Abstract
1. The Ca(2+)-dependent kinetics of large-conductance Ca(2+)-activated K+ channels from cultured rat skeletal muscle were studied with the patch clamp technique. Data were collected in the absence of Na+ and Mg2+, which can alter the kinetics. About 2 x 10(5) open and shut intervals were analysed from each of five different excised membrane patches containing a single active channel. Analysis was restricted to activity in the normal mode, which includes 96% of the intervals. 2. The open probability (Popen) and dwell-time distributions of open and shut intervals were obtained at three to four different [Ca2+]i for each of the channels. Popen data were also obtained from some multichannel patches. 3. Increasing [Ca2+]i increased Popen. At a pH of 7.0 the Hill coefficient was 3.7 +/- 0.8 (range of 3.0-5.0) and a Popen of 0.5 occurred at 14 +/- 7 microM [Ca2+]i (K0.5) for data obtained at +30 mV (n = 6). At a pH of 7.2 the Hill coefficient was 3.0 +/- 0.5 (range of 2.2-3.7) and K0.5 was 9 +/- 6 microM-Ca2+ (n = 7). The large standard deviations for K0.5 reflect the observation that fourfold differences in K0.5 could be observed for different channels studied under the same experimental conditions. 4. Hill coefficients that can be greater than 3 suggest that the channel may bind four or more Ca2+ to become fully activated. The binding of four Ca2+ before opening would require a minimum of five shut states. This estimate of the minimum number of shut states is in general agreement with that obtained from the number of exponential components in the dwell-time distributions of shut intervals. Thus, two different methods give similar estimates of the minimum number of shut states. If the channel can open with different numbers of bound Ca2+, then this could give rise to the three to four open states suggested by the three to four exponential components in the open dwell-time distributions. 5. Kinetic schemes consistent with the Ca(2+)-dependent kinetics were developed by simultaneously fitting open and shut dwell-time distributions obtained at three to four different [Ca2+]i, using maximum likelihood techniques and corrections for missed events. Such simultaneous fitting can provide an increased ability to define models and rate constants.(ABSTRACT TRUNCATED AT 400 WORDS)
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ball F. G., Sansom M. S. Ion-channel gating mechanisms: model identification and parameter estimation from single channel recordings. Proc R Soc Lond B Biol Sci. 1989 May 22;236(1285):385–416. doi: 10.1098/rspb.1989.0029. [DOI] [PubMed] [Google Scholar]
- Balser J. R., Roden D. M., Bennett P. B. Global parameter optimization for cardiac potassium channel gating models. Biophys J. 1990 Mar;57(3):433–444. doi: 10.1016/S0006-3495(90)82560-1. [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]
- Bates S. E., Sansom M. S., Ball F. G., Ramsey R. L., Usherwood P. N. Glutamate receptor-channel gating. Maximum likelihood analysis of gigaohm seal recordings from locust muscle. Biophys J. 1990 Jul;58(1):219–229. doi: 10.1016/S0006-3495(90)82367-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bauer R. J., Bowman B. F., Kenyon J. L. Theory of the kinetic analysis of patch-clamp data. Biophys J. 1987 Dec;52(6):961–978. doi: 10.1016/S0006-3495(87)83289-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blatz A. L., Magleby K. L. Adjacent interval analysis distinguishes among gating mechanisms for the fast chloride channel from rat skeletal muscle. J Physiol. 1989 Mar;410:561–585. doi: 10.1113/jphysiol.1989.sp017549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Blatz A. L., Magleby K. L. Quantitative description of three modes of activity of fast chloride channels from rat skeletal muscle. J Physiol. 1986 Sep;378:141–174. doi: 10.1113/jphysiol.1986.sp016212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christensen O., Zeuthen T. Maxi K+ channels in leaky epithelia are regulated by intracellular Ca2+, pH and membrane potential. Pflugers Arch. 1987 Mar;408(3):249–259. doi: 10.1007/BF02181467. [DOI] [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]
- 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]
- 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]
- Colquhoun D., Hawkes A. G. Stochastic properties of ion channel openings and bursts in a membrane patch that contains two channels: evidence concerning the number of channels present when a record containing only single openings is observed. Proc R Soc Lond B Biol Sci. 1990 Jun 22;240(1299):453–477. doi: 10.1098/rspb.1990.0048. [DOI] [PubMed] [Google Scholar]
- Colquhoun D., Sakmann B. Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. J Physiol. 1985 Dec;369:501–557. doi: 10.1113/jphysiol.1985.sp015912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Colquhoun D. Single channel analysis costs time. Trends Pharmacol Sci. 1988 May;9(5):157–158. doi: 10.1016/0165-6147(88)90027-2. [DOI] [PubMed] [Google Scholar]
- Dani J. A. Ion-channel entrances influence permeation. Net charge, size, shape, and binding considerations. Biophys J. 1986 Mar;49(3):607–618. doi: 10.1016/S0006-3495(86)83688-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Gibb A. J., Kojima H., Carr J. A., Colquhoun D. Expression of cloned receptor subunits produces multiple receptors. Proc Biol Sci. 1990 Nov 22;242(1304):108–112. doi: 10.1098/rspb.1990.0112. [DOI] [PubMed] [Google Scholar]
- Golowasch J., Kirkwood A., Miller C. Allosteric effects of Mg2+ on the gating of Ca2+-activated K+ channels from mammalian skeletal muscle. J Exp Biol. 1986 Sep;124:5–13. doi: 10.1242/jeb.124.1.5. [DOI] [PubMed] [Google Scholar]
- 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]
- Horn R. Statistical methods for model discrimination. Applications to gating kinetics and permeation of the acetylcholine receptor channel. Biophys J. 1987 Feb;51(2):255–263. doi: 10.1016/S0006-3495(87)83331-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kerry C. J., Ramsey R. L., Sansom M. S., Usherwood P. N. Glutamate receptor channel kinetics: the effect of glutamate concentration. Biophys J. 1988 Jan;53(1):39–52. doi: 10.1016/S0006-3495(88)83064-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kienker P. Equivalence of aggregated Markov models of ion-channel gating. Proc R Soc Lond B Biol Sci. 1989 Apr 22;236(1284):269–309. doi: 10.1098/rspb.1989.0024. [DOI] [PubMed] [Google Scholar]
- Korn S. J., Horn R. Statistical discrimination of fractal and Markov models of single-channel gating. Biophys J. 1988 Nov;54(5):871–877. doi: 10.1016/S0006-3495(88)83023-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kume H., Takagi K., Satake T., Tokuno H., Tomita T. Effects of intracellular pH on calcium-activated potassium channels in rabbit tracheal smooth muscle. J Physiol. 1990 May;424:445–457. doi: 10.1113/jphysiol.1990.sp018076. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Latorre R., Miller C. Conduction and selectivity in potassium channels. J Membr Biol. 1983;71(1-2):11–30. doi: 10.1007/BF01870671. [DOI] [PubMed] [Google Scholar]
- Latorre R., Oberhauser A., Labarca P., Alvarez O. Varieties of calcium-activated potassium channels. Annu Rev Physiol. 1989;51:385–399. doi: 10.1146/annurev.ph.51.030189.002125. [DOI] [PubMed] [Google Scholar]
- 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]
- Läuger P. Internal motions in proteins and gating kinetics of ionic channels. Biophys J. 1988 Jun;53(6):877–884. doi: 10.1016/S0006-3495(88)83168-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MONOD J., WYMAN J., CHANGEUX J. P. ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. J Mol Biol. 1965 May;12:88–118. doi: 10.1016/s0022-2836(65)80285-6. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Magleby K. L., Weiss D. S. Estimating kinetic parameters for single channels with simulation. A general method that resolves the missed event problem and accounts for noise. Biophys J. 1990 Dec;58(6):1411–1426. doi: 10.1016/S0006-3495(90)82487-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magleby K. L., Weiss D. S. Identifying kinetic gating mechanisms for ion channels by using two-dimensional distributions of simulated dwell times. Proc Biol Sci. 1990 Sep 22;241(1302):220–228. doi: 10.1098/rspb.1990.0089. [DOI] [PubMed] [Google Scholar]
- Marty A. Blocking of large unitary calcium-dependent potassium currents by internal sodium ions. Pflugers Arch. 1983 Feb;396(2):179–181. doi: 10.1007/BF00615524. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- McManus O. B., Blatz A. L., Magleby K. L. Sampling, log binning, fitting, and plotting durations of open and shut intervals from single channels and the effects of noise. Pflugers Arch. 1987 Nov;410(4-5):530–553. doi: 10.1007/BF00586537. [DOI] [PubMed] [Google Scholar]
- McManus O. B., Magleby K. L. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J Physiol. 1988 Aug;402:79–120. doi: 10.1113/jphysiol.1988.sp017195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McManus O. B., Magleby K. L. Kinetic time constants independent of previous single-channel activity suggest Markov gating for a large conductance Ca-activated K channel. J Gen Physiol. 1989 Dec;94(6):1037–1070. doi: 10.1085/jgp.94.6.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McManus O. B., Weiss D. S., Spivak C. E., Blatz A. L., Magleby K. L. Fractal models are inadequate for the kinetics of four different ion channels. Biophys J. 1988 Nov;54(5):859–870. doi: 10.1016/S0006-3495(88)83022-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Millhauser G. L., Salpeter E. E., Oswald R. E. Diffusion models of ion-channel gating and the origin of power-law distributions from single-channel recording. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1503–1507. doi: 10.1073/pnas.85.5.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Oberhauser A., Alvarez O., Latorre R. Activation by divalent cations of a Ca2+-activated K+ channel from skeletal muscle membrane. J Gen Physiol. 1988 Jul;92(1):67–86. doi: 10.1085/jgp.92.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pallotta B. S. Calcium-activated potassium channels in rat muscle inactivate from a short-duration open state. J Physiol. 1985 Jun;363:501–516. doi: 10.1113/jphysiol.1985.sp015724. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Singer J. J., Walsh J. V., Jr Characterization of calcium-activated potassium channels in single smooth muscle cells using the patch-clamp technique. Pflugers Arch. 1987 Feb;408(2):98–111. doi: 10.1007/BF00581337. [DOI] [PubMed] [Google Scholar]
- Vergara C., Latorre R. Kinetics of Ca2+-activated K+ channels from rabbit muscle incorporated into planar bilayers. Evidence for a Ca2+ and Ba2+ blockade. J Gen Physiol. 1983 Oct;82(4):543–568. doi: 10.1085/jgp.82.4.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weiss D. S., Magleby K. L. Gating scheme for single GABA-activated Cl- channels determined from stability plots, dwell-time distributions, and adjacent-interval durations. J Neurosci. 1989 Apr;9(4):1314–1324. doi: 10.1523/JNEUROSCI.09-04-01314.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong B. S., Lecar H., Adler M. Single calcium-dependent potassium channels in clonal anterior pituitary cells. Biophys J. 1982 Sep;39(3):313–317. doi: 10.1016/S0006-3495(82)84522-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yellen G. Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells. J Gen Physiol. 1984 Aug;84(2):157–186. doi: 10.1085/jgp.84.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]