Summary
Voltage clamp experiments were performed on myelinated nerve fibres of Rana esculenta. The combined effects of increasing extracellular H+ concentration and lowering the Na+ concentration on sodium currents were studied. The presence of negative charges of two types at the external membrane surface could explain the observed shifts in theI Na-V curves and the reduction ofI Na induced by H+. Accordingly, from the data of shifts of the conductance voltage curves we calculate a density of −1e o/(20 Å)2 for unsepecific charges with an intrinsic pKa=4.3. From the reduction ofI Na induced by H+ we estimate a density of −1e o/Na channel for specific charges with an intrinsic pKa=4.5. Na+ ions would bind to these specific charges when passing through the sodium channels and Na+ transport would be blocked if these groups are protonated.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Brismar, T.: Effects of ionic concentration on permeability properties of nodal membrane in myelinated nerve fibres of Xenopus laevis. Potential clamp experiments. Acta physiol. scand.87, 474–484 (1973)
Chandler, W. K., Hodgkin, A. L., Meves, H.: The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons. J. Physiol. (Lond.)180, 821–836 (1965)
Cole, K. S.: Zeta potential and discrete vs. uniform surface charges. Biophys. J.9, 465–469 (1969)
D'Arrigo, J. S.: Possible screening of surface charges on crayfish axons by polyvalent metal ions. J. Physiol. (Lond.)231, 117–128 (1973)
Davies, C. W.: Ion association. London: Butterworths 1962
Dodge, F. A., Frankenhaeuser, B.: Membrane currents in isolated frog nerve fibre under voltage clamp conditions. J. Physiol. (Lond.)143, 76–90 (1958)
Drouin, H., The, R.: The effect of reducing extracellular pH on the membrane currents of the Ranvier node. Pflügers Arch.313, 80–88 (1969)
Drouin, H.: The interaction of Na+ and H+ ions with the membrane of the Ranvier node. Proc. Int. Union Physiol. Sci.9, 150 (1971)
Dubois, J. M., Bergman, C.: Variation de la conductance sodium de la membrane nodale en fonction de la concentration en ions Na+ C.R. Acad. Sci. (Paris)272, 2796–2799 (1971)
Durst, R. A., Staples, B. R.: Tris/Tris · HCl: A standard buffer for use in the physiologic pH range. Clin. Chem.18, 206–208 (1972)
Ehrenstein, G., Gilbert, D. L.: Evidence for membrane surface charge from measurement of potassium kinetics as a function of external divalent cation concentration. Biophys. J.13, 495–497 (1973)
Fox, J. M.: Selective blocking of the nodal sodium channels by ultraviolet radiation: II. Interaction of Ca++, H+, and hyperpolarization. Pflügers Arch. (in press) (1974)
Gilbert, D. L., Ehrenstein, G.: Effect of divalent cations on potassium conductance of squid axons: Determination of surface charge. Biophys. J.9, 447–463 (1969)
Gilbert, D. L., Ehrenstein, G.: Use of a fixed charge model to determine the pK of the negative sites on the external membrane surface. J. gen. Physiol.55, 822–825 (1970)
Gilbert, D. L.: Fixed surface charges. In: Biophysics and Physiology of excitable membranes. W. J. Adelman, Jr., Ed., New York: van Nostrand Reinhold 1971
Grahame, D. C.: The electrical double layer and the theory of electrocapillarity. Chem. Rev.41, 441–501 (1947)
Hartz, T., Ulbricht, W.: Comparison of the effects of calcium and lanthanum on the crayfish giant axon. Pflügers Arch.345, 281–294 (1973)
Haydon, D. A., Myers, V. B.: Surface charge, surface dipoles and membrane conductance. Biochim. biophys. Acta (Amst.)307, 429–443 (1973)
Hille, B.: The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J. gen. Physiol.50, 1287–1302 (1967)
Hille, B.: Charges and potentials at the nerve surface. Divalent ions and pH. J. gen. Physiol.51, 221–236 (1968)
Hille, B.: Potassium channels in myelinated nerve: Selective permeability to small cations. J. gen. Physiol.61, 669–686 (1973)
Hille, B., Woodhull, A. M., Shapiro, B. I.: Negative surface charge near sodium channels of nerve: Divalent ions, monovalent ions, and pH. Phil. Trans. Roy Soc. (in press)
Hladky, S. B., Haydon, D. A.: Membrane conductance and surface potential. Biochim. biophys. Acta (Amst.)318, 464–468 (1973)
Hodgkin, A. L., Huxley, A. F.: Currents carried by sodium and potassium ions through the membrane of the giant axon of loligo. J. Physiol. (Lond.)116, 449–472 (1952)
Kilb, H., Stämpfli, R.: Ein Vielwegehahn zur raschen Umschaltung auf verschiedene Durchströmungsflüssigkeiten. Helv. physiol. pharmacol. Acta.13, 191–194 (1955)
Läuger, P., Neumcke, B.: Theoretical analysis of ion conductance in lipid bilayer membranes. In: Membranes, a series of advances, Vol. 2, lipid bilayers and antibiotics. G. Eisenman, Ed. New York: Marcel Dekker 1973
McLaughlin, S., Harary, H.: Phospholipid flip-flop and the distribution of surface charges in excitable membranes. Biophys. J.14, 200–208 (1974)
McLaughlin, S., Szabo, G., Eisenman, G.: Divalent ions and the surface potential of charged phospholipid membranes. J. gen. Physiol.58, 667–687 (1971)
Mozhayeva, G. N., Naumov, A. P.: Effect of surface charge on the steady state potassium conductance of nodal membrane. Nature (Lond.)228, 164–165 (1970)
Mozhayeva, G. N., Naumov, A. P.: Tetraethylammonium ion inhibition of potassium conductance of the nodal membrane. Biochim. biophys. Acta (Amst.)290, 248–255 (1972a)
Mozhayeva, G. N., Naumov, A. P.: Effect of the surface charge on the steady potassium conductivity of the membrane of a node of Ranvier. I. Change in pH of external solution. Biophysics17, 429–439 (1972b)
Mozhayeva, G. N., Naumov, A. P.: Effect of the surface charge on the steady potassium conductivity of the membrane of a node of Ranvier. II. Change in ionic strength of the external solution. Biophysics17, 644–649 (1972c)
Mozhayeva, G. N., Naumov, A. P.: Influence of the surface charge on the steady potassium conductivity of the membrane of a node of Ranvier. III. Effect of bivalent cations. Biophysics17, 839–847 (1972d)
Muller, R. U., Finkelstein, A.: The effect of surface charge on the voltage dependent conductance induced in thin lipid membranes by monazomycin. J. gen. Physiol.60, 285–306 (1972)
Neumcke, B.: Ion flux across lipid bilayer membranes with charged surfaces. Biophysik6, 231–240 (1970)
Nonner, W.: A new voltage clamp method for Ranvier nodes. Pflügers Arch.309, 176–192 (1969)
Overbeek, J. Th. G.: The dissociation and titration constants of polybasic acids. Bull. Soc. Chim. Belg.57, 252–261 (1948)
Rojas, E., Atwater, I.: An experimental approach to determine membrane charges in squid giant axons. J. gen. Physiol.51, 131s-145s (1968)
Shrager, P., Profera, C.: Inhibition of the receptor for tetrodotoxin in nerve membranes by reagents modifying carboxyl groups. Biochim. biophys. Acta (Amst.)318, 141–146 (1973)
Stämpfli, R.: Bau und Funktion markhaltiger isolierter Nervenfasern. Ergebn. Physiol.47, 70–165 (1952)
Stämpfli, R.: Dissection of single nerve fibres and measurement of membrane potential changes of Ranvier nodes by means of the double air gap method. In: Laboratory Techniques in Membrane Biophysics. H. Passow and R. Stämpfli, Eds., Berlin-Heidelberg-New York: Springer 1969
Vogel, W.: Effect of lanthanum at the nodal membrane. Experientia (Basel)29, 1517 (1973)
Woodhull, A. M.: Ionic blockage of sodium permeability in voltage clamped frog nerve. Doctoral dissertation. University of Washington Seattle. University Microfilms, Inc. Ann Arbor, Michigan (1972)
Woodhull, A. M.: Ionic blockage of sodium channels in nerve. J. gen. Physiol.61, 687–708 (1973)
Yap, W.: Binding of ions to oligopeptides. Biophys. J.13, 1160–1165 (1973)
Author information
Authors and Affiliations
Additional information
Supported by Deutsche Forschungsgemeinschaft, Bad Godesberg—SFB 38 “Membranforschung”.
Rights and permissions
About this article
Cite this article
Drouin, H., Neumcke, B. Specific and unspecific charges at the sodium channels of the nerve membrane. Pflugers Arch. 351, 207–229 (1974). https://doi.org/10.1007/BF00586919
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00586919