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Quantal charge redistributions accompanying the structural transitions of sodium channels

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Abstract

Asymmetric displacement currents, Ig, associated with the gating of nerve sodium channels have been recorded in cell-attached macropatches of Xenopus laevis oocytes injected with exogenous mRNA coding for rat-brain-II sodium channels. The Ig properties were found to be similar to those of gating currents previously observed in native nerve preparations. Ig fluctuations were measured in order to ascertain the discreteness of the conformational changes which precede the channel opening. The autocorrelation of the fluctuations is consistent with a shot-like character of the elementary Ig contributions. The variance of the fluctuations indicates that most of the gating-charge movement that accompanies the activation of a single sodium channel occurs in 2 to 3 brief packets, each carrying an equivalent of about 2.3 electron charges.

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References

  • Aldrich RW, Corey DP, Stevens CF (1983) A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature 306:436–441

    Article  CAS  Google Scholar 

  • Armstrong CM, Bezanilla F (1974) Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol 63:533–552

    Article  CAS  Google Scholar 

  • Armstrong CM, Bezanilla F (1977) Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol 70:567–590

    Article  CAS  Google Scholar 

  • Conti F (1986) The relationship betwen electrophysiological data and thermodynamics of ion channel conformations. Neurol Neurobiol 20:25–41

    CAS  Google Scholar 

  • Conti F, Stühmer W (1988) Gating currents and their fluctuations in sodium channels expressed in Xenopus oocytes after injection of exogenous mRNA. 11th Annual Meeting of the European Neuroscience Association

  • Conti F, Palmieri G (1968) Nerve fiber behaviour in heavy water under voltage-clamp. Biophysik 5:71–77

    Article  CAS  Google Scholar 

  • Conti F, Wanke E (1975) Channel noise in nerve membranes and lipid bilayers. Q Rev Biophys 8:451–506

    Article  CAS  Google Scholar 

  • Conti F, DeFelice LJ, Wanke E (1975) Potassium and sodium ion current noise in the membrane of the squid giant axon. J Physiol (London) 248:45–82

    Article  CAS  Google Scholar 

  • Conti F, Neumcke B, Nonner W, Stämpfli R (1980) Conductance fluctuations from the inactivation process of sodium channels in myelinated nerve fibres. J Physiol (London) 308:217–239

    Article  CAS  Google Scholar 

  • Conti F, Inoue I, Kukita F, Stühmer W (1984) Pressure dependence of sodium gating currents in the squid giant axon. Eur Biophys J 11:137–147

    Article  CAS  Google Scholar 

  • DeFelice LJ (1981) Introduction to membrane noise. Plenum Press, New York

    Book  Google Scholar 

  • Dubois JM, Schneider MF (1982) Kinetics of intramembrane charge movement and sodium current in frog node of Ranvier. J Gen Physiol 79:571–602

    Article  CAS  Google Scholar 

  • Edmonds DT (1987) A comparison of sodium channel kinetics in the squid axon, the frog node and the frog node with BTX using the “silent gate‘ model. Eur Biophys J 15:27–33

    Article  CAS  Google Scholar 

  • FitzHugh R (1965) A kinetic model of the conductance changes in nerve membrane. J Cell Comp Physiol 66:111–118

    Article  CAS  Google Scholar 

  • French RJ, Horn R (1983) Sodium channel gating: models, mimics, and modifiers. Annu Rev Biophys Bioeng 12:319–356

    Article  CAS  Google Scholar 

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100

    Article  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol (London) 117:500–544

    Article  CAS  Google Scholar 

  • Horn R, Vandenberg CA (1984) Statistical properties of single sodium channels. J Gen Physiol 84:505–534

    Article  CAS  Google Scholar 

  • Katz B, Miledi R (1970) Membrane noise produced by acetylcholine. Nature 226:962–963

    Article  CAS  Google Scholar 

  • Keynes RD (1983) Voltage-gated ion channels in the nerve membrane. Proc R Soc Lond B220:1–30

    Article  CAS  Google Scholar 

  • Keynes RD, Rojas E (1976) The temporal and steady-state relationships between activation of the sodium conductance and movement of the gating particles in the squid giant axon. J Physiol 255:157–189

    Article  CAS  Google Scholar 

  • Methfessel C, Witzemann V, Takahashi T, Mishina M, Numa S, Sakmann B (1986) Patch clamp measurements on Xenopus laevis oocytes: currents through endogenous channels and implanted acetylcholine receptor and sodium channels. Pflügers Arch 407:577–588

    Article  CAS  Google Scholar 

  • Meves H (1974) The effect of holding potential on the asymmetry currents in squid giant axons. J Physiol (London) 243:847–867

    Article  CAS  Google Scholar 

  • Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260:799–802

    Article  CAS  Google Scholar 

  • Neher E, Stevens CA (1977) Conductance fluctuation and ionic prores in membranes. Annu Rev Biophys Bioeng 6:345–381

    Article  CAS  Google Scholar 

  • Neumcke B, Nonner W, Stämpfli R (1976) Asymmetrical displacement current and its relation of the activation of sodium current in the membrane of frog myelinated nerve. Pflügers Arch 363:193–203

    Article  CAS  Google Scholar 

  • Noda M, Ikeda T, Suzuki H, Takeshima H, Kuno M, Numa S (1986) Expression of functional sodium channels from cloned cDNA. Nature 322:826–828

    Article  CAS  Google Scholar 

  • Schauf CL, Bullock JO (1979) Modifications of sodium channel gating in Myxicola giant axons by deuterium oxide, temperature, and internal cations. Biophys J 27:193–208

    Article  CAS  Google Scholar 

  • Schottky W (1918) Über spontane Stromschwankungen in verschiedenen Elektrizitätsleitern. Ann Phys 57:541–567

    Article  Google Scholar 

  • Schwarz G (1978) On the physico-chemical basis of voltage-dependent molecular gating mechanisms in biological membranes. J Membr Biol 43:127–148

    Article  CAS  Google Scholar 

  • Sigworth FJ (1977) Sodium channels in nerve apparently have two conductance states. Nature 270:265–267

    Article  CAS  Google Scholar 

  • Stimers JR, Bezanilla F, Taylor RE (1985) Sodium channel activation in the squid giant axon. Steady state properties. J Gen Physiol 85:65–82

    Article  CAS  Google Scholar 

  • Stühmer W, Methfessel C, Sakmann B, Noda M, Numa S (1987) Patch clamp characterization of sodium channels expressed from rat brain cDNA. Eur Biophys J 14:131–138

    Article  Google Scholar 

  • Stühmer W, Conti F, Suzuki H, Wang X, Noda M, Yahagi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature (in press)

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Authors and Affiliations

  1. Istituto di Cibernetica e Biofisica, CNR, I-16146, Genova, Italy

    F. Conti

  2. Abteilung Membranbiophysik, Max-Planck-Institut für biophysikalische Chemie, Am Fassberg, D-3400, Göttingen, Germany

    W. Stühmer

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  1. F. Conti
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  2. W. Stühmer
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Conti, F., Stühmer, W. Quantal charge redistributions accompanying the structural transitions of sodium channels. Eur Biophys J 17, 53–59 (1989). https://doi.org/10.1007/BF00257102

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  • DOI: https://doi.org/10.1007/BF00257102

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