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The Journal of Membrane Biology

, Volume 30, Issue 1, pp 1–44 | Cite as

Influence of molecular variations of ionophore and lipid on the selective ion permeability of membranes: I. Tetranactin and the methylation of nonactin-type carriers

  • S. Krasne
  • G. Eisenman
Article

Summary

The manner in which the molecular structure of the carrier and the lipid composition of the membrane modulate the membrane selectivity among monovalent cations has been investigated for nonactin, trinactin, and tetranactin, which differ only in their degrees of methylation, and for membranes made of two lipids, phosphatidyl ethanolamine and glyceryl dioleate, in which “equilibrium” and “kinetic” aspects of permeation, respectively, are emphasized. Bilayer permeability ratios for Li, Na, K, Rb, Cs, Tl, and NH4 have been characterized and resolved into “equilibrium” and “kinetic” components using a model for carrier-mediated membrane transport which includes both a trapezoidal energy barrier for translocation of the complex across the membrane interior and a potential-dependence of the loading and unloading of ions at the membrane-solution interfaces. The bilayer permeability properties due to tetranactin have been characterized in each of these lipids and found not only to be regular but to be systematically related to those of the less methylated homologues, trinactin and nonactin. This analysis has led to the following conclusions: (1) The change in lipid composition alters the relative contributions of “kinetic”vs. “equilibrium” components to the observed carrier-mediated selectivity. (2) Increased methylation of the carrier increases the contribution of the “kinetic” component to the selectivity relative to that of the “equilibrium” component and additionally alters the “equilibrium” component sufficiently that an inversion in Cs−Na selectivity occurs between trinactin and tetranactin. (3) For all ions and carriers examined, the “reaction plane” for ion-carrier complexation and the width for the “diffusion barrier” can be represented by the same two parameters, independent of the ion or carrier, so that in all cases the complexation reaction senses 10% of the applied potential and the plateau of the “diffusion barrier” extends across 70% of the membrane interior.

Keywords

Ethanolamine Lipid Composition Phosphatidyl Ethanolamine Glyceryl Diffusion Barrier 
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. Andersen, O., Fuchs, M. 1975. Potential energy barriers to ion transport within lipid bilayers. Studies with tetraphenylborate.Biophys. J. 15:795Google Scholar
  2. Benz, R., Stark, G. 1975. Kinetics of macrotetralide-induced ion transport across lipid bilayer membranes.Biochim. Biophys. Acta 382:27Google Scholar
  3. 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
  4. Ciani, S. 1976. The influence of molecular variations of ionophore and lipid on the selective ion permeability of membranes. II. A theoretical model.J. Membrane Biol. 30:45Google Scholar
  5. Ciani, S.M., Eisenman, G., Laprade, R., Szabo, G. 1973a. Theoretical analysis of carrier-mediated electrical properties of bilayer membranes.In: Membranes — A Series of Advances. G. Eisenman, editor. Vol. 2, p. 61. Marcel Dekker, New YorkGoogle Scholar
  6. Ciani, S., 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. 1:1Google Scholar
  7. Ciani, S., Gambale, F., Gliozzi, A., Rolandi, R. 1975. Effects of unstirred layers on the steady-state zero-current conductance of bilayer membranes mediated by neutral carriers by ions.J. Membrane Biol. 24:1Google Scholar
  8. Ciani, S., Laprade, R., Eisenman, G., Szabo, G. 1973b. Theory for carrier-mediated zero-current conductance of bilayers extended to allow for nonequilibrium of interfacial reactions, spatially dependent mobilities and barrier shape.J. Membrane Biol. 11:255Google Scholar
  9. Eisenman, G. 1961. On the elementary atomic origin of equilibrium ionic specificity.In: Symposium on Membrane Transport and Metabolism. A. Kleinzeller and A. Kotyk, editors, p. 163. New York, Academic PressGoogle Scholar
  10. Eisenman, G. 1969. Theory of membrane electrode potentials: An examination of the parameters determining the selectivity of solid and liquid ion exchangers and of neutral ion-sequestering molecules.In: Ion-Selective Electrodes. R.A. Durst, editor. National Bureau of Standards Special Publications314:1–56Google Scholar
  11. 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. 27:1289Google Scholar
  12. Eisenman, G., Ciani, S., Szabo, G. 1969. The effects of the macrotetralide actin antibiotics on the equilibrium extraction of alkali metal salts into organic solvents.J. Membrane Biol. 1:294Google Scholar
  13. Eisenman, G., Krasne, S. 1975. The ion selectivity of carrier molecules, membranes and enzymes. MTP International Review of Science, Biochemistry Series. C.F. Fox, editor. Vol. 2, pp. 27–59. Butterworths, LondonGoogle Scholar
  14. Eisenman, G., Krasne, S., Ciani, S. 1975. The kinetic and equilibrium components of selective ionic permeability mediated by nactin- and valinomycin-type carriers having system-atically varied degrees of methylation.In: Annals of the New York Academy of Sciences. International Conference on Carriers and Channels in Biological Systems.264:34Google Scholar
  15. Eisenman, G., Szabo, G., Ciani, S., McLaughlin, S.G.A., Krasne, S. 1973. Ion binding and ion transport produced by lipid soluble molecules.Prog. Surf. Membr. Sci. 6:139Google Scholar
  16. 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. 20:269Google Scholar
  17. Hall, J.E., Mead, C.A., Szabo, G. 1973. A barrier model for current flow in lipid bilayer membranes.J. Membrane Biol. 11:75Google Scholar
  18. 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
  19. Hille, B. 1975. Ionic selectivity of Na and K channels of nerve membranes.In: Membranes —A Series of Advances. G. Eisenman, editor, Vol. 3, Ch. 4. Marcel Dekker, New YorkGoogle Scholar
  20. Hladky, S.B. 1972. The steady-state theory of the carrier transport of ions.J. Membrane Biol. 10:67Google Scholar
  21. Hladky, S.B. 1973. The effect of stirring on the flux of carriers into black lipid membranes.Biochim. Biophys. Acta 307:261Google Scholar
  22. Hladky, S.B. 1974. The energy barriers to ion transport by nonactin across thin lipid membranes.Biochim. Biophys. Acta 352:71Google Scholar
  23. Hladky, S.B., Haydon, D.A. 1973. Membrane conductance and surface potential.Biochim. Biophys. Acta 318:464Google Scholar
  24. Iitaka, Y., Sakamaki, T., Nawata, Y. 1972. The molecular structure of tetranactin and its alkali metal ion complexes.Chem. Lett. 1225Google Scholar
  25. Kilbourn, B.T., Dunitz, J.D., Pioda, L.A.R., Simon, W. 1967. Structure of the K+ complex with nonactin, a macrotetralide antibiotic possessing highly specific K+ transport properties.J. Mol. Biol. 30:559Google Scholar
  26. Kostetsky, P.V., Ivanov, V.T., Ovchinnikov, Yu.A., Shchembelov, G. 1973. The nature of the metal-ligand bonding in the complexes of ionophores with alkali metal ions. A quantum mechanical study of the N,N-dimethyl acetamide and methyl acetate interaction with Na+ and Li+ FEBS Letters30:205Google Scholar
  27. Krasne, S., Eisenman, G. 1973. The molecular basis of ion selectivity.In: Membranes —A Series of Advances. G. Eisenman, editor. Vol. 2, pp. 277–328. Marcel Dekker, New YorkGoogle Scholar
  28. Laprade, R., Ciani, S.M., Eisenman, G., Szabo, G. 1975. The kinetics of carrier-mediated ion permeation in lipid bilayers and its theoretical interpretation.In: Membranes — A Series of Advances. G. Eisenman, editor. Vol. 3, Ch. 2. Marcel Dekker, New YorkGoogle Scholar
  29. Läuger, P., Stark, G. 1970. Kinetics of carrier-mediated ion transport across lipid bilayer membranes.Biochim. Biophys. Acta 211:458Google Scholar
  30. Markin, V.S., Kristalik, L.I., Liberman, E.A., Topaly, V.P. 1969. Cell Biophysics. Mechanism of conductivity of artificial phospholipid membranes in the presence of ion carriers.Biofizika, No. 214:256Google Scholar
  31. Murrell, J.N., Kettle, S.F.A., Tedder, J.M. 1965. Valence Theory. Ch. 16. John Wiley and Sons, Ltd., LondonGoogle Scholar
  32. Neumcke, B., Läuger, P. 1969. Nonlinear electrical effects in lipid bilayer membranes. II. Integration of the generalized Nernst-Planck equation.Biophys. J. 9:1160Google Scholar
  33. Phillies, G.D.J., Asher, I.M., Stanley, H.E. 1975. Electrostatic and steric effects in the selective complexation of cations.Science 188:1027Google Scholar
  34. Pressman, B.C., Harris, E.J., Jagger, W.S., Johnson, J.H. 1967. Antibiotic-mediated transport of alkali ions across lipid barriers.Proc. Nat. Acad. Sci. 58:1949Google Scholar
  35. Pullmann, A., Schuster, P. 1974. Model studies on the binding of metal cations to macrocyclic ligands. The interaction of Li+ with carbonyl groups.Chem. Phys. Lett. 24:472Google Scholar
  36. Stark, G., Benz, R. 1971. The transport of potassium through lipid bilayer membranes by the neutral carriers valinomycin and monactin.J. Membrane Biol. 5:133Google Scholar
  37. Szabo, G., Eisenman, G. 1973. Enhanced cation permeation in glyceryl oleate bilayers.Biophys. Soc. Abstr. 175a Google Scholar
  38. Szabo, G., Eisenman, G., Ciani, S., 1969. The effects of the macrotetralide actin antibiotics on the electrical properties of phospholipid bilayer membranes.J. Membrane Biol. 1:346Google Scholar
  39. Szabo, G., Eisenman, G., Ciani, S.M., Laprade, R., Krasne, S. 1973. Experimentally observed effects of carriers on the electrical properties of membranes. The equilibrium domain.In: Membranes — A Series of Advances. G. Eisenman, editor. Vol. 2, p. 179 Marcel Dekker, New YorkGoogle Scholar
  40. White, S. 1970. Thickness changes in lipid bilayer membranes.Biochim. Biophys. Acta 323:7Google Scholar
  41. White, S. 1972. Analysis of the torus surrounding planar lipid bilayer membranes.Biophys. J. 12:432Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1976

Authors and Affiliations

  • S. Krasne
    • 1
    • 2
  • G. Eisenman
    • 1
    • 2
  1. 1.Department of PhysiologyUniversity of California Medical SchoolLos Angeles
  2. 2.Brain Research InstituteUniversity of California Medical SchoolLos Angeles

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