Gating of Channels in Nerve and Muscie: A Stochastic Approach

Publisher Summary Gating is the process that underlies the opening and closing of channels. This simplistic view suggests that channels are merely rigid pores, which can be opened and closed by a gate. It is becoming apparent, however, that open channels are not necessarily rigid pores, and that gating processes, when fast enough, cannot be distinguished from open channel properties. In spite of this ambiguity, channels often appear to open and close in discrete jumps. This chapter addresses some of the experimental and theoretical details of this process. Several aspects of gating are common to most, if not all, types of ionic channels. The general properties of the gating of single channels are discussed in the chapter. One might imagine that a channel opens slowly as it undergoes a conformational change from a resting to an activated state. For example, a “gate” could open in tiny increments, with the conductance of the single channel increasing in tiny increments. Alternatively, a channel could flip suddenly into and out of a conducting state. Choosing the correct alternative requires single-channel recording; noise measurements alone cannot do it. Stochastic representations of channel gating and experimental findings are discussed in the chapter.

[1]  Frederick Sachs,et al.  Single ionic channels observed in tissue-cultured muscle , 1979, Nature.

[2]  R Horn,et al.  Statistical analysis of single sodium channels. Effects of N-bromoacetamide. , 1984, Biophysical journal.

[3]  A G Hawkes,et al.  Relaxation and fluctuations of membrane currents that flow through drug-operated channels , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  C F Stevens,et al.  An analysis of the dose‐response relationship at voltage‐clamped frog neuromuscular junctions. , 1978, The Journal of physiology.

[5]  R. Horn,et al.  Acetylcholine-induced current in perfused rat myoballs , 1980, The Journal of general physiology.

[6]  E Neher,et al.  Sodium and calcium channels in bovine chromaffin cells , 1982, The Journal of physiology.

[7]  E Wanke,et al.  Channel noise in nerve membranes and lipid bilayers , 1975, Quarterly Reviews of Biophysics.

[8]  L. Byerly,et al.  Voltage‐clamp analysis of the potassium current that produces a negative‐going action potential in Ascaris muscle. , 1979, The Journal of physiology.

[9]  W Schwarz,et al.  Ca2+-activated K+ channels in erythrocytes and excitable cells. , 1983, Annual review of physiology.

[10]  T. Dwyer,et al.  Block of endplate channels by permeant cations in frog skeletal muscle , 1981, The Journal of general physiology.

[11]  M. D. Leibowitz,et al.  Acetylcholine receptor kinetics. A description from single-channel currents at snake neuromuscular junctions. , 1982, Biophysical journal.

[12]  J P Changeux,et al.  Fast kinetic studies on the interaction of a fluorescent agonist with the membrane-bound acetylcholine receptor from Torpedo marmorata. , 1979, European journal of biochemistry.

[13]  R. Latorre,et al.  Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Hawkes,et al.  On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  Gary Yellen,et al.  Single Ca2+-activated nonselective cation channels in neuroblastoma , 1982, Nature.

[16]  B. Sakmann,et al.  Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells , 1981, Nature.

[17]  A. Hawkes,et al.  On the stochastic properties of single ion channels , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  R. Kado,et al.  Sodium channels induced by depolarization of the Xenopus laevis oocyte. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R Horn,et al.  Estimating kinetic constants from single channel data. , 1983, Biophysical journal.

[20]  B. Sakmann,et al.  Fluctuations in the microsecond time range of the current through single acetylcholine receptor ion channels , 1981, Nature.

[21]  S. Hagiwara,et al.  Studies of calcium channels in rat clonal pituitary cells with patch electrode voltage clamp , 1982, The Journal of physiology.

[22]  M B Jackson,et al.  Successive openings of the same acetylcholine receptor channel are correlated in open time. , 1983, Biophysical journal.

[23]  H. Meves Inactivation of the sodium permeability in squid giant nerve fibres. , 1978, Progress in biophysics and molecular biology.

[24]  R. Latorre,et al.  Kinetics of Ca2+-activated K+ channels from rabbit muscle incorporated into planar bilayers. Evidence for a Ca2+ and Ba2+ blockade , 1983, The Journal of general physiology.

[25]  Y. Fukushima,et al.  Blocking kinetics of the anomalous potassium rectifier of tunicate egg studied by single channel recording , 1982, The Journal of physiology.

[26]  R. Keynes,et al.  Fractionation of the asymmetry current in the squid giant axon into inactivating and non-inactivating components , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  C F Stevens,et al.  Inferences about membrane properties from electrical noise measurements. , 1972, Biophysical journal.

[28]  E Neher,et al.  Conductance fluctuations and ionic pores in membranes. , 1977, Annual review of biophysics and bioengineering.

[29]  J. Castillo,et al.  Hyperpolarizing Action Potentials recorded from the Œsophagus of Ascaris lumbricoides , 1964, Nature.

[30]  Alan G. Hawkes,et al.  The Principles of the Stochastic Interpretation of Ion-Channel Mechanisms , 1983 .

[31]  K L Magleby,et al.  Properties of single calcium‐activated potassium channels in cultured rat muscle , 1982, The Journal of physiology.

[32]  Y. Fukushima Identification and kinetic properties of the current through a single Na+ channel. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. Horn,et al.  Effect of protein cross-linking reagents on membrane currents of squid axon. , 1980, The American journal of physiology.

[34]  A. Auerbach,et al.  Flickering of a nicotinic ion channel to a subconductance state. , 1983, Biophysical journal.

[35]  A. Hodgkin,et al.  The action of calcium on the electrical properties of squid axons , 1957, The Journal of physiology.

[36]  P. Gage,et al.  Effects of permeant monovalent cations on end‐plate channels. , 1979, The Journal of physiology.

[37]  C. F. Stevens,et al.  A reinterpretation of mammalian sodium channel gating based on single channel recording , 1983, Nature.

[38]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[39]  R. Tsien Calcium channels in excitable cell membranes. , 1983, Annual review of physiology.

[40]  R. Eckert,et al.  Inactivation of Ca channels. , 1984, Progress in biophysics and molecular biology.

[41]  W. Trautwein,et al.  Acetylcholine activation of single muscarinic K+ channels in isolated pacemaker cells of the mammalian heart , 1983, Nature.

[42]  C. Eisenhart,et al.  Tables for Testing Randomness of Grouping in a Sequence of Alternatives , 1943 .

[43]  P. Usherwood,et al.  Non-random openings and concentration-dependent lifetimes of glutamate-gated channels in muscle membrane , 1981, Nature.

[44]  R. Meech,et al.  Calcium-dependent potassium activation in nervous tissues. , 1978, Annual review of biophysics and bioengineering.

[45]  F Bezanilla,et al.  Inactivation of the sodium channel. II. Gating current experiments , 1977, The Journal of general physiology.

[46]  R. Neubig,et al.  Conformations of Torpedo acetylcholine receptor associated with ion transport and desensitization. , 1982, Biochemistry.

[47]  Bert Sakmann,et al.  Bursts of Openings in Transmitter-Activated Ion Channels , 1983 .

[48]  R Horn,et al.  Effect of N-bromoacetamide on single sodium channel currents in excised membrane patches , 1982, The Journal of general physiology.

[49]  C. F. Stevens,et al.  Properties of single calcium channels in cardiac cell culture , 1982, Nature.

[50]  C. Armstrong,et al.  Sodium channels and gating currents. , 1981, Physiological reviews.

[51]  F J Sigworth,et al.  Covariance of nonstationary sodium current fluctuations at the node of Ranvier. , 1981, Biophysical journal.

[52]  S. Hagiwara,et al.  Studies of single calcium channel currents in rat clonal pituitary cells. , 1983, The Journal of physiology.

[53]  W. Almers,et al.  Gating currents and charge movements in excitable membranes. , 1978, Reviews of physiology, biochemistry and pharmacology.

[54]  A. Brown,et al.  Similarity of unitary Ca2+ currents in three different species , 1982, Nature.

[55]  H Lecar,et al.  Electrically gated ionic channels in lipid bilayers , 1977, Quarterly Reviews of Biophysics.

[56]  K L Magleby,et al.  A quantitative description of end‐plate currents , 1972, The Journal of physiology.

[57]  F. Bezanilla,et al.  Temperature effects on gating currents in the squid giant axon. , 1978, Biophysical journal.

[58]  E. Neher,et al.  Inward current channels activated by intracellular Ca in cultured cardiac cells , 1981, Nature.

[59]  C. Stevens,et al.  Sodium channels need not open before they inactivate , 1981, Nature.

[60]  E. Neher,et al.  Local anaesthetics transiently block currents through single acetylcholine‐receptor channels. , 1978, The Journal of physiology.

[61]  H. Meves,et al.  Calcium inward currents in internally perfused giant axons , 1973, The Journal of physiology.

[62]  E. Neher,et al.  Single acetylcholine-activated channels show burst-kinetics in presence of desensitizing concentrations of agonist , 1980, Nature.

[63]  E. Neher,et al.  Single Na+ channel currents observed in cultured rat muscle cells , 1980, Nature.

[64]  W. Chandler,et al.  Voltage clamp experiments on internally perfused giant axons. , 1965, The Journal of physiology.

[65]  R. P. Swenson A slow component of gating current in crayfish giant axons resembles inactivation charge movement. , 1983, Biophysical journal.

[66]  C. Loan,et al.  Nineteen Dubious Ways to Compute the Exponential of a Matrix , 1978 .

[67]  K. Rubinson The sodium currents of nerve under voltage clamp as heterogeneous kinetics. A model that is consistent with possible kinetic behavior. , 1982, Biophysical chemistry.

[68]  A. Fox Voltage-dependent inactivation of a calcium channel. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R Horn,et al.  Sodium channel gating: models, mimics, and modifiers. , 1983, Annual review of biophysics and bioengineering.

[70]  G. Weiland,et al.  Ligand specificity of state transitions in the cholinergic receptor: behavior of agonists and antagonists. , 1979, Molecular pharmacology.

[71]  L. Schlichter Spontaneous action potentials produced by Na and Cl channels in maturing Rana pipiens oocytes. , 1983, Developmental biology.

[72]  S. Provencher A Fourier method for the analysis of exponential decay curves. , 1976, Biophysical journal.

[73]  S. Cull-Candy,et al.  Rapid kinetics of single glutamate-receptor channels , 1982, Nature.

[74]  J. Steinbach,et al.  Activation of a nicotinic acetylcholine receptor. , 1984, Biophysical journal.

[75]  K. Beam,et al.  A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C , 1983, The Journal of general physiology.

[76]  R Latorre,et al.  Gating kinetics of Ca2+-activated K+ channels from rat muscle incorporated into planar lipid bilayers. Evidence for two voltage- dependent Ca2+ binding reactions , 1983, The Journal of general physiology.

[77]  M. D. Leibowitz,et al.  Single-channel acetylcholine receptor kinetics. , 1984, Biophysical journal.

[78]  A. Marty,et al.  Interaction of permeant ions with channels activated by acetylcholine in Aplysia neurones. , 1979, The Journal of physiology.

[79]  J. Yeh A pharmacological approach to the structure of the Na channel in squid axon. , 1982, Progress in clinical and biological research.

[80]  Fred J. Sigworth,et al.  Fitting and Statistical Analysis of Single-Channel Records , 1983 .