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Kinetics of Channel Gating in Excitable Membranes

Published online by Cambridge University Press:  17 March 2009

L. Goldman
Affiliation:
Department of Physiology, School of Medicine, University of Maryland, Baltimore, Maryland, 21201

Extract

To a certain degree, the events underlying the action potential are understood. For each ion to which the membrane is permeable, there exists an equilibrium potential, whose physical origin is in the activity gradient for that ion. The membrane potential is then the summation of these individual ionic batteries each weighted according to the membrane permeability to that ion. In nerve fibres at rest the potassium permeability is relatively high and the membrane potential is near to the equilibrium potential for potassium. During excitation there is a transitory increase in the permeability to sodium and a slower transitory increase in the potassium permeability also. The membrane potential, therefore, temporarily moves to a value near to the sodium equilibrium potential and then returns to its resting value. Less well understood are the molecular mechanisms responsible for these selective changes in membrane permeability, i.e. how it is that a channel (pathway bywhich an ion traverses the membrane) changes its availability for ion passage as a response to a change in the membrane potential. This is the gating process.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1976

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References

REFERENCES

Adelman, W. J. & Palti, Y. (1969). The effects of external potassium and long duration voltage conditioning on the amplitude of sodium currents in the giant axon of the squid, Loligo pealei. J. gen. Physiol. 54, 589606.CrossRefGoogle ScholarPubMed
Alvarez, O., Diaz, E. & Latorre, R. (1975). Voltage-dependent conductance induced by hemocyanin in black lipid films. Biochim. biophys. Acta 389, 444–8.CrossRefGoogle ScholarPubMed
Argibay, J. A. & Hutter, O. F. (1973). Voltage-clamp experiments on the inactivation of the delayed potassium current in skeletal muscle fibres. J. Physiol., Lond. 232, 4143P.Google ScholarPubMed
Argibay, J. A., Hutter, O. F. & Slack, J. R. (1974). Consecutive activation and inactivation of the delayed rectifier in skeletal muscle fibres. J. Physiol., Lond. 237, 4647P.Google ScholarPubMed
Armstrong, C. M. (1970). Comparison of gk inactivation caused by quarternary ammonium ion with g Na inactivation. Biophys. Soc. Ann. Meet. Abstr. 10, 185a.Google Scholar
Armstrong, C. M. (1974). Ionic pores, gates, and gating currents. Q. Rev. Biophys. 7, 179209.CrossRefGoogle ScholarPubMed
Armstrong, C. M. & Bezanilla, F. (1973). Currents related to movement of the gating particles of the sodium channels. Nature, Lond. 242, 459–61.CrossRefGoogle ScholarPubMed
Armstrong, C. M. & Bezanilla, F. (1974). Charge movement associated with the opening and closing of the activation gates of the Na channels. J. gen. Physiol. 63, 533–52.CrossRefGoogle ScholarPubMed
Armstrong, C. M., Bezanilla, F. & Rojas, E. (1973). Destruction of sodium conductance inactivation in squid axon perfused with Pronase. J. gen. Physiol. 62, 375–91.CrossRefGoogle ScholarPubMed
Baumann, G. & Mueller, P. (1974). A molecular model of membrane excitability. J. Supramol. Struct. 2, 538–57.CrossRefGoogle ScholarPubMed
Begenisich, T. & Stevens, C. F. (1975). How many conductance states do potassium channels have? Biophys. J. 15, 843–6.CrossRefGoogle Scholar
Bezanilla, F. & Armstrong, C. M. (1974). Gating currents of the sodium channels: three ways to block them. Science, N.Y. 183, 753–4.CrossRefGoogle Scholar
Bezanilla, F. & Armstrong, C.M. (1975). Kinetic properties and inactivation of the gating currents of sodium channels in squid axon. Phil. Trans. R. Soc. B 270, 449–58.Google ScholarPubMed
Boheim, G. (1974). Statistical analysis of alamethicin channels in black lipid membranes. J. Membrane Biol. 19, 277303.CrossRefGoogle Scholar
Campbell, D. T. & Hille, B. (1976). Kinetic and pharmacological properties of the sodium channel of frog skeletal muscle. J. gen. Physiol. 67, 309–24.CrossRefGoogle ScholarPubMed
Chandler, W. K., Hodgkin, A. L. & Meves, H. (1965). The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons. J. Physiol., Land. 180, 821–36.CrossRefGoogle ScholarPubMed
Chandler, W. K. & Meves, H. (1965). Voltage clamp experiments on internally perfused giant axons. J. Physiol., Land. 180, 788820.CrossRefGoogle ScholarPubMed
Chandler, W. K. & Meves, H. (1970). Evidence for two types of sodium conductance in axons perfused with sodium fluoride solution. J. Physiol., Land. 211, 653–78.CrossRefGoogle ScholarPubMed
Chiu, S. Y. (1976). Observations on sodium channel inactivation in frog nerve. Biophys. J. 16, 25a.Google Scholar
Cole, K. S. (1949). Dynamic electrical characteristics of the squid axon membrane. Archs Sci. Physiol. 3, 253–8.Google Scholar
Connor, J. A. (1976). Sodium current inactivation in crustacean axons. Biophys. J. 16, 24a.Google Scholar
Dudel, J. & Rüdel, R. (1970). Voltage and time dependence of excitatory sodium current in cooled sheep Purkinje fibres. Pflügers Arch. Eur. J. Physiol. 315, 136–58.CrossRefGoogle ScholarPubMed
Ehrenstein, G. & Gilbert, D. L. (1966). Slow changes of potassium permeability in the squid giant axon. Biophys. J. 6, 553–66.CrossRefGoogle ScholarPubMed
Ehrenstein, G., Lecar, H. & Nossal, R. (1970). The nature of the negative resistance in bimolecular lipid membranes containing excitabilityinducing material. J. gen. Physiol. 55, 119–33.CrossRefGoogle ScholarPubMed
Eisenberg, M., Hall, J. E. & Mead, C. A. (1973). The nature of the voltagedependent conductance induced by alamethicin in black lipid membranes. J. Membrane Biol. 14, 143–76.CrossRefGoogle ScholarPubMed
Fishman, H. M., Moore, L. E., Poussart, D. J. M. & Siebenga, E. (1976). Non first order K+ conduction impedance and noise feature in squid axon membrane. Biophys. J. 16, 26a.Google Scholar
Fozzard, H. A. & Hiraoka, M. (1973). The positive dynamic current and its inactivation properties in cardiac Purkinje fibres. J. Physiol., Land. 234, 569–86.CrossRefGoogle ScholarPubMed
Frankenhaeuser, B. (1963 a). A quantitative description of potassium currents in myelinated nerve fibres of Xenopus laevis. J. Physiol., Land. 169, 424–30.CrossRefGoogle ScholarPubMed
Frankenhaeuser, B. (1963 b). Inactivation of the sodium carrying mechanism in myelinated nerve fibres of Xenopus laevis. J. Physiol, Lond. 169, 445–51.CrossRefGoogle ScholarPubMed
Frankenhaeuser, B. & Hodgkin, A. L. (1957). The action of calcium on the electrical properties of squid axons. J. Physiol., Land. 137, 218–44.CrossRefGoogle ScholarPubMed
Gettes, L. S. & Reuter, H. (1974). Slow recovery from inactivation of inward currents in mammalian myocardial fibres. J. Physiol., Land. 240, 703–24.CrossRefGoogle ScholarPubMed
Goldman, D. E. (1964). A molecular structural basis for the excitation properties of axons. Biaphys. J. 4, 1688.Google Scholar
Goldman, L. (1975 a). Pronase and models for the sodium conductance. J. gen. Physiol. 65, 551–2.CrossRefGoogle ScholarPubMed
Goldman, L. (1975 b). Quantitative description of the sodium conductance of the giant axon of Myxicola in terms of a generalized second-order variable. Biophys. J. 15, 119–36.CrossRefGoogle ScholarPubMed
Goldman, L. & Hahin, R. (1975). Interpretation of a coupled activation– inactivation model for the g Na. Abstr. 5th Internat. Biophys. Cong., Copenhagen. I.U.P.A.B. 119.Google Scholar
Goldman, L. & Schauf, C. L. (1972). Inactivation of the sodium current in Myxicola giant axons; evidence for coupling to the activation process. J. gen. Physiol. 59, 659–75.CrossRefGoogle Scholar
Goldman, L. & Schauf, C. L. (1973). Quantitative description of sodium and potassium currents and computed action potentials in Myxicola giant axons. J. gen. Physiol. 61, 361-84.CrossRefGoogle ScholarPubMed
Gordon, L. G. M. & Haydon, D. A. (1972). The unit conductance channel of alamethicin. Biochim. biophys. Acta 255, 1014–18.CrossRefGoogle Scholar
Gotoh, H. (1975). A model of the activation process of Na+ conductance in the squid axon: an approach with interactive desorption kinetics of divalent cations. J. theor. Biol. 53, 309–25.CrossRefGoogle Scholar
Haas, H. G., Kern, R., Benninger, C. & Einwächter, H. M. (1975). Effects of prenylamine on cardiac membrane currents and contractility. J. Pharmacol. exp. Ther. 192, 688701.Google ScholarPubMed
Haas, H. G., Kern, R., Einwächter, H. M. & Tarr, M. (1971). Kinetics of Na inactivation in frog atria. Pflüger's Arch. Eur. J. Physiol. 323, 141–57.CrossRefGoogle ScholarPubMed
Hahin, R. & Goldman, L. (1975). Unpublished computations.Google Scholar
Hodgkin, A. L. & Huxley, A. F. (1952 a). Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J. Physiol, Lond. 116, 449–72.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Huxley, A. F. (1952 b). The components of membrane conductance in the giant axon of Loligo. J. Physiol, Lond. 116, 473–96.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Huxley, A. F. (1952 c). The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J. Physiol., Lond. 116, 497506.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Huxley, A. F. (1952 d). A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol., Lond. 117, 500–44.CrossRefGoogle ScholarPubMed
Hodgkin, A. L., Huxley, A. F. & Katz, B. (1952). Measurements of current– voltage relations in the membrane of the giant axon of Loligo. J. Physiol., Land. 116, 424–48.CrossRefGoogle ScholarPubMed
Hoyt, R. C. (1963). The squid giant axon. Mathematical models. Biophys. J. 3, 339431.CrossRefGoogle ScholarPubMed
Hoyt, R. C. (1968). Sodium inactivation in nerve fibres. Biophys. J. 8, 1074–97.CrossRefGoogle Scholar
Hoyt, R. C. (1976). A three state coupled model for the sodium channel in nerve fibers. (To be published.)Google Scholar
Hoyt, R. C. & Adelman, W. J. (1970). Sodium inactivation. Experimental test of two models. Biophys. J. 10, 610–17.CrossRefGoogle ScholarPubMed
Jakousson, E. (1976 a). An assessment of a coupled three-state kinetic model for sodium conductance changes. Biophys. J. 16, 291302.CrossRefGoogle Scholar
Jakobsson, E. (1976 b). Fully coupled transient excited state model for the sodium channel. Biophys. J. 16, 78a.Google Scholar
Keynes, R. D. (1975 a). The ionic channels in excitable membranes. In Energy Transformation in Biological Systems. Ciba Foundation Symposium 31, pp. 191203. Amsterdam.CrossRefGoogle Scholar
Keynes, R. D. (1975 b). The organization of the ionic channels in nerve membranes. In The Nervous System. Vol. I. The Basic Neurosciences (ed. Tower, D. B.), pp. 165–75. New York: Raven Press.Google Scholar
Keynes, R. D. & Rojas, E. (1973). Characteristics of sodium gating currents in the squid giant axon. J. Physiol, Lond. 233, 2830P.Google ScholarPubMed
Keynes, R. D. & Rojas, E.Kinetics and steady-state properties of the charged system controlling sodium conductance in the squid giant axon. J. Physiol, Lond. 239, 393434.CrossRefGoogle Scholar
Keynes, R. D. & 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, Lond. 255, 157–90.CrossRefGoogle ScholarPubMed
McLaughlin, S. & Eisenberg, M. (1975). Antibiotics and membrane biology. A. Rev. Biophys. Bioeng. 4, 335–66.CrossRefGoogle ScholarPubMed
Meves, H. (1974). The effect of holding potential on the asymmetry currents in squid giant axons. J. Physiol., Land. 243, 847–67.CrossRefGoogle Scholar
Meves, H. (1975). Asymmetry currents in intracellularly perfused squid giant axons. Phil. Trans. R. Soc. B 270, 493500.Google ScholarPubMed
Moore, J. W. (1976). Unpublished data.Google Scholar
Moore, J. W. & Cox, E. B. (1976). A kinetic model for the sodium conductance system in squid axon. Biophys. J. 16, 171–92.CrossRefGoogle ScholarPubMed
Moore, L. E. & Jakobsson, E. (1971). Interpretation of the sodium permeability changes of myelinated nerve in terms of linear relaxation theory. J. theor. Biol. 33, 7789.CrossRefGoogle ScholarPubMed
Mueller, P. (1975 a). Membrane excitation through voltage-induced aggregation of channel precursors. Ann. N. Y. Acad. Sci. 264, 247–64.CrossRefGoogle ScholarPubMed
Mueller, P. (1975 b). Electrical excitability in bilayers and cell membranes. In International Review of Science, Biochemistry Series: Energy Transducing Mechanisms (ed. Racker, E.), pp. 75120. London: Butterworths Press.Google Scholar
Mueller, P. & Rudin, D. O. (1968). Action potentials induced in bimolecular lipid membranes. Nature, Land. 217, 713–19.CrossRefGoogle Scholar
Mueller, P., Rudin, D. O., Tien, H. T. & Wescott, W. C. (1962). Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature, Lond. 194, 979–80.CrossRefGoogle ScholarPubMed
Muller, R. U. & Finkelstein, A. (1972). Voltage-dependent conductance induced in thin lipid membranes by monazomycin. J. gen. Physiol. 60, 263–84.CrossRefGoogle ScholarPubMed
Mullins, L. J. (1959). An analysis of conductance changes in squid axon. J. gen. Physiol. 42, 1013–35.CrossRefGoogle ScholarPubMed
Nonner, W., Rojas, E. & Stämpfli, R. (1975). Gating currents in the node of Ranvier. Phil. Trans. R. Soc. B 270, 483–92.Google ScholarPubMed
Oxford, G. S. & Pooler, J. P. (1975). Selective modification of sodium channel gating in lobster axons by 2, 4, 6-trinitrophenol; evidence for two inactivation mechanisms. J. gen. Physiol. 66, 765–80.CrossRefGoogle ScholarPubMed
Palti, Y., Ganot, G. & Stämpfli, R. (1976). Effect of conditioning potential on potassium current kinetics in the frog node. Biophys. J. 16, 261–74.CrossRefGoogle ScholarPubMed
Peganov, E. M. (1973). Kinetics of sodium channel inactivation in the frog Ranvier node. Bull. exp. Biol. Med. 76, 59.CrossRefGoogle Scholar
Peganov, E. M., Khodorov, B. I. & Shishkova, L. D. (1973). Slow sodium inactivation in the Ranvier node membrane; role of external potassium. Bull. Exp. Biol. Med. 76, 1519.CrossRefGoogle ScholarPubMed
Peganov, E. M., Timin, E. N. & Khodorov, B. I. (1973). The link between sodium activation and inactivation. Bull. Exp. Biol. Med. 76, 711CrossRefGoogle Scholar
Ramón, F., Anderson, N., Joyner, R. W. & Moore, J. W. (1975). Axon voltage clamp simulations. IV. A multicellular preparation. Biophys. J. 15, 5570.CrossRefGoogle Scholar
Rojas, E. & Keynes, R. D. (1975). On the relation between displacement currents and activation of the sodium conductance in the squid giant axon. Phil. Trans. R. Soc. B 270, 459–82.Google ScholarPubMed
Rudy, B. (1975). Slow recovery of the inactivation of sodium conductance in Myxicola giant axons. J. Physiol, Lond. 249, 2224P.Google ScholarPubMed
Rudy, B. (1976 a). Sodium gating currents in Myxicola giant axons. (To be published.)Google Scholar
Rudy, B. (1976 b). Unpublished data.Google Scholar
Schauf, C. L. (1974). Sodium currents in Myxicola axons; non exponential recovery from the inactive state. Biophys. J. 14, 151–4.CrossRefGoogle Scholar
Schauf, C. L. (1976). Comparison of two-pulse sodium inactivation with reactivation in Myxicola giant axons. Biophys. J. 16, 245–8.CrossRefGoogle ScholarPubMed
Schauf, C. L. & Davis, F. Q. (1975). Further studies of activation–inactivation coupling in Myxicola axons. Insensitivity to changes in calcium concentration. Biophys. J. 15, 1111–16.CrossRefGoogle ScholarPubMed
Trautwein, W. (1973). Membrane currents in cardiac muscle fibers. Physiol. Rev. 53, 793835.CrossRefGoogle Scholar
Tredgold, R. H. (1973). A possible mechanism for the negative resistance characteristic of axon membranes. Nature (New Biol.) 242, 209–10.CrossRefGoogle ScholarPubMed
Ulbricht, W. (1974). Ionic channels through the axon membrane (a review). Biophys. Str. Mech. I, 116.Google Scholar
Ulbricht, W. & Wagner, H. H. (1975). The influence of pH on equilibrium effects of tetrodotoxin on myelinated nerve fibres of Rana esculenta. J. Physiol., Lond. 252, 159–84.CrossRefGoogle ScholarPubMed