Hostname: page-component-5b777bbd6c-skqgd Total loading time: 0 Render date: 2025-06-24T02:07:19.073Z Has data issue: false hasContentIssue false
  • English
  • Français

Ionic pores, gates, and gating currents

Published online by Cambridge University Press:  17 March 2009

Clay M. Armstrong
Clay M. Armstrong
Affiliation:
University of Rochester, School of Medicine and Dentistry, 260, Crittenden, Rochester, New York 14642
Get access Rights & Permissions [Opens in a new window]

Extract

The current phase of axon physiology began with the invention of the voltage clamp by Cole (1949) and its use by Hodgkin & Huxley (1952d) to produce an astonishingly complete analysis of the ionic permeabilities that are responsible for the action potential. Their description did notcontain much in the way of molecular detail, and left open such questions as whether ions cross the membrane by way of pores or carriers, and the nature of the ‘gating‘ processes that increase ordecrease ion permeability in response to changes of the membrane potential. In the last few years our picture of the ionicchannels has grown considerably more tangible, though it still falls far short of a detailed molecular description. This article describes this sharpened picture and reviews the evidence for it. The viewpoint expressed is a very personal one, andno attempt has been made to review the literature of axonology comprehensively.

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 7 , Issue 2 , May 1974 , pp. 179 - 209
Copyright
Copyright © Cambridge University Press 1974

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Adelman, W. J. & Senft, J. P. (1968). Dynamic asymmetries in the squid axon membrane. J. gen. Physiol. 51, 102–14s.CrossRefGoogle ScholarPubMed
Anderson, C. R. & Stevens, C. F. (1973). Voltage-clamp analysis of acetylcholine produced fluctuations at frog neuromuscular junction. J. Physiol., Lond. 235, 655–691.CrossRefGoogle ScholarPubMed
Armstrong, C. M. (1966). Time course of TEA+induced anomalous rectification in squid giant axon. J. gen. Physiol. 50, 491–503.CrossRefGoogle Scholar
Armstrong, C. M. (1969). Inactivation of the potassium conductance and related phenomena caused by quaternary ammonium ion injected in squid axon. J. gen. Physiol. 54, 553–75.CrossRefGoogle Scholar
Armstrong, C. M. (1970). Comparison of g K inactivation caused by quaternary ammonium ion with g Na inactivation. Biophys. Soc. Ann. Meet. Abstr. 10, 185 a.Google Scholar
Armstrong, C. M. (1971). Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons. J. gen. Physiol. 58, 413–37.CrossRefGoogle ScholarPubMed
Armstrong, C. M. (1974). K pores of nerve and muscle membrane. In Membranes: A Series of Advances, vol. 3 (ed. Eisenman, G.). New York: Marcel Dekker.Google Scholar
Armstrong, C. M. & Bezanilla, F. (1973 a). Properties of gating currents of sodium channels. Biol. Bull. mar. biol. Lab., Woods Hole 145, 423.Google Scholar
Armstrong, C. M. & Bezanilla, F. (1973 b). Currents related to the movement of gating particles of the sodium channels. Nature, Lond. 242, 459–61.CrossRefGoogle Scholar
Armstrong, C. M., Bezanilla, F. M. & Horowicz, P. (1972). Twitches in the presence of ethylene-glycol bis (β-aminoethyl ether)-N, N'-tetraacetic acid. Biochim. biophys. Acta 267, 605–8.CrossRefGoogle Scholar
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
Armstrong, C. M. & Binstock, L. (1965). Anomalous rectification in the squid giant axon injected with tetraethylammonium chloride. J. gen. Physiol. 48, 859–72.CrossRefGoogle ScholarPubMed
Armstrong, C. M. & Hille, B. (1972). The inner quaternary ammonium ion receptor in potassium channels of node of Ranvier. J. gen. Physiol. 59, 388–400.CrossRefGoogle ScholarPubMed
Baker, P. F., Hodgkin, A. L. & Ridgway, E. B. (1971). Depolarization and calciumentry in squid giant axon. J. Physiol., Lond. 218, 709–55.CrossRefGoogle Scholar
Begenisich, T. & Lynch, C. (1973). Reversible blockage of ionic currents by internal Zn. Biol. Bull. mar. biol. Lab., Woods Hole 145, 424.Google Scholar
Bergman, C. (1970). Increase of sodium concentration near the inner surface of nodal membrane. Pfüuger's Arch. Eur. J. Physiol. 317, 287–302.CrossRefGoogle ScholarPubMed
Bezanilla, F. & Armstrong, C. M. (1972). Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axon. J. gen. Physiol. 60, 588–608.CrossRefGoogle Scholar
Bezanilla, F. & Armstrong, C. M. (1973). Unpublished data.Google Scholar
Bezanilla, F. & Armstrong, C. M. (1974.). Gating currents of the sodium channels: three waysto block them. Science, N. Y. (In the Press.)CrossRefGoogle Scholar
Ciani, S., Eisenman, G. & Szabo, G. (1969). A theory for the effects of neutral carriers such as the macrotetralide actin antibiotics on electrical properties of bilayer membranes. J. molec. Biol. I, 1–36.Google Scholar
Cohen, L. B., Keynes, D. & Landowne, D. (1972). Changes in axon light scatteringthat accompany the action potential: current dependent component. J. Physiol., Lond. 224, 727–52.CrossRefGoogle Scholar
Cohen, L. B., Hille, B. & Keynes, R. D. (1970). Changes in axon birefringence during action potential. J. Physiol., Lond. 211, 495–515.CrossRefGoogle ScholarPubMed
Cole, K. S.Dynamic electrical characteristics of the squid axon membrane. Archs. Sci. Physiol. 3, 253–8.Google Scholar
Colquhoun, D. R., Henderson, R. & Ritchie, J. M. (1972). The binding of tetrodotoxin to non-myelinated nerve fibers. J. Physiol., Lond. 227, 95–125.CrossRefGoogle Scholar
Davila, H. V., Salzberg, B. M. & Cohen, L. B. (1972). Changes of fluorescence ofsquid axon during activity. Biol. Bull. mar. biol. Lab., Woods Hole 143, 457.Google Scholar
Davila, H. V., Salzberg, B. M. & Cohen, L. B. (1973). Use of fluorescent merocyanine dye for measuring axon membrane potential. Nature New Biol. 241, 159–60.CrossRefGoogle Scholar
Diamond, J. M. & Wright, E. M. (1969). Biological membranes: The physical basis of ion and nonelectrolyte selectivity. A. Rev. Physiol. 31, 581–646.CrossRefGoogle ScholarPubMed
Eisenman, G. (1962). Cation selective glass electrodes and their mode of operation. Biophys. J. 2, 259–323s.CrossRefGoogle ScholarPubMed
Fishman, H. S. (1972). Excess noise from small patches of squid axon membrane. Biophys. Soc. Ann. Meet. Abst. 12, 119.Google Scholar
Fishman, H. S. (1973). Relaxation spectra of potassium channel noise from squid axon membranes. Proc. natn. Acad. Sci. (U.S.A.) 70, 876–9.CrossRefGoogle ScholarPubMed
Frankenhaeuser, B. & Hodgkin, A. L. (1957). The action of calcium on electrical properties of squid axon. J. Physiol., Lond. 137, 218–44.CrossRefGoogle Scholar
Frankenhabuser, B. & Moore, L. E. (1963). The effect of temperature on the sodium and potassium permeability changes in myelinated fibers of Xenopus laevis. J. Physiol., Lond. 169, 431–7.CrossRefGoogle Scholar
Goldman, L. & Schauf, C. L. (1972). Inactivation of the sodium current in myxicola giantaxons. J. gen. Physiol. 59,659–75CrossRefGoogle Scholar
Hagiwara, S. & Saito, N. (1959). Voltage-current relationships in nerve cell membranes of Onchidium verruculatum. J. Physiol., Lond. 148, 161–79.CrossRefGoogle Scholar
Hille, B. (1966). Common mode of action of three agents that decrease the transient change in sodiumpermeability in nerves. Nature, Lond. 210, 1220–2.CrossRefGoogle Scholar
Hille, B. (1970). Ionic channels in nerve membranes. prog. Biophys. & Mol. Biol. 21, 1–32.CrossRefGoogle ScholarPubMed
Hille, B. (1967). The selective inhibition of delayed potassium currents in nerves by tetraethylammonium ions. J. gen. Physiol. 50, 1287–302.CrossRefGoogle Scholar
Hille, B. (1971). The permeability of sodium channels to organic cations in myelinated nerves. J. gen. Physiol. 58, 599–619.CrossRefGoogle Scholar
Hille, B. (1972). The permeability of sodium channels to metal cations in myelinated nerves. J. gen. Physiol. 59, 637–58.CrossRefGoogle Scholar
Hille, B. (1973). Potassium channels in myelinated nerves. J. gen. Physiol. 61,669–86.CrossRefGoogle Scholar
Hladky, S. B. & Haydon, D. A. (1970). Discreteness of conductance change in biomolecularlipid membranes in the presence of certain antibiotics. Nature, Lond. 225, 451–3.CrossRefGoogle ScholarPubMed
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 inthe giant axon of Loligo. J. Physiol., Lond. 116, 473–96.CrossRefGoogle Scholar
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, 497–506.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Huxley, A. F. (1952 d). A quantitative description of membrane current and its application to conductance and excitation in nerve. J. Physiol., Lond. 117, 500–44.CrossRefGoogle ScholarPubMed
Hodgkin, A. L., Huxley, A. F. & Katz, B. (1952). Measurements of current voltagerelations in the membrane of the giant axon of Loligo. J. Physiol., Lond. 116, 424–48.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Keynes, R. D. (1955). The potassium permeability of a giant nerve fibre. J. Physiol., Lond. 128, 61–88.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Keynes, R. D. (1957). Movements of labelled calcium in squid giant axon. J. Physiol., Lond. 138, 253–81.CrossRefGoogle Scholar
Horowicz, P., Gage, P. W. & Eisenberg, R. S. (1968). The role of electrochemicalgradient in determining potassium fluxes in frog striated muscle. J. gen. Physiol. 51, 193–203S.CrossRefGoogle ScholarPubMed
Hoyt, R. C. (1968). Sodium inactivation in nerve fibers. Biophys. J. 8, 1074–97.CrossRefGoogle ScholarPubMed
Katz, & Miledi, (1972). The statistical nature of the acetyicholine potential and its molecular components. J. Physiol., Lond. 224, 665–699.CrossRefGoogle Scholar
Keynes, R. D., Ritchie, J. M. & Rojas, E. (1971). The binding of tetrodotoxin to nerve membranes. J. Physiol. 213, 235–54.CrossRefGoogle ScholarPubMed
Keynes, R. D. & Rojas, E. (1973). Characteristics of sodium gating currents in the squidgiant axon. J. Physiol. 233, 28–30P.Google ScholarPubMed
Keynes, R. D., Rojas, E. & Taylor, R. E. (1973). Saxitoxin, tetrodotoxin barriers and binding sites in squid giant axon. J. gen. Physiol. 6, 267.Google Scholar
Kilbourn, B. T., Dunitz, J. D., Dioda, L. A. & Simon, W. (1967). Structure of the K+ complex with nonactin a macrotetralide antibiotic possessing highly specific K+ transport properties. J. Molec. Biol. 30, 559–63.CrossRefGoogle Scholar
Krasne, S., Eisenman, G. & Szabo, G. (1971). Freezing and melting of lipid bilayers and the mode of action of nonactin, valinomycin, and grarnicidin. Science, N.Y. 174, 412–15.CrossRefGoogle Scholar
Laüger, P. (1972). Carrier-mediated ion transport. Science, N.Y. 178, 24–30.CrossRefGoogle ScholarPubMed
Moora, J. W., Narahashi, T. & Shaw, T. I. (1967). An upper limit to the number of sodium channels in nerve membrane? J. Physiol., Lond. 188, 99–105.CrossRefGoogle Scholar
Mullins, L. J. (1959). An analysis of conductance changes in squid axon. J. gen. Physiol. 42, 1013–35.CrossRefGoogle ScholarPubMed
Mullins, L. J. (1968). A single channel or a dual channel mechanism for nerve excitation. J. gen. Physiol. 52, 550–3.CrossRefGoogle ScholarPubMed
Narahashi, T., Moore, J. W. & Scott, W. R. (1964). Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J. gen. Physiol. 47, 965–74.CrossRefGoogle ScholarPubMed
Parsegian, A. (1969). Energy of an ion crossing a low dielectric membrane: Solutions to four relevant electrostatic problems. Nature, Lond. 221, 844–6.CrossRefGoogle Scholar
Poussart, D. J. M. (1971). Membrane current noise in lobster axon under voltage clamp. Biophys. J. II, 211–34.CrossRefGoogle Scholar
Siebenga, E. A., Meyer, W. A. & Verveen, A. A. (1973). Membrane shot-noise in electrically depolarized nodes of Ranvier. Pflüger's Arch. Eur. J. Physiol. 341, 87–96.CrossRefGoogle ScholarPubMed
Strichartz, G. R. (1973). The inhibition of sodium currents in myelinated nerve by quaternary derivatives of lidocaine. J. gen. Physiol. 62, 37–57.CrossRefGoogle ScholarPubMed
Tasaki, I. & Hagiwara, S. (1957). Demonstration of two stable potential states in squid giant axon under tetraethylammonium chloride. J. gen.Physiol. 40, 851–85.CrossRefGoogle ScholarPubMed
Urry, D. W. (1971). The gramicidin A transmembrane channel: A proposed π(L, D) helix. Proc. natn. Acad. Sci. U.S.A. 68, 672–6.CrossRefGoogle Scholar
Urry, D. W. (1972). A molecular theory of ion-conducting channels: A field dependent transition between conducting and non-conducting conformations. Proc. natn. Acad. Sci. U.S.A. 69, 1610–14.CrossRefGoogle Scholar
Verveen, A. A. & Derksen, H. E. (1968). Fluctuation phenomena in nerve membrane. Proc. IEEE 56, 906–16.CrossRefGoogle Scholar
Winkler, R. (1969). Kinetik und Mechanismus der Alkali-und Erdalkalimetalkomplexbildung in Methanol. Ph.D. Dissertation, Göttingen— Wien.Google Scholar
Woodhull, A. M. (1973). Ionic blockage of sodium channels in nerve. J. gen. Physiol. 61, 687–708.CrossRefGoogle ScholarPubMed