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PMID: 6296366 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Properties of single calcium-activated potassium channels in cultured rat muscle.

The Journal of physiology ·Vol. 331 ·1982-10-00 ·Pages 211-30

Barrett JN, Magleby KL, Pallotta BS

Abstract

1. Properties of the Ca-activated K channel were studied in excised patches of surface membrane from cultured rat muscle cells using single channel recording techniques.2. Increasing the concentration of calcium at the intracellular membrane surface [Ca](i), increased both the frequency and effective duration of channel openings. Ca at the extracellular membrane surface was not sufficient to activate the channels.3. An approximate third power relationship (slope = 2.7) was observed between [Ca](i) and the percentage of time the channels spent in the open state.4. Both the frequency and effective duration of channel openings increased as the intracellular membrane surface was made more positive; the percentage of time spent in the open state increased e-fold for a 15 mV depolarization for low levels of activity.5. The percentage of time spent with 1, 2,...n channels open in membrane patches with n channels was described by the binomial distribution, suggesting that the channels opened and shut independently of one another.6. Single channel conductance (144 mM-K on both sides of the membrane) was essentially independent of membrane potential (-50 to +50 mV) and [Ca](i) (0.1 muM -1 mM), but did increase with temperature, from 100 pS at 1 degrees C to 300 pS at 37 degrees C.7. Channel activity occurred in apparent bursts, with the duration of the apparent bursts increasing with increasing [Ca](i).8. Two exponentials were required to describe the distribution of observed channel open times, suggesting two different open channel states of apparently normal conductance. The observed mean channel open time of these states at +30 mV was 0.34 and 2.2 msec with 0.1 muM-Ca(i) and was 0.47 and 6.9 msec with 0.5 muM-Ca(i).9. The channel occasionally entered an apparent third open channel state with a single channel current amplitude about 40% the amplitude of the normally observed single channel currents. The reduced conductance state was immediately preceded and followed by a normal conducting state.10. While the kinetics of the Ca-activated K channel appear complex, its large conductance and high Ca and voltage sensitivity suggest that it is uniquely suited to resist depolarizations of the cell membrane potential that are accompanied by increases in intracellular Ca.

MeSH Terms
Animals Calcium/pharmacology Cells, Cultured Electric Conductivity In Vitro Techniques Ion Channels/drug effects,metabolism Membrane Potentials Muscles/metabolism,physiology Potassium/metabolism Rats Stimulation, Chemical Temperature Time Factors
Chemicals
Ion Channels Potassium Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Barrett J N
Magleby K L
Pallotta B S
References (35)
35 references, click to expand
  1. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  2. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture.
    Nature. 1981 Oct 8;293(5832):471-4 PMID: 6273730
  3. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes.
    Nature. 1981 Jun 11;291(5815):497-500 PMID: 6262657
  4. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction.
    J Physiol. 1973 Dec;235(3):655-91 PMID: 4543940
  5. Single acetylcholine-activated channels show burst-kinetics in presence of desensitizing concentrations of agonist.
    Nature. 1980 Jul 3;286(5768):71-3 PMID: 6248795
  6. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo.
    J Physiol. 1952 Apr;116(4):449-72 PMID: 14946713
  7. Single-channel currents recorded from membrane of denervated frog muscle fibres.
    Nature. 1976 Apr 29;260(5554):799-802 PMID: 1083489
  8. A transition temperature for acetylcholine channel conductance in chick myoballs.
    J Physiol. 1978 Jul;280:527-36 PMID: 690915
  9. Single channel recordings of K+ currents in squid axons.
    Nature. 1980 May 15;285(5761):140-3 PMID: 6246440
  10. Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones.
    J Physiol. 1976 Mar;255(3):737-74 PMID: 1083431
  11. The M. omohyoideus of the mouse as a convenient mammalian muscle preparation. A study of junctional and extrajunctional acetylcholine receptors by noise analysis and cooperativity.
    Pflugers Arch. 1976 Dec 28;367(2):115-22 PMID: 1034907
  12. On the stochastic properties of single ion channels.
    Proc R Soc Lond B Biol Sci. 1981 Mar 6;211(1183):205-35 PMID: 6111797
  13. Single channel currents from excised patches of muscle membrane.
    Proc Natl Acad Sci U S A. 1980 Nov;77(11):6930-4 PMID: 6256772
  14. Calcium-dependent potassium activation in nervous tissues.
    Annu Rev Biophys Bioeng. 1978;7:1-18 PMID: 352237
  15. Fluctuations in the microsecond time range of the current through single acetylcholine receptor ion channels.
    Nature. 1981 Dec 3;294(5840):464-6 PMID: 6273743
  16. The calcium current and the activation of a slow potassium conductance in voltage-clamped mouse neuroblastoma cells.
    J Physiol. 1979 Jul;292:307-23 PMID: 490359
  17. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia.
    J Physiol. 1976 Nov;262(2):349-82 PMID: 994042
  18. The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes.
    Pflugers Arch. 1978 Jul 18;375(2):219-28 PMID: 567789
  19. Non-random openings and concentration-dependent lifetimes of glutamate-gated channels in muscle membrane.
    Nature. 1981 Jun 4;291(5814):423-5 PMID: 6113544
  20. Potassium conductance and internal calcium accumulation in a molluscan neurone.
    J Physiol. 1980 Nov;308:287-313 PMID: 7230018
  21. A K+-selective, three-state channel from fragmented sarcoplasmic reticulum of frog leg muscle.
    J Membr Biol. 1981;61(1):31-8 PMID: 6267285
  22. Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells.
    Nature. 1981 Dec 3;294(5840):462-4 PMID: 6273742
  23. The determination of the stability constant for calcium-EGTA.
    Biochim Biophys Acta. 1976 Nov 18;451(1):321-5 PMID: 827309
  24. Potassium activation associated with intraneuronal free calcium.
    Science. 1978 Apr 28;200(4340):437-9 PMID: 644308
  25. Calcium-dependent slow potassium conductance in rat skeletal myotubes.
    Dev Biol. 1981 Mar;82(2):258-66 PMID: 7227642
  26. Single channel activity associated with the calcium dependent outward current in Helix pomatia.
    Pflugers Arch. 1981 Mar;389(3):293-5 PMID: 6262709
  27. Single glutamate-activated channels in locust muscle.
    Nature. 1979 Apr 12;278(5705):643-5 PMID: 450063
  28. A quantitative description of end-plate currents.
    J Physiol. 1972 May;223(1):173-97 PMID: 5046143
  29. Ionic blockage of sodium channels in nerve.
    J Gen Physiol. 1973 Jun;61(6):687-708 PMID: 4541078
  30. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx.
    J Physiol. 1975 Jul;249(2):211-39 PMID: 1177091
  31. Properties of a facilitating calcium current in pace-maker neurones of the snail, Helix pomatia.
    J Physiol. 1976 Nov;262(2):319-48 PMID: 994041
  32. Voltage dependence of agonist effectiveness at the frog neuromuscular junction: resolution of a paradox.
    J Physiol. 1975 Oct;251(2):245-70 PMID: 1081139
  33. Single ionic channels observed in tissue-cultured muscle.
    Nature. 1979 Dec 20-27;282(5741):861-3 PMID: 514365
  34. Calcium-dependent potassium conductance studied on internally dialysed nerve cells.
    Neuroscience. 1980;5(12):2187-92 PMID: 6258102
  35. Effect of measured calcium chloride injections on the membrane potential and internal pH of snail neurones.
    J Physiol. 1980 Jan;298:111-29 PMID: 6153718
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1982-10-00
Pages
211-30
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1197747
Subset
IM
Grants
NINDS NIH HHS · NS 06081 · United States
NINDS NIH HHS · NS 10277 · United States
NINDS NIH HHS · NS 12207 · United States
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