Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1983 Nov;344:585–604. doi: 10.1113/jphysiol.1983.sp014957

Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle.

K L Magleby, B S Pallotta
PMCID: PMC1193858  PMID: 6317853

Abstract

The stochastic properties of single Ca-activated K channels in excised patches of surface membrane from cultured rat muscle cells were studied using the patch-clamp technique. The distribution of all open intervals was described by the sum of two exponential distributions of short and long mean open time, suggesting at least two major open-channel states. Increasing the concentration of Ca at the inner membrane surface, [Ca]i, increased the mean duration of the long open distribution, while having little effect on the mean duration of the short open distribution. The frequency of openings to each distribution increased with [Ca]i. The rate of increase was a much steeper function of [Ca]i for openings in the long open distribution than for openings in the short open distribution; about 80% of the openings were to the long open distribution with 0.1 microM-Cai, increasing to 97% with 1 microM-Cai (+ 30 mV). These results suggest that openings in both open distributions are Ca-dependent, with openings in the long open distribution requiring the binding of more Ca ions than openings in the short open distribution. The distribution of all shut intervals at 0.5 microM-Cai and + 30 mV was described by the sum of three exponential distributions with mean durations of: 0.21 msec (short shut distribution), 1.90 msec (intermediate shut), and 44 msec (long shut). These results indicate that the channel typically enters at least three closed channel states during normal channel activity. In addition, a few longer shut intervals not accounted for by the above distributions suggested that there was a fourth infrequently occurring inactivated closed-channel state. The mean duration of the distribution of long shut intervals decreased with a power of about 2 with increasing [Ca]i under conditions where most openings were to the long open state (+ 30 mV, 0.25-1 microM-Cai). This observation suggests that openings to the long open distribution typically require the binding of two or more Ca ions. The mean intermediate shut interval appeared to increase slightly with increasing [Ca]i while the mean short shut interval was relatively Cai-independent. The percentage of all shut intervals that were short shut intervals increased with increasing [Ca]i while the percentage of long shut intervals decreased.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
590

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrett E. F., Barret J. N. Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol. 1976 Mar;255(3):737–774. doi: 10.1113/jphysiol.1976.sp011306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barrett J. N., Barrett E. F., Dribin L. B. Calcium-dependent slow potassium conductance in rat skeletal myotubes. Dev Biol. 1981 Mar;82(2):258–266. doi: 10.1016/0012-1606(81)90450-4. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Colquhoun D., Hawkes A. G. On the stochastic properties of single ion channels. Proc R Soc Lond B Biol Sci. 1981 Mar 6;211(1183):205–235. doi: 10.1098/rspb.1981.0003. [DOI] [PubMed] [Google Scholar]
  5. Colquhoun D., Hawkes A. G. Relaxation and fluctuations of membrane currents that flow through drug-operated channels. Proc R Soc Lond B Biol Sci. 1977 Nov 14;199(1135):231–262. doi: 10.1098/rspb.1977.0137. [DOI] [PubMed] [Google Scholar]
  6. Colquhoun D., Sakmann B. Fluctuations in the microsecond time range of the current through single acetylcholine receptor ion channels. Nature. 1981 Dec 3;294(5840):464–466. doi: 10.1038/294464a0. [DOI] [PubMed] [Google Scholar]
  7. Cull-Candy S. G., Parker I. Rapid kinetics of single glutamate-receptor channels. Nature. 1982 Feb 4;295(5848):410–412. doi: 10.1038/295410a0. [DOI] [PubMed] [Google Scholar]
  8. Dionne V. E., Steinbach J. H., Stevens C. F. An analysis of the dose-response relationship at voltage-clamped frog neuromuscular junctions. J Physiol. 1978 Aug;281:421–444. doi: 10.1113/jphysiol.1978.sp012431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eckert R., Tillotson D. Potassium activation associated with intraneuronal free calcium. Science. 1978 Apr 28;200(4340):437–439. doi: 10.1126/science.644308. [DOI] [PubMed] [Google Scholar]
  10. Gorman A. L., Thomas M. V. Potassium conductance and internal calcium accumulation in a molluscan neurone. J Physiol. 1980 Nov;308:287–313. doi: 10.1113/jphysiol.1980.sp013472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  12. Heyer C. B., Lux H. D. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia. J Physiol. 1976 Nov;262(2):349–382. doi: 10.1113/jphysiol.1976.sp011599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heyer C. B., Lux H. D. Properties of a facilitating calcium current in pace-maker neurones of the snail, Helix pomatia. J Physiol. 1976 Nov;262(2):319–348. doi: 10.1113/jphysiol.1976.sp011598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Horn R., Patlak J. Single channel currents from excised patches of muscle membrane. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6930–6934. doi: 10.1073/pnas.77.11.6930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Krnjević K., Lisiewicz A. Injections of calcium ions into spinal motoneurones. J Physiol. 1972 Sep;225(2):363–390. doi: 10.1113/jphysiol.1972.sp009945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Latorre R., Vergara C., Hidalgo C. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci U S A. 1982 Feb;79(3):805–809. doi: 10.1073/pnas.79.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lux H. D., Neher E., Marty A. Single channel activity associated with the calcium dependent outward current in Helix pomatia. Pflugers Arch. 1981 Mar;389(3):293–295. doi: 10.1007/BF00584792. [DOI] [PubMed] [Google Scholar]
  18. Magleby K. L., Pallotta B. S. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:605–623. doi: 10.1113/jphysiol.1983.sp014958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature. 1981 Jun 11;291(5815):497–500. doi: 10.1038/291497a0. [DOI] [PubMed] [Google Scholar]
  20. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  21. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Methfessel C., Boheim G. The gating of single calcium-dependent potassium channels is described by an activation/blockade mechanism. Biophys Struct Mech. 1982;9(1):35–60. doi: 10.1007/BF00536014. [DOI] [PubMed] [Google Scholar]
  23. Neher E., Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 1976 Apr 29;260(5554):799–802. doi: 10.1038/260799a0. [DOI] [PubMed] [Google Scholar]
  24. Neher E., Sakmann B., Steinbach J. H. The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pflugers Arch. 1978 Jul 18;375(2):219–228. doi: 10.1007/BF00584247. [DOI] [PubMed] [Google Scholar]
  25. Owen J. D. The determination of the stability constant for calcium-EGTA. Biochim Biophys Acta. 1976 Nov 18;451(1):321–325. doi: 10.1016/0304-4165(76)90282-8. [DOI] [PubMed] [Google Scholar]
  26. Pallotta B. S., Magleby K. L., Barrett J. N. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature. 1981 Oct 8;293(5832):471–474. doi: 10.1038/293471a0. [DOI] [PubMed] [Google Scholar]
  27. Patlak J. B., Gration K. A., Usherwood P. N. Single glutamate-activated channels in locust muscle. Nature. 1979 Apr 12;278(5705):643–645. doi: 10.1038/278643a0. [DOI] [PubMed] [Google Scholar]
  28. Patlak J., Horn R. Effect of N-bromoacetamide on single sodium channel currents in excised membrane patches. J Gen Physiol. 1982 Mar;79(3):333–351. doi: 10.1085/jgp.79.3.333. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES