Log in

Alkali ion transport through lipid bilayer membranes mediated by enniatin A and B and beauvericin

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Stationary conductance measurements with lipid bilayer membranes in the presence of enniatin A and B and beauvericin were performed. For comparison, some valinomycin systems were investigated. It was found that the conductance in the case of enniatin A and B is caused by a carrier ion complex with a 1∶1 stoichiometry, whereas for beauvericin, a 3∶1 carrier ion complex has to be assumed to explain the dependence of the conductance on carrier and ion concentration in the aqueous phase. The current-voltage curves measured with dioleoyl phosphatidylcholine membranes show a superlinear behavior for the three carriers in the presence of potassium. On the other hand, supralinear current-voltage curves were observed with membranes from different monoglycerides, except for beauvericin. The results obtained with enniatin A and B are in a satisfactory agreement with an earlier proposed carrier model assuming a complexation between carrier and ion at the membrane water interface.

The discrimination between potassium and sodium ions is much smaller for the enniatins than for valinomycin. This smaller selectivity as well as the fact that potassium ions cause the highest conductance with lipid bilayer membranes may be due to the smaller size of the cyclic enniatin molecules, which contain 6 residues in the ringvs. 12 in the case of valinomycin. Charge-pulse relaxation studies were performed with enniatin A and B, beauvericin, and valinomycin. For monoolein membranes only in the case of valinomycin, all three relaxations predicted by the model could be resolved. In the case of the probably more fluid membranes from monolinolein (Δ9, 12-C18: 2) and monolinolenin (Δ9, 12, 15-C18: 3) for all carrier systems except for beauvericin, three relaxations were observed.

The association rate constantk R , the dissociation rate constantk D , and the two translocation rate constantsk MS andk s for complexed and free carrier, respectively, could be calculated from the relaxation data. The carrier concentration in the aqueous phase had no influence on the rate constants in all cases, whereas a strong saturation of the association rate constantk R with increasing ion concentration was found for the enniatins. Because of the saturation,k R did not exceed a value of 4×105 m −1 sec−1 with 1m salt irrespective of carrier, ion, or membrane-forming lipid.

A similar but less pronounced saturation behavior was also observed for the translocation rate constantk S of the free carrier. The other two rate constants were independent of the ion concentration in the aqueous phase. In the case of the enniatins, the translocation rate constantk MS was not independent from the kind of the transported ion. In the series K+, Rb+ and Cs+,k MS increases about threefold. The turnover numbers for the carriers as calculated from the rate constants range between 104 sec−1 and 105 sec−1 and do not show a strong difference between the individual carriers. The conductance difference in the systems investigated here is therefore mainly caused by the partition coefficients, which are smaller for the enniatins than for valinomycin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Benz, R., Fröhlich, O., Läuger, P. 1977. Influence of membrane structure on the kinetics of carrier mediated ion transport through lipid bilayers.Biochim. Biophys. Acta 464:465

    Google Scholar 

  2. Benz, R., Gisin, B.F., Ting-Beall, H.P., Tosteson, D.C., Läuger, P. 1976. Mechanism of ion transport through bilayer membranes mediated by peptide-cyclo-(d-Val-l-Pro-l-Val-d-Pro)3.Biochim. Biophys. Acta 455:665

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  5. Benz, R., Stark, G. 1975. Kinetics of macrotetrolide-induced ion transport across lipid bilayer membranes.Biochim. Biophys. Acta 282:27

    Google Scholar 

  6. 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 

  7. Burgermeister, W., Winkler-Oswatitsch R. 1977. Complex formation of monovalent cations with bio-functional ligands.In: Topics of Current Chemistry. F.L. Boschke, editor. p. 91. Springer Verlag, Berlin-Heidelberg

    Google Scholar 

  8. Ciani, S.M., Eisenman, G., Szabo, G. 1969. A theory for the effects of neutral carriers such as the macrotetralide actin antibiotics on the electrical properties of bilayer membranes.J. Membrane Biol. 1:1

    Google Scholar 

  9. Eisenman, G., Ciani, S.M., Szabo, G. 1968. Some theoretically expected and experimentally observed properties of lipid bilayer membranes containing neutral molecular carriers of ions.Fed. Proc. 27:1289

    Google Scholar 

  10. Eisenman, G., Ciani, S.M., Szabo, G. 1969. The effects of the macrotetralide actin antibiotics on the equilibrium extraction of alkali metal salts into organic solvents.J. Membrane Biol. 1:294

    Google Scholar 

  11. Eisenman, G., Krasne, S. 1974. The ion selectivity of carrier molecules, membranes and enzymes.In: MTP International Review of Science. Biochemistry Series. C.F. Fox, editor. Vol. 2, p. 1 Butterworths, London

    Google Scholar 

  12. Eisenman, G., Krasne, S., Ciani, S.M. 1975. The kinetic and equilibrium components of selective ionic permeability mediated by nactin- and valinomycin-type carriers having systematically varied degrees of methylation.Ann. N. Y. Acad. Sci. 264:34

    Google Scholar 

  13. 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 

  14. 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 

  15. Grell, E., Funk, T., Eggers, F. 1975. Structure and dynamic properties of ion-specific antibiotics.In: Membranes, a Series of Advances. G. Eisenman, editor. Vol. 3, p. 1. Marcel Dekker, New York

    Google Scholar 

  16. Hamill, R.L., Higgins, C.E., Braz, M.E., Gorman, M. 1969. The structure of beauvericin, a new depsipeptide antibiotic toxic to artimia salina.Tetrahedron Lett. 49:4255

    Google Scholar 

  17. Hladky, S.B. 1975. Tests of the carrier model for ion transport by nonactin and trinactin.Biochim. Biophys. Acta 375:327

    Google Scholar 

  18. Ivanov, V.T., Evstratov, A.V., Gumskaya, L.V., Melnik, E.J., Chumburidze, T.S., Portnova, S.L., Balashova, T.A., Ovkinnikov, Y.A. 1973. Sandwich complexes as a functional form of the enniatin ionophores.FEBS Lett. 36:65

    Google Scholar 

  19. Knoll, W., Stark, G. 1975. An extended kinetic analysis of valinomycin-induced Rb-transport through monoglyceride membranes.J. Membrane Biol. 25:249

    Google Scholar 

  20. Krasne, S., Eisenman, G., Szabo, G. 1971. Freezing and melting of bilayers and the mode of action of nonactin, valinomycin and gramicidin.Science 174:412

    Google Scholar 

  21. 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 York

    Google Scholar 

  22. Läuger, P. 1972. Carrier-mediated ion transport.Science 178:24

    Google Scholar 

  23. Läuger, P., Stark, G. 1970. Kinetics of carrier mediated ion transport across lipid bilayer membranes.Biochim. Biophys. Acta 211:458

    Google Scholar 

  24. Markin, V.S., Kristalik, L.J., Liberman, E.A., Topaly, V.P. 1969. Mechanism of conductivity of artificial phospholipid membranes in presence of ion carriers.Biofisika 14:256

    Google Scholar 

  25. McLaughlin, S.G.A., Szabo, G., Ciani, S.M., Eisenman, G. 1972. The effects of a cyclic polyether on the electrical properties of phospholipid bilayer membranes.J. Membrane Biol. 9:3

    Google Scholar 

  26. Morf, W.E., Züst, Ch.U., Simon, W. 1972. Alkali cation specificity of antibiotics, their behaviours in bulk membranes and in ion selective sensors.In: Proceedings of the Symposium on Molecular Mechanism of Antibiotic Action on Protein Biosynthesis and Membranes. E. Munoz, F. Garcia-Fernandiz, and D. Vasquez, editors. p. 523. Elsevier, Amsterdam

    Google Scholar 

  27. Mueller, P., Rudin, D.O. 1967. Development of K+−Na+ discrimination in experimental bimolecular lipid membranes by macrocyclic antibiotics.Biochem. Biophys. Res. Commun. 26:398

    Google Scholar 

  28. Plattner, P.A., Nager, U. 1948. Analyse und Charakterisierung der Enniatine. Über das Verhalten vonN-Methylaminosäuren im Papierchromatogramm.Helv. Chim. Acta 31:2203

    Google Scholar 

  29. Plattner, P.A., Nager, U., Boller, A. 1948. Über die Isolierung neuartiger Antibiotika aus Fusarien.Helv. Chim. Acta 31:594

    Google Scholar 

  30. Plattner, P.A., Vogler, K., Studer, R.O., Quitt, P., Keller-Schierlein, W. 1963. Synthese von Enniatin B.Helv. Chim. Acta 46:927

    Google Scholar 

  31. Quitt, P., Studer, R.O., Vogler, K. 1963. Synthese von Enniatin A.Helv. Chim. Acta 46:1715

    Google Scholar 

  32. Shemyakin, M.M., Ovchinnikov, Yu.A., Ivanov, V.T., Antonov, V.K., Vinogradova, E.I., Shkrob, A.M., Malenkov, G.G., Evstratov, A.V., Laine, I.A., Melnik, E.I., Ryabova, I.D. 1969. Cyclodepsipeptides as chemical tools for studying ionic transport through membranes.J. Membrane Biol. 1:402

    Google Scholar 

  33. Stark, G., Benz, R. 1971. The transport of potassium through lipid bilayer membranes by the neutral carriers valinomycin and monactin: Experimental studies to a previously proposed model.J. Membrane Biol. 5:133

    Google Scholar 

  34. Stark, G., Ketterer, B., Benz, R., Läuger, P. 1971. The rate constants of valinomycin-mediated ion transport through thin lipid membranes.Biophys. J. 11:981

    Google Scholar 

  35. Ting-Beall, H.P., Tosteson, M.T., Gisin, B.F., Tosteson, D.C. 1974. Effect of peptide PV on the ionic permeability of lipid bilayer membranes.J. Gen. Physiol. 63:492

    Google Scholar 

  36. Tosteson, D.C. 1968. Effect of macrocyclic compounds on the ionic permeability of artificial and natural membranes.Fed. Proc. 27:1969

    Google Scholar 

  37. Tosteson, D.C., Andreoli, T.E., Tieffenberg, M., Cook, P. 1963. The effects of macrocyclic compounds on cation transport in sheep red cells and thin and thick lipid membranes.J. Gen. Physiol. 51:373

    Google Scholar 

  38. Wipf, H.-K., Pioda, L.A.R., Stefanac, Z., Simon, W. 1968. Komplexe von Enniatinen und anderen Antibiotica mit Alkalimetall-Ionen.Helv. Chim. Acta 51:377

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benz, R. Alkali ion transport through lipid bilayer membranes mediated by enniatin A and B and beauvericin. J. Membrain Biol. 43, 367–394 (1978). https://doi.org/10.1007/BF01871697

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01871697

Keywords

Navigation