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. 1990 Jul;58(1):219–229. doi: 10.1016/S0006-3495(90)82367-5

Glutamate receptor-channel gating. Maximum likelihood analysis of gigaohm seal recordings from locust muscle.

S E Bates 1, M S Sansom 1, F G Ball 1, R L Ramsey 1, P N Usherwood 1
PMCID: PMC1280954  PMID: 1696510

Abstract

Gigaohm recordings have been made from glutamate receptor channels in excised, outside-out patches of collagenase-treated locust muscle membrane. The channels in the excised patches exhibit the kinetic state switching first seen in megaohm recordings from intact muscle fibers. Analysis of channel dwell time distributions reveals that the gating mechanism contains at least four open states and at least four closed states. Dwell time autocorrelation function analysis shows that there are at least three gateways linking the open states of the channel with the closed states. A maximum likelihood procedure has been used to fit six different gating models to the single channel data. Of these models, a cooperative model yields the best fit, and accurately predicts most features of the observed channel gating kinetics.

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Selected References

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

  1. Ball F. G., Kerry C. J., Ramsey R. L., Sansom M. S., Usherwood P. N. The use of dwell time cross-correlation functions to study single-ion channel gating kinetics. Biophys J. 1988 Aug;54(2):309–320. doi: 10.1016/S0006-3495(88)82961-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ball F. G., Rice J. A. A note on single-channel autocorrelation functions. Math Biosci. 1989 Nov;97(1):17–26. doi: 10.1016/0025-5564(89)90041-2. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Ball F. G., Sansom M. S. Single-channel autocorrelation functions: the effects of time interval omission. Biophys J. 1988 May;53(5):819–832. doi: 10.1016/S0006-3495(88)83161-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Colquhoun D., Hawkes A. G. A note on correlations in single ion channel records. Proc R Soc Lond B Biol Sci. 1987 Feb 23;230(1258):15–52. doi: 10.1098/rspb.1987.0008. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. Dudel J., Franke C., Hatt H., Ramsey R. L., Usherwood P. N. Rapid activation and desensitization by glutamate of excitatory, cation-selective channels in locust muscle. Neurosci Lett. 1988 May 16;88(1):33–38. doi: 10.1016/0304-3940(88)90311-4. [DOI] [PubMed] [Google Scholar]
  13. Evans M. L., Usherwood P. N. The effect of lectins on desensitisation of locust muscle glutamate receptors. Brain Res. 1985 Dec 9;358(1-2):34–39. doi: 10.1016/0006-8993(85)90945-x. [DOI] [PubMed] [Google Scholar]
  14. Franke C., Dudel J. Single glutamate-gated synaptic channels at the crayfish neuromuscular junction. I. The effect of enzyme treatment. Pflugers Arch. 1987 Mar;408(3):300–306. doi: 10.1007/BF02181473. [DOI] [PubMed] [Google Scholar]
  15. Gration K. A., Lambert J. J., Ramsey R. L., Rand R. P., Usherwood P. N. Agonist potency determination by patch clamp analysis of single glutamate receptors. Brain Res. 1981 Dec 28;230(1-2):400–405. doi: 10.1016/0006-8993(81)90423-6. [DOI] [PubMed] [Google Scholar]
  16. Gration K. A., Lambert J. J., Ramsey R. L., Rand R. P., Usherwood P. N. Closure of membrane channels gated by glutamate receptors may be a two-step process. Nature. 1982 Feb 18;295(5850):599–603. doi: 10.1038/295599a0. [DOI] [PubMed] [Google Scholar]
  17. Gration K. A., Lambert J. J., Ramsey R., Usherwood P. N. Non-random openings and concentration-dependent lifetimes of glutamate-gated channels in muscle membrane. Nature. 1981 Jun 4;291(5814):423–425. doi: 10.1038/291423a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Karlin A. On the application of "a plausible model" of allosteric proteins to the receptor for acetylcholine. J Theor Biol. 1967 Aug;16(2):306–320. doi: 10.1016/0022-5193(67)90011-2. [DOI] [PubMed] [Google Scholar]
  22. Kerry C. J., Kits K. S., Ramsey R. L., Sansom M. S., Usherwood P. N. Single channel kinetics of a glutamate receptor. Biophys J. 1987 Jan;51(1):137–144. doi: 10.1016/S0006-3495(87)83318-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Liebovitch L. S., Sullivan J. M. Fractal analysis of a voltage-dependent potassium channel from cultured mouse hippocampal neurons. Biophys J. 1987 Dec;52(6):979–988. doi: 10.1016/S0006-3495(87)83290-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Mathers D. A., Usherwood P. N. Concanavalin A blocks desensitisation of glutamate receptors on insect muscle fibres. Nature. 1976 Feb 5;259(5542):409–411. doi: 10.1038/259409a0. [DOI] [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. 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]
  31. McManus O. B., Spivak C. E., Blatz A. L., Weiss D. S., Magleby K. L. Fractal models, Markov models, and channel kinetics. Biophys J. 1989 Feb;55(2):383–385. doi: 10.1016/S0006-3495(89)82817-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Millhauser G. L., Salpeter E. E., Oswald R. E. Rate-amplitude correlation from single-channel records. A hidden structure in ion channel gating kinetics? Biophys J. 1988 Dec;54(6):1165–1168. doi: 10.1016/S0006-3495(88)83051-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Papke R. L., Millhauser G., Lieberman Z., Oswald R. E. Relationships of agonist properties to the single channel kinetics of nicotinic acetylcholine receptors. Biophys J. 1988 Jan;53(1):1–10. doi: 10.1016/S0006-3495(88)83059-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Sansom M. S., Ball F. G., Kerry C. J., McGee R., Ramsey R. L., Usherwood P. N. Markov, fractal, diffusion, and related models of ion channel gating. A comparison with experimental data from two ion channels. Biophys J. 1989 Dec;56(6):1229–1243. doi: 10.1016/S0006-3495(89)82770-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Steinberg I. Z. Frequencies of paired open-closed durations of ion channels. Method of evaluation from single-channel recordings. Biophys J. 1987 Jul;52(1):47–55. doi: 10.1016/S0006-3495(87)83187-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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