635:307–31

    Google Scholar 

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Chanturiya, A.N., Nikoloshina, H.V. Correlations between changes in membrane capacitance induced by changes in ionic environment and the conductance of channels incorporated into bilayer lipid membranes. J. Membarin Biol. 137, 71–77 (1994). https://doi.org/10.1007/BF00234999

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  • DOI: https://doi.org/10.1007/BF00234999

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