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. 1986 Sep;378:141–174. doi: 10.1113/jphysiol.1986.sp016212

Quantitative description of three modes of activity of fast chloride channels from rat skeletal muscle.

A L Blatz, K L Magleby
PMCID: PMC1182857  PMID: 2432249

Abstract

The steady-state kinetic properties of single Cl- channels with fast kinetics active at resting membrane potentials in cultured rat skeletal muscle were studied using the patch-clamp technique. Membrane patches containing single active Cl- channels were often observed, and binomial analysis of the percentage open time in membrane patches containing several Cl- channels indicated that the channels did not occur as obligatory dimers and that they gated independently of one another. Channel activity could be divided into three categories: normal, which included about 99% of the openings and closings; buzz mode, which included about 1% and consisted of bursts of about 50 brief open and shut intervals; and inactivated shut states which included about 0.01% of the shut intervals and lasted for seconds, and occasionally minutes. The method of maximum likelihood was used to determine the number of significant exponential components required to fit the distributions of open and shut intervals during normal activity. Open interval distributions required at least two components, with time constants of 0.52 and 1.5 ms at -40 mV and 7.6 degrees C. Shut interval distributions required at least five exponential components, with time constants of 0.064, 0.72, 1.9, 12.3 and 350 ms. Kinetic reaction schemes were developed for the normal and buzz mode using maximum likelihood techniques to determine the most likely models and rate constants. In developing these models the effects of limited time resolution and missed events were taken into account. Each model tested typically had two or more sets of equally likely rate constants. Incorrect sets of rate constants resulting from the effect of missed events could be eliminated by analysis of the data with different time resolutions. Normal activity could be accounted for by several different seven-state models with two open and five shut states. As different models could be found that gave identical descriptions of the data, the distributions of open and shut intervals were not sufficient to define a unique model. It was established that no other seven-state models would be found that describe the distributions of open and shut intervals during normal activity better than the most likely presented models.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Adrian R. H., Bryant S. H. On the repetitive discharge in myotonic muscle fibres. J Physiol. 1974 Jul;240(2):505–515. doi: 10.1113/jphysiol.1974.sp010620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian R. H., Freygang W. H. The potassium and chloride conductance of frog muscle membrane. J Physiol. 1962 Aug;163(1):61–103. doi: 10.1113/jphysiol.1962.sp006959. [DOI] [PMC free article] [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. Blatz A. L., Magleby K. L. Correcting single channel data for missed events. Biophys J. 1986 May;49(5):967–980. doi: 10.1016/S0006-3495(86)83725-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blatz A. L., Magleby K. L. Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle. J Gen Physiol. 1984 Jul;84(1):1–23. doi: 10.1085/jgp.84.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blatz A. L., Magleby K. L. Single chloride-selective channels active at resting membrane potentials in cultured rat skeletal muscle. Biophys J. 1985 Jan;47(1):119–123. doi: 10.1016/S0006-3495(85)83884-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blatz A. L., Magleby K. L. Single voltage-dependent chloride-selective channels of large conductance in cultured rat muscle. Biophys J. 1983 Aug;43(2):237–241. doi: 10.1016/S0006-3495(83)84344-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clay J. R., DeFelice L. J. Relationship between membrane excitability and single channel open-close kinetics. Biophys J. 1983 May;42(2):151–157. doi: 10.1016/S0006-3495(83)84381-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Coronado R., Latorre R. Detection of K+ and Cl-channels from calf cardiac sarcolemma in planar lipid bilayer membranes. Nature. 1982 Aug 26;298(5877):849–852. doi: 10.1038/298849a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Fukuda J., Fischbach G. D., Smith T. G., Jr A voltage clamp study of the sodium, calcium and chloride spikes of chick skeletal muscle cells grown in tissue culture. Dev Biol. 1976 Apr;49(2):412–424. doi: 10.1016/0012-1606(76)90184-6. [DOI] [PubMed] [Google Scholar]
  15. Gray P. T., Bevan S., Ritchie J. M. High conductance anion-selective channels in rat cultured Schwann cells. Proc R Soc Lond B Biol Sci. 1984 Jun 22;221(1225):395–409. doi: 10.1098/rspb.1984.0041. [DOI] [PubMed] [Google Scholar]
  16. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HUTTER O. F., NOBLE D. The chloride conductance of frog skeletal muscle. J Physiol. 1960 Apr;151:89–102. [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hess P., Lansman J. B., Tsien R. W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984 Oct 11;311(5986):538–544. doi: 10.1038/311538a0. [DOI] [PubMed] [Google Scholar]
  20. Horn R., Lange K. Estimating kinetic constants from single channel data. Biophys J. 1983 Aug;43(2):207–223. doi: 10.1016/S0006-3495(83)84341-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Horn R., Vandenberg C. A. Statistical properties of single sodium channels. J Gen Physiol. 1984 Oct;84(4):505–534. doi: 10.1085/jgp.84.4.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hutter O. F., Warner A. E. The voltage dependence of the chloride conductance of frog muscle. J Physiol. 1972 Dec;227(1):275–290. doi: 10.1113/jphysiol.1972.sp010032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jackson M. B. Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3901–3904. doi: 10.1073/pnas.81.12.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jackson M. B., Wong B. S., Morris C. E., Lecar H., Christian C. N. Successive openings of the same acetylcholine receptor channel are correlated in open time. Biophys J. 1983 Apr;42(1):109–114. doi: 10.1016/S0006-3495(83)84375-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Labarca P., Rice J. A., Fredkin D. R., Montal M. Kinetic analysis of channel gating. Application to the cholinergic receptor channel and the chloride channel from Torpedo californica. Biophys J. 1985 Apr;47(4):469–478. doi: 10.1016/S0006-3495(85)83939-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Läuger P. Ionic channels with conformational substates. Biophys J. 1985 May;47(5):581–590. doi: 10.1016/S0006-3495(85)83954-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Magleby K. L., Pallotta B. S. Calcium dependence of open and shut interval distributions from calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:585–604. doi: 10.1113/jphysiol.1983.sp014957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. McManus O. B., Blatz A. L., Magleby K. L. Inverse relationship of the durations of adjacent open and shut intervals for C1 and K channels. Nature. 1985 Oct 17;317(6038):625–627. doi: 10.1038/317625a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Miller C. Open-state substructure of single chloride channels from Torpedo electroplax. Philos Trans R Soc Lond B Biol Sci. 1982 Dec 1;299(1097):401–411. doi: 10.1098/rstb.1982.0140. [DOI] [PubMed] [Google Scholar]
  32. Miller C., White M. M. A voltage-dependent chloride conductance channel from Torpedo electroplax membrane. Ann N Y Acad Sci. 1980;341:534–551. doi: 10.1111/j.1749-6632.1980.tb47197.x. [DOI] [PubMed] [Google Scholar]
  33. Moczydlowski E., Latorre R. Gating kinetics of Ca2+-activated K+ channels from rat muscle incorporated into planar lipid bilayers. Evidence for two voltage-dependent Ca2+ binding reactions. J Gen Physiol. 1983 Oct;82(4):511–542. doi: 10.1085/jgp.82.4.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Neher E. The charge carried by single-channel currents of rat cultured muscle cells in the presence of local anaesthetics. J Physiol. 1983 Jun;339:663–678. doi: 10.1113/jphysiol.1983.sp014741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nelson D. J., Tang J. M., Palmer L. G. Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells. J Membr Biol. 1984;80(1):81–89. doi: 10.1007/BF01868692. [DOI] [PubMed] [Google Scholar]
  36. Palade P. T., Barchi R. L. Characteristics of the chloride conductance in muscle fibers of the rat diaphragm. J Gen Physiol. 1977 Mar;69(3):325–342. doi: 10.1085/jgp.69.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Patlak J. B., Ortiz M. Slow currents through single sodium channels of the adult rat heart. J Gen Physiol. 1985 Jul;86(1):89–104. doi: 10.1085/jgp.86.1.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Roux B., Sauvé R. A general solution to the time interval omission problem applied to single channel analysis. Biophys J. 1985 Jul;48(1):149–158. doi: 10.1016/S0006-3495(85)83768-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sakmann B., Patlak J., Neher E. Single acetylcholine-activated channels show burst-kinetics in presence of desensitizing concentrations of agonist. Nature. 1980 Jul 3;286(5768):71–73. doi: 10.1038/286071a0. [DOI] [PubMed] [Google Scholar]
  41. Woodbury J. W., Miles P. R. Anion conductance of frog muscle membranes: one channel, two kinds of pH dependence. J Gen Physiol. 1973 Sep;62(3):324–353. doi: 10.1085/jgp.62.3.324. [DOI] [PMC free article] [PubMed] [Google Scholar]

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