Summary
We studied the influence of mucosal Ba2+ ions on the recently described (Zeiske & Van Driessche, 1979a, J. Membrane Biol. 47:77) transepithelial, mucosa towards serosa directed K+ transport in the skin ofRana temporaria. The transport parametersG (conductance), PD (potential difference),I sc (short-circuit current, “K+ current”), as well as the noise ofI sc were recorded. Addition of millimolar concentrations of Ba2+ to the mucosal K+-containing solution resulted in a sudden but quickly reversible drop inI sc.G andI sc decreased continuously with increasing Ba2+ concentration, (Ba2+) o . The apparent Michaelis constant of the inhibition by Ba2+ lies within the range 40–80 μm. The apical membrane seems to remain permselective for K+ up to 500 μm (Ba2+) o . Higher (Ba2+) o , however, appears to induce a shunt (PD falls,G increases). This finding made an accurate determination of the nature of the inhibition difficult but our results tend to suggest a K+-channel block by K+−Ba2+ competition. In the presence of Ba2+, the power spectrum of the K+ current shows a second Lorentzian component in the low-frequency range, in addition to the high-frequency Lorentzian caused by spontaneous K+-channel fluctuations (Van Driessche & Zeiske, 1980). Both Lorentzian components are only present with mucosal K+ and can be depressed by addition of Cs+ ions, thus indicating that Ba2+ ions induce K+-channel fluctuations. The dependence of the parameters of the induced Lorentzian on (Ba2+) o , shows a rise in the plateau values to a maximum around 60 μm (Ba2+) o , followed by a sharp and progressive decrease to very low values. The corner frequency which reflects the rate of the Ba2+-induced fluctuations, however, increases quasi-linearly up to 1mm (Ba2+) o with a tendency to saturate at higher (Ba2+) o . Based on a three-state model for the K+ channel (having one open state, one closed by the spontaneous fluctuation and one blocked by Ba2+) computer calculations compared favorably with our results. The effect of Ba2+ could be explained by assuming reversible binding at the outer side of the apical K+ channel, thereby blocking the open channel in competition with K+. The association-dissociation of Ba2+ at its receptor site is thought to cause a chopping of the K+ current, resulting in modulated current fluctuations.
Similar content being viewed by others
References
Adelman, W.J., Jr. 1971. Electrical studies of internally perfused squid axons.In: Biophysics and Physiology of Excitable Membranes. W.J. Adelman, editor. p. 274. Van Nostrand Reinhold, New York-Cincinnati-Toronto-London-Melbourne
Chen, Y., Hill, T.L. 1973. Fluctuations and noise in kinetic systems. Application to K+ channels in the squid axon.,Biophys. J. 13:1276
Conti, F., Neumcke, B., Nonner, W., Stämpfli, R. 1979. Low frequency fluctuations of Na current in myelinated nerve.Pfluegers Arch. 379:R40
Coronado, R., Miller, C. 1979. Voltage-dependent cesium blockade of a cation channel from fragmented sarcoplasmic reticulum.Nature (London) 280:807
Droogmans, G., Raeymaekers, L., Casteels, R. 1977. Electro- and pharmacomechanical coupling in the smooth muscle cells of the rabbit ear artery.J. Gen. Physiol. 70:129
Ehrlich, E.N., Crabbé, J. 1968. The mechanism of action of amipramizide.Pfluegers Arch. 302:79
Fishman, H.M., Moore, L.E., Poussart, D.J.M. 1977a. Potassiumion conduction noise in squid axon membrane.J. Membrane Biol. 24:305
Fishman, H.M., Moore, L.E., Poussart, D.J.M. 1977. Ion movements and kinetics in squid axon: II. Spontaneous electrical fluctuations.In: Electrical Properties of Biological Polymers. S. Takashima and H.M. Fishman, Editors.Ann. N.Y. Acad. Sci. 303:399
Fishman, H.M., Poussart, D.J.M., Moore, L.E. 1975b. Noise measurements in squid axon membrane.J. Membrane Biol. 24:281
Gebhardt, U., Fuchs, W., Lindemann, B. 1972. Resistance response of frog skin to brief and long lasting changes of (Na) o and (K) o .In: Role of Membranes in Secretory Process. L. Bolis, R.D. Keynes, and W. Wilbrandt, editors. p. 284. North-Holland, Amsterdam
Goldman, D.E. 1943. Potential, impedance, and rectification in membranes.J. Gen. Physiol. 27:37
Hill, T.L., Chen, Y.D. 1972. On the theory of ion transport across the nerve membrane. V. Two models for the Cole-Moore K+-hyperpolarization delay.Biophys. J. 12:960
Hille, B. 1966. The common mode of action of three agents that decrease the transient change in sodium permeability in nerves.Nature (London) 210:1220
Hille, B. 1967. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion.J. Gen. Physiol. 50:1287
Hirschmann, W., Nagel, W. 1978. The outer membrane of frog skin: Impermeable to K+?Pfluegers Arch. 373:R48
Isenberg, G. 1976. Cardiac Purkinje fibers: Cesium as tool to block inward rectifying potassium currents.Pfluegers Arch. 365:99
Lindemann, B., Van Driessche, W. 1977. Sodium-specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover.Science 195:292
Lindemann, B., Van Driessche, W. 1978. The mechanism of Na-uptake through Na-selective channels in the epithelium of frog skin.In: Membrane transport processes. Vol. 1, p. 155. J.F. Hoffman, editor. Raven Press, New York
Lindemann, B., Voûte, C. 1976. Structure and function of the epidermis.In: Frog Neurobiology. R. Llinas and W. Precht, editors. p. 169. Springer-Verlag, Berlin-Heidelberg
Mandel, L.J., Curran, P.F. 1973. Response of the frog skin to steady-state voltage clamping. II. The active pathway.J. Gen. Physiol. 62:1
Mayer, C.J., van Breemen, C., Casteels, R. 1972. The action of lanthanum and D-600 on the calcium exchange in the smooth muscle cells of the guinea-pigtaenia coli.Pfluegers Arch. 337:333
Moore, L.E., Fishman, H.M., Poussart, D.J.M. 1979. Chemically induced K+ conduction noise in squid axon.J. Membrane Biol. 47:99
Nagel, W. 1978. Ba++ decreasesG K in frog skin.Fed. Proc. 37 (3):1869
Nagel, W., Hirschmann, W. 1980. K+-permeability of the outer border of the frog skin (R. temporaria).J. Membrane Biol. 52:107
Smythies, J.R., Benington, F., Bradley, R.J., Bridgers, W.F., Morin, R.D. 1974. The molecular structure of the sodium channel.J. Theor. Biol. 43:29
Sperelakis, N., Schneider, M.F., Harris, E.J. 1967. Decreased K+ conductance produced by Ba++ in frog sartorius fibers.J. Gen. Physiol. 50:1565
Stevens, C.F. 1972. Inferences about membrane properties from electrical noise measurements.Biophys. J. 12:1028
Van Driessche, W., Hegel, U. 1978. Amiloride induced fluctuations of short circuit current through toad urinary bladder.In: Sixth International Biophysics Congress Abstracts. p. 215, Kyoto
Van Driessche, W., Lindemann, B. 1978. Low-noise amplification of voltage and current fluctuations arising in epithelia.Rev. Sci. Instrum. 49:52
Van Driessche, W., Zeiske, W. 1978. Fluctuations of the K+-current in the frog skin (Rana temporaria).Arch. Int. Physiol. Biochem 86:684
Van Driessche, W., Zeiske, W. 1980. Spontaneous fluctuations of potassium channels in the apical membrane of frog skin.J. Physiol. (London) 299:101
Zeiske, W. 1975. The influence of 2,4,6-triaminopyrimidine on Na-transport in frog skin.Pfluegers Arch. 359:R127
Zeiske, W. 1979. Ph.D. Thesis. University of the Saarland, Saarbrücken.
Zeiske, W., Lindemann, B. 1974. Chemical stimulation of Na-current through the outer surface of frog skin epithelium.Biochim. Biophys. Acta 352:323
Zeiske, W., Van Driessche, W. 1978. K+-uptake across the outer border of frog skin (R. temp.) and its inhibition by Cs+-ions.Pfluegers Arch. 373:R48
Zeiske, W., Van Driessche, W. 1979a. Saturable K+ pathway across the outer border of frog skin (Rana Temporaria): Kinetics and inhibition by Cs+ and other cations.J. Membrane Biol. 47:77
Zeiske, W., Van Driessche, W. 1979b. Kinetics of K+ channels in the apical membrane of frog skin: Control by voltage, pH and polyvalent cations.Arch. Int. Physiol. Biochem. 87:331
Zeiske, W., Van Driessche, W. 1979c. Influence of Ba2+ on K+-current noise in frog skin.Pfluegers Arch. 382:R23
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Van Driessche, W., Zeiske, W. Ba2+-Induced conductance fluctuations of spontaneously fluctuating K+ channels in the apical membrane of frog skin (Rana temporaria). J. Membrain Biol. 56, 31–42 (1980). https://doi.org/10.1007/BF01869349
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01869349