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Ion conductance and ion selectivity of potassium channels in snail neurones

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Summary

Delayed potassium channels were studied in internally perfused neurone somata from land snails. Relaxation and fluctuation analysis of this class of ion channels revealed Hodgkin-Huxley type K channels with an average single channel conductance (γ K) of 2.40±0.15 pS. The conductance of open channels is independent of voltage and virtually all K channels seem to be open at maximum K conductance (g K) of the membrane. Voltage dependent time constants of activation ofg K, calculated from K current relaxation and from cut-off frequencies of power spectra, are very similar indicating dominant first-order kinetics. Ion selectivity of K channels was studied by ion substitution in the external medium and exhibited the following sequence: T1+>K+>Rb+>Cs+>NH +4 >Li+>Na+. The sequence of the alkali cations does not conform to any of the sequences predicted by Eisenman's theory. However, the data are well accommodated by a new theory assuming a single rate-limiting barrier that governs ion movement through the channel.

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References

  • Adams, D.J., Gage, P.W. 1979. Ionic currents in response to membrane depolarization in anAplysia neurone.J. Physiol. (London) 289:115

    Google Scholar 

  • Anderson, C.R., Stevens, C.F. 1973. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction.J. Physiol. (London) 235:655

    Google Scholar 

  • Armstrong, C.M. 1975. Ionic pores, gates, and gating currents.Q. Rev. Biophys. 7:179

    Google Scholar 

  • Begenisich, T., Stevens, C.F. 1975. How many conductance states do potassium channels have?Biophys. J. 15:843

    Google Scholar 

  • Bezanilla, F., Armstrong, C.M. 1972. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons.J. Gen. Physiol. 60:588

    Google Scholar 

  • Bockris, J.O'M., Reddy, A.K.N. 1973. Modern Electrochemistry, Vol. 1. Plenum, New York

    Google Scholar 

  • Born, M. 1920. Volumen und Hydratationswärme der Ionen.Z. Phys. 1:45

    Google Scholar 

  • Buckingham, A.D. 1957. A theory of ion-solvent interaction.Faraday Soc. Disc. 24:151

    Google Scholar 

  • Connor, J.A., Stevens, C.F. 1971a. Inward and delayed outward membrane currents in isolated neural somata under voltage clamp.J. Physiol. (London) 213:1

    Google Scholar 

  • Connor, J.A., Stevens, C.F. 1971b. Voltage clamp studies of a transient outward membrane current in gastropod neural somata.J. Physiol. (London) 213:21

    Google Scholar 

  • Conti, F., DeFelice, L.J., Wanke, E. 1975. Potassium and sodium ion current noise in the membrane of the squid giant axon.J. Physiol. (London) 248:45

    Google Scholar 

  • Diamond, J.M., Wright, E.M. 1969. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Annu. Rev. Physiol. 31:581

    Google Scholar 

  • Dogonadze, R.R., Kornyshev, A.A. 1974. Polar solvent structure in the theory of ionic solvation.J. Chem. Soc. Faraday Trans. 2.70:1121

    Google Scholar 

  • Eisenman, G. 1963. Cation selective glass electrodes and their mode of operation.Biophys. J. 2 (suppl. 2):259

    Google Scholar 

  • Fishman, H.M., Moore, L.E., Poussart, D.J.M. 1975. Potassiumion conduction noise in squid axon membrane.J. Membrane Biol. 24:305

    Google Scholar 

  • Gay, L.A., Stanfield, P.R. 1978. The selectivity of the delayed potassium conductance of frog skeletal muscle fibers.Pfluegers Arch. 378:177

    Google Scholar 

  • Goldman, D.E. 1943. Potential impedance and rectification in membranes.J. Gen. Physiol. 27:37

    Google Scholar 

  • Heyer, C.B., Lux, H.D. 1976. Control of the delayed outward potassium currents in bursting pace-makers neurones of the snail.Helix Pomatia.J. Physiol. (London) 262:349

    Google Scholar 

  • Hille, B. 1973. Potassium channels in myelinated nerve. Selective permeability to small ions.J. Gen. Physiol. 61:669

    Google Scholar 

  • Hille, B. 1975. Ionic selectivity of Na and K channels of nerve membranes.In: Membranes — A Series of Advances, Vol. 3, Dynamic Properties of Lipid Bilayers & Biological Membranes. G. Eisenman, editor. p. 255. Marcel Dekker, Inc., New York

    Google Scholar 

  • Hille, B. 1977. Ionic basis of resting and action potentials.In: Handbook of Physiology, The Nervous System I. E. Kandel, editor. p. 99. Williams & Wilkin, Baltimore

    Google Scholar 

  • Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37

    Google Scholar 

  • Horn, R., Stevens, C.F. 1980. Relation between structure and function of ion channels.Comm. Mol. Cell. Biophys. (in press)

  • Huang, L.M., Catterall, W.A., Ehrenstein, G. 1978. Selectivity of cations and nonelectrolytes for acetylcholine-activated channels in cultured muscle cells.J. Gen. Physiol. 71:397

    Google Scholar 

  • Joesten, M.D., Schaad, L.J. 1974. Hydrogen Bonding. Marcel Dekker, Inc., New York

    Google Scholar 

  • Kostyuk, P.G., Krishtal, O.A. 1977. Separation of sodium and calcium currents in the somatic membrane of mollusc neurones.J. Physiol. (London) 270:545

    Google Scholar 

  • Kostyuk, P.G., Krishtal, O.A., Doroshenko, P.A. 1975. Outward currents in isolated snail neurones. II. Effect of TEA.Comp. Biochem. Physiol. 51C:265

    Google Scholar 

  • Kostyuk, P.G., Krishtal, O.A., Pidoplichko, U.T. 1975. Effects of internal fluoride and phosphate on membrane currents during intracellular dialysis of nerve cells.Nature (London) 257:691

    Google Scholar 

  • Krasne, S., Eisenman, G. 1973. The molecular basis of ion selectivity.In: Membranes—A Series of Advances, Vol. 2, G. Eisenman, editor. p. 179. Marcel Dekker, Inc., New York

    Google Scholar 

  • Lee, A.G. 1977. The coordination chemistry of thallium (I).Coord. Chem. Rev. 8:281

    Google Scholar 

  • Lee, K.S., Akaike, N., Brown, A.M. 1978. Properties of internally perfused, voltage clamped, isolated nerve cell bodies.J. Gen. Physiol. 71:489

    Google Scholar 

  • Matsuoka, O., Clementi, E., Yoshimine, M. 1976. Cl study of the water dimer potential surface.J. Chem. Phys. 64:1351

    Google Scholar 

  • Meech, R.W. 1978. Calcium-dependent potassium activation in nervous tissue.Ann. Rev. Biophys. Bioeng. 7:1

    Google Scholar 

  • Meech, R.W., Standen, N.B. 1975. Potassium activation inHelix aspersa neurones under voltage clamp: A component mediated by calcium influx.J. Physiol. (London) 249:211

    Google Scholar 

  • Meves, H. 1968. The ionic requirements for the production of action potentials inHelix pomatia neurones.Pfluegers Arch. 304:215

    Google Scholar 

  • Neher, E. 1971. Two fast transient current components during voltage clamp on snail neurones.J. Gen. Physiol. 58:36

    Google Scholar 

  • Neher, E., Lux, H.D. 1973. Rapid changes of potassium concentration at the outer surface of exposed neurones during membrane current flow.J. Gen. Physiol. 61:385

    Google Scholar 

  • Neher, E., Stevens, C.F. 1977. Conductance fluctuations and ionic pores in membranes.Annu. Rev. Biophys. Bioeng. 6:345

    Google Scholar 

  • Noyes, R.M. 1962. Thermodynamics of ion hydration as a measure of effective dielectric properties of water.J. Am. Chem. Soc. 84:513

    Google Scholar 

  • Partridge, L.D., Stevens, C.F. 1976. A mechanism for spike frequency adaptation.J. Physiol. (London) 256:315

    Google Scholar 

  • Payzant, J.D., Cunningham, A.J., Kebarle, P. 1973. Gas phase solvation of the ammonium ion by NH3 and H2O and stabilities of mixed clusters NHa(NH3)n(H2O)w.Can. J. Chem. 51:3242

    Google Scholar 

  • Robinson, R.A., Stokes, R.H. 1959. Electrolyte Solutions. Butterworths, London

    Google Scholar 

  • Scheiner, S., Kern, C.W. 1977. Theoretical studies of environmental effects on protein conformation. 1. Flexibility of the peptide bond.J. Am. Chem. Soc. 99:7042

    Google Scholar 

  • Siebenga, E., Meyer, A.W.A., Verveen, A.A. 1973. Membrane shotnoise in electrically depolarized nodes ofRanvier.Pfluegers Arch. 341:87

    Google Scholar 

  • Sigworth, F.J. 1979. Analysis of nonstationary sodium current fluctuations in frog myelinated nerve. Ph.D. Thesis, Yale University, New Haven, Connecticut

    Google Scholar 

  • Stevens, C.F. 1972. Inferences about membrane properties from electrical noise measurements.Biophys. J. 12:1028

    Google Scholar 

  • Stevens, C.F., Tsien, R.W. 1979. Membrane Transport Processes. Vol. 3. Ion Permeation Through Membrane Channels. Raven Press, New York

    Google Scholar 

  • Thompson, S.H. 1977. Three pharmacologically distinct potassium channels in molluscan neurones.J. Physiol. (London) 265:465

    Google Scholar 

  • Wolbarsht, M.L., MacNichol, E.F., Wagner, H.G. 1960. Glass insulated platinum electrode.Science 132:1309

    Google Scholar 

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This paper is dedicated to the memory of Walther Wilbrandt.

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Reuter, H., Stevens, C.F. Ion conductance and ion selectivity of potassium channels in snail neurones. J. Membrain Biol. 57, 103–118 (1980). https://doi.org/10.1007/BF01868997

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