Summary
An osmotic method was used to study the salt permeability induced by gramicidin A in liposomes. Sequences of cation permeation were obtained for iodide, salycilate, acetate und formate salts in liposomes below and above their transition temperature. Salycilate and formate salts, unlike acetate and iodide salts, exhibit the same sequences for cation selectivity in liposomes below and above their transition temperature. These results can be explained by assuming three mechanisms for salt permeation across gramicidin-containing liposomes: (i) the anion moves by the lipid part of the membrane whereas the cation moves by the gramicidin channel, (ii) movement of the undissociated acid species occurs through the lipid part of the membrane followed by cation-proton exchange via the gramicidin channel and (iii) the cation and anion may move simultaneously via the gramicidin channel.
When the movement of the anion or undissociated acid across the lipid part of the membrane is not rate limiting the permeation process, the cation selectivity obtained agrees with the cation selectivity of the gramicidin A channel, as determined by others using independent measurements.
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Alger, J.R., Prestegard, J.H. 1979. Nuclear magnetic resonance study of acetic acid permeation of large unilamellar vesicle membranes.Biophys. J. 28:1–14
Archer, D.W., Monk, C.B. 1964. Ion-association of some acetates by pH (glass-electrode) measurements.J. Chem. Soc. (1964):3117–3122
Bamberg, E., Apell, H.J., Alpes, H. 1977. Structure of the gramicidin A channel: Discrimination between the {ie87-1 helix and the β helix by electrical measurements with lipid bilayer membranes}.Proc. Natl. Acad. Sci. USA 74:2402–2406
Bangham, A.D., Hill, M.W., Miller, N. 1974. Preparation and use of liposomes as models of biological membranes.In: Methods in Membrane Biology. Vol. 1, pp. 1–68. E.D. Korn, editor. Plenum Press, New York
Bangham, A.D., Standish, M., Watkins, J.C. 1965. Diffusion of univalent ions across the lamellae of swollen phospholipids.J. Mol. Biol. 13:238–252
Boehler, B.A., De Gier, J., Van Deenen, L.L.M. 1978. The effect of gramicidin A on the temperature dependence of water permeation through liposomal membranes prepared from phosphatidyl-cholines with different chain lengths.Biochim. Biophys. Acta 512:480–488
Bray, G.A. 1960. A simple efficient liquid scintillator for counting aqueous solutions in a liquid scintillation counter.Anal. Biochem. 1:279–285
Chapman, D., Urbina, J., Keough, K.M. 1974. Biomembrane phase transition: Studies of lipid-water system using differential scanning calorimetry.J. Biol. Chem. 249:2512–2521
Chappell, J.B., Crofts, A.R. 1965. Gramicidin and ion transport in isolated liver mitochondria.Biochem. J. 95:393–402
Cohen, B.E. 1975a. The permeability of liposomes to nonelectrolytes: I. Activation energies for permeation.J. Membrane Biol. 20:205–234
Cohen, B.E. 1975b. The permeability of liposomes to nonelectrolytes: II. The effect of nystatin and gramicidin A.J. Membrane Biol. 20:235–268
Cohen, B.E., Bangham, A.D. 1972. Diffusion of small nonelectrolytes across liposomes membranes.Nature (London) 236:173–174
Collander, R. 1950. The distribution of organic compounds between isobutanol and water.Acta Chem. Scand 4:1085–1098
Eisenman, G. 1961. On the elementary atomic origin of equilibrium ionic specificity.In: Symposium on Membrane Transport and Metabolism. A. Kleinzeller and A. Kotyk, editor pp. 163–179. Academic Press, New York
Eisenman, G., Krasne, S., Ciani, S. 1976. Further studies on ion selectivity.In: Ion and Enzyme Electrodes in Biology and Medicine. pp. 3–21. M. Kessler, L. Clark, D. Lubbers, I. Silver, and W. Simon, editor. Urban & Schwarzenberg, Munich
Eisenman, G., Sandblom, J., Neher, E. 1977. Ionic selectivity, saturation, binding and block in the gramicidin A channel: A preliminary report.In: Metal-ligand Interaction in Organic Chemistry and Biochemistry. B. Pullman and N. Goldblum, editors. Part 2, pp. 1–36. D. Reidel, Dordrecht-Holland
Eisenman, G., Sandblom, J., Neher, E. 1978. Interactions in cation permeation through the gramicidin channel. Cs, Rb, K, Na, Li, Tl, H and effects of anion binding.Biophys. J. 22:307–346
Finkelstein, A., Cass, A. 1968. Permeability and electric properties of thin lipid membranes.J. Gen. Physiol. 52:145s-172s
Goodall, M.C. 1971. Thickness dependence in the action of gramicidin A on lipid bilayers.Arch. Biochim. Biophys. 147:129–135
Haydon, D.A., Hladky, S.B. 1972. Ion transport across thin lipid membranes: A critical discussion of mechanism in selected systems.Q. Rev. Biophys. 5:187–282
Henderson, P.J.F., McGivan, J.D., Chappell, J.B. 1969. The action of certain antibiotics on mitochondrial, erythrocyte and artificial phospholipid membranes.Biochem. J. 111:521–535
Hendrikson, J.B., Cram, D.J., Hammond, G.S. 1970. Organic Chemistry. McGraw-Hill, New York
Hill, M.W., Cohen, B.E. 1972. A simple method of determining relative permeabilities of liposomes to nonelectrolytes.Biochim. Biophys. Acta 290:403–407
Hladky, S.B. 1972. The two site lattice model for the pore. Appendix B′ Ph.D. dissertation, Cambridge University, England
Hladky, S.B., Haydon, D.A. 1970. Discreteness of conductance changes in bimolecular lipid membranes in the presence of certain antibiotics.Nature (London) 255:451–453
Hladky, S.B., Haydon, D.A. 1972. Ion transfer across lipid membranes in the presence of gramicidin A. I. Studies of the unit conductance channel.Biochim. Biophys. Acta 274:294–312
Krasne, S., Eisenman, G., Szabo, G. 1971. Freezing and melting of lipid bilayers and the mode of action of nonactin, valinomycin and gramicidin.Science 174:412–415
Läuger, P. 1973. Ion transport through pores. A rate-theory analysis.Biochim. Biophys. Acta 311:423–441
McLaughlin, S. 1973. Salicylates and phospholipid bilayer membranes.Nature (London) 243:234–236
McLaughlin, S.G.A., Szabo, G., Eisenman, G., Ciani, S.M. 1970. Surface charge and the conductance of phospholipid membranes.Proc. Natl. Acad. Sci. USA 67:1268–1275
Monk, C.B. 1961. Electrolytic dissociation. P. 271. Academic Press, New York
Mueller, P., Rudin, D.O. 1967. Development of K+−Na+ discrimination in experimental bimolecular lipid membranes by macrocyclic antibiotics.Biochem. Biophys. Res. Commun. 26:398–404
Myers, V.B., Haydon, D.A. 1972. Ion transfer across lipid membranes in the presence of gramicidin A: II. The ion selectivity.Biochim. Biophys. Acta 274:313–322
Oldfield, E., Meadows, M., Rice, D., Jacobs, R. 1978. Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems.Biochemistry 17:2727–2740
Papahadjopoulos, D., Miller, N. 1967. Phospholipid model membranes: I. Structural characteristics of hydrated liquid crystals.Biochim. Biophys. Acta 135:624–638
Pressman, B.C. 1965. Induced active transport of ions into mitochondria.Proc. Natl. Acad. Sci. USA 53:1076–1083
Robinson, R.A., Stokes, R.H. 1970. Electrolyte Solutions. (2nd ed.) Butterworths, London
Rosenberg, P.A., Finkelstein, A. 1978. Water permeability of gramicidin A-treated lipid bilayer membranes.J. Gen. Physiol. 72:341–350
Sandblom, J., Eisenman, G., Neher, E. 1977. Ionic selectivity, saturation and block in gramicidin A channels: I. Theory for the electric properties of ion selective channels having two pairs of binding sites and multiple conductance states.J. Membrane Biol. 31:383–417
Singer, M.A. 1973. Transfer of anions across phospholipid membranes.Can. J. Physiol. Pharmacol. 51:523–531
Singer, M.A., Bangham, A.D. 1971. The consequences of inducing salt permeability in liposomes.Biochim. Biophys. Acta 241:687–692
Szabo, G., Eisenman, G., McLaughlin, S., Krasne, S. 1972. Ionic probes of membrane structures.Ann. N.Y. Acad. Sci. 195:273–295
Tosteson, D.C. 1968. Effect of macrocyclic compounds on the ionic permeability of artificial and natural membranes.Fed. Proc. 27:1269–1277
Urban, B.W., Hladky, S.B., Haydon, D.A. 1980. Ion movements in gramicidin pores. An example of single-file transport.Biochim. Biophys. Acta 602:331–354
Urry, D.W. 1971. The gramicidin A transmembrane channel. A proposed {ie88-1 helices}.Proc. Natl. Acad. Sci. USA 68:672–676
Urry, D.W., Goodall, M.C., Glickson, J.D., Mayers, D.F. 1971. The gramicidin A transmembrane channel: Characteristics of head to head dimerized {ie88-2 helices}.Proc. Natl. Acad. Sci. USA 68:1907–1911
Veatch, W.R., Fossel, E.T., Blout, E.R. 1974. The conformation of gramicidin A.Biochemistry 13:5249–5256
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Cohen, B.E. Effect of anions on the cation selectivity of gramicidin-containing liposomes. J. Membrain Biol. 68, 79–88 (1982). https://doi.org/10.1007/BF01872256
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DOI: https://doi.org/10.1007/BF01872256