Abstract
We have used data obtained from measurements of ionic and gating currents to study the process of K+ channel activation in squid giant axons. A marked improvement in the recording of K+ channel gating currents (IKg) was obtained by total replacement of Cl- in the external solution by NO-3, which eliminates approximately 50% of the Na+ channel gating current with no effect on IKg. The midpoint of the steady state charge-voltage (Qrel - V) relationship is approximately 40 mV hyperpolarized to that of the steady state activation (fo - V) curve, which is an indication that the channel has many nonconducting states. Ionic and gating currents have similar time constants for both ON and OFF pulses. This eliminates any Hodgkin-Huxley nx scheme for K+ channel activation. An interrupted pulse paradigm shows that the last step in the activation process is not rate limiting. IKg shows a nonartifactual rising phase, which indicates that the first step is either the slowest step in the activation sequence or is voltage independent. These data are consistent with the following general scheme for K+ channel activation: (formula; see text)
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Selected References
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- Aldrich R. W., Corey D. P., Stevens C. F. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 1983 Dec 1;306(5942):436–441. doi: 10.1038/306436a0. [DOI] [PubMed] [Google Scholar]
- Almers W., Armstrong C. M. Survival of K+ permeability and gating currents in squid axons perfused with K+-free media. J Gen Physiol. 1980 Jan;75(1):61–78. doi: 10.1085/jgp.75.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol. 1977 Nov;70(5):567–590. doi: 10.1085/jgp.70.5.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M. Time course of TEA(+)-induced anomalous rectification in squid giant axons. J Gen Physiol. 1966 Nov;50(2):491–503. doi: 10.1085/jgp.50.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barrett J. N., Magleby K. L., Pallotta B. S. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982 Oct;331:211–230. doi: 10.1113/jphysiol.1982.sp014370. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bezanilla F. Gating charge movements and kinetics of excitable membrane proteins. Prog Clin Biol Res. 1982;79:3–16. [PubMed] [Google Scholar]
- Colquhoun D., Hawkes A. G. On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Philos Trans R Soc Lond B Biol Sci. 1982 Dec 24;300(1098):1–59. doi: 10.1098/rstb.1982.0156. [DOI] [PubMed] [Google Scholar]
- Conti F., Neher E. Single channel recordings of K+ currents in squid axons. Nature. 1980 May 15;285(5761):140–143. doi: 10.1038/285140a0. [DOI] [PubMed] [Google Scholar]
- DEL CASTILLO J., KATZ B. On the localization of acetylcholine receptors. J Physiol. 1955 Apr 28;128(1):157–181. doi: 10.1113/jphysiol.1955.sp005297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilly W. F., Armstrong C. M. Divalent cations and the activation kinetics of potassium channels in squid giant axons. J Gen Physiol. 1982 Jun;79(6):965–996. doi: 10.1085/jgp.79.6.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilly W. F., Armstrong C. M. Gating current and potassium channels in the giant axon of the squid. Biophys J. 1980 Mar;29(3):485–492. doi: 10.1016/S0006-3495(80)85147-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leibowitz M. D., Dionne V. E. Single-channel acetylcholine receptor kinetics. Biophys J. 1984 Jan;45(1):153–163. doi: 10.1016/S0006-3495(84)84144-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muller R. U., Peskin C. S. The kinetics of monazomycin-induced voltage-dependent conductance. II. Theory and a demonstration of a form of memory. J Gen Physiol. 1981 Aug;78(2):201–229. doi: 10.1085/jgp.78.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nass M. M., Lester H. A., Krouse M. E. Response of acetylcholine receptors to photoisomerizations of bound agonist molecules. Biophys J. 1978 Oct;24(1):135–160. doi: 10.1016/S0006-3495(78)85352-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oxford G. S. Some kinetic and steady-state properties of sodium channels after removal of inactivation. J Gen Physiol. 1981 Jan;77(1):1–22. doi: 10.1085/jgp.77.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- TAYLOR R. E., MOORE J. W., COLE K. S. Analysis of certain errors in squid axon voltage clamp measurements. Biophys J. 1960 Nov;1:161–202. doi: 10.1016/s0006-3495(60)86882-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor R. E., Bezanilla F. Sodium and gating current time shifts resulting from changes in initial conditions. J Gen Physiol. 1983 Jun;81(6):773–784. doi: 10.1085/jgp.81.6.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
