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. 1993 Nov;471:659–678. doi: 10.1113/jphysiol.1993.sp019921

Activation and inactivation of the bursting potassium channel from fused Torpedo synaptosomes.

J Edry-Schiller 1, R Rahamimoff 1
PMCID: PMC1143982  PMID: 8120828

Abstract

1. The voltage dependence of the bursting potassium channel in fused synaptosomes from Torpedo electric organ was studied in vitro, using the inside-out and the cell-attached configurations of the patch clamp technique. 2. The patch of membrane was held at various holding potentials (-140 to -50 mV) and then stepped to test potentials (-50 to +40 mV) for periods ranging from 5 to 300 ms. Each potential step was repeated 200-600 times. After subtraction of the capacitative transients and the leakage currents, an ensemble-averaged current was obtained. This ensemble current showed a marked activation upon depolarization, followed by an inactivation. 3. The activation of the bursting potassium channel is markedly dependent on the voltage step. Activation was detected at voltages positive to -50 mV. The peak of the ensemble current increases with the degree of depolarization, while the time to the peak decreases. With progressively larger depolarization, there is a shortening in the delay between the onset of the voltage step and the opening of the bursting potassium channels. 4. The inactivation phase of the ensemble current could be described adequately in most of the experiments, as a single exponential decay to a steady-state inactivation level. The time constant of inactivation was not markedly voltage dependent. 5. Single channel analysis of the inactivation reveals that it is due to a reduction in the number of channel openings and not due to changes in single channel current amplitude or channel mean open time along the pulse. 6. The holding potential has a marked effect on the peak amplitude of the ensemble current, indicating that hyperpolarization removes inactivation and depolarization induces it. The peak amplitude vs. voltage relation was fitted by the Boltzmann equation. The half-maximal inactivation was -105.2 +/- 5.8 mV (mean +/- S.E.M.), suggesting that at the resting potential a substantial fraction of the bursting potassium channels is in an inactivated state. 7. Two-pulse experiments show that the recovery from inactivation is a slow process which lasts well over 1 s. 8. High-frequency stimulation (20-66.7 Hz) by 5 ms pulses produces a progressive decline in the peak ensemble current amplitude. The decline is larger at higher stimulation frequencies.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Adams P. R., Brown D. A., Constanti A. M-currents and other potassium currents in bullfrog sympathetic neurones. J Physiol. 1982 Sep;330:537–572. doi: 10.1113/jphysiol.1982.sp014357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belluzzi O., Sacchi O., Wanke E. A fast transient outward current in the rat sympathetic neurone studied under voltage-clamp conditions. J Physiol. 1985 Jan;358:91–108. doi: 10.1113/jphysiol.1985.sp015542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cooper E., Shrier A. Inactivation of A currents and A channels on rat nodose neurons in culture. J Gen Physiol. 1989 Nov;94(5):881–910. doi: 10.1085/jgp.94.5.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cooper E., Shrier A. Single-channel analysis of fast transient potassium currents from rat nodose neurones. J Physiol. 1985 Dec;369:199–208. doi: 10.1113/jphysiol.1985.sp015896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Edry-Schiller J., Ginsburg S., Rahamimoff R. A bursting potassium channel in isolated cholinergic synaptosomes of Torpedo electric organ. J Physiol. 1991 Aug;439:627–647. doi: 10.1113/jphysiol.1991.sp018685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Furukawa Y., Kandel E. R., Pfaffinger P. Three types of early transient potassium currents in Aplysia neurons. J Neurosci. 1992 Mar;12(3):989–1000. doi: 10.1523/JNEUROSCI.12-03-00989.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gustafsson B., Galvan M., Grafe P., Wigström H. A transient outward current in a mammalian central neurone blocked by 4-aminopyridine. Nature. 1982 Sep 16;299(5880):252–254. doi: 10.1038/299252a0. [DOI] [PubMed] [Google Scholar]
  9. HAGIWARA S., KUSANO K., SAITO N. Membrane changes of Onchidium nerve cell in potassium-rich media. J Physiol. 1961 Mar;155:470–489. doi: 10.1113/jphysiol.1961.sp006640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Hermann A., Gorman A. L. Effects of 4-aminopyridine on potassium currents in a molluscan neuron. J Gen Physiol. 1981 Jul;78(1):63–86. doi: 10.1085/jgp.78.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hochner B., Klein M., Schacher S., Kandel E. R. Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8794–8798. doi: 10.1073/pnas.83.22.8794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoshi T., Zagotta W. N., Aldrich R. W. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 1990 Oct 26;250(4980):533–538. doi: 10.1126/science.2122519. [DOI] [PubMed] [Google Scholar]
  14. Huguenard J. R., Coulter D. A., Prince D. A. A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. J Neurophysiol. 1991 Oct;66(4):1304–1315. doi: 10.1152/jn.1991.66.4.1304. [DOI] [PubMed] [Google Scholar]
  15. Jackson M. B., Konnerth A., Augustine G. J. Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):380–384. doi: 10.1073/pnas.88.2.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jan L. Y., Jan Y. N. How might the diversity of potassium channels be generated? Trends Neurosci. 1990 Oct;13(10):415–419. doi: 10.1016/0166-2236(90)90123-r. [DOI] [PubMed] [Google Scholar]
  17. Kaang B. K., Pfaffinger P. J., Grant S. G., Kandel E. R., Furukawa Y. Overexpression of an Aplysia shaker K+ channel gene modifies the electrical properties and synaptic efficacy of identified Aplysia neurons. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1133–1137. doi: 10.1073/pnas.89.3.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaczmarek L. K. Voltage-dependent potassium channels: minK and Shaker families. New Biol. 1991 Apr;3(4):315–323. [PubMed] [Google Scholar]
  19. Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
  20. Katz B., Miledi R. The release of acetylcholine from nerve endings by graded electric pulses. Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):23–38. doi: 10.1098/rspb.1967.0011. [DOI] [PubMed] [Google Scholar]
  21. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J Physiol. 1968 Mar;195(2):481–492. doi: 10.1113/jphysiol.1968.sp008469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lichtinghagen R., Stocker M., Wittka R., Boheim G., Stühmer W., Ferrus A., Pongs O. Molecular basis of altered excitability in Shaker mutants of Drosophila melanogaster. EMBO J. 1990 Dec;9(13):4399–4407. doi: 10.1002/j.1460-2075.1990.tb07890.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Magleby K. L., Zengel J. E. A quantitative description of tetanic and post-tetanic potentiation of transmitter release at the frog neuromuscular junction. J Physiol. 1975 Feb;245(1):183–208. doi: 10.1113/jphysiol.1975.sp010840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Magleby K. L., Zengel J. E. Augmentation: A process that acts to increase transmitter release at the frog neuromuscular junction. J Physiol. 1976 May;257(2):449–470. doi: 10.1113/jphysiol.1976.sp011378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mallart A., Angaut-Petit D., Bourret-Poulain C., Ferrús A. Nerve terminal excitability and neuromuscular transmission in T(X;Y)V7 and Shaker mutants of Drosophila melanogaster. J Neurogenet. 1991 Feb;7(2-3):75–84. doi: 10.3109/01677069109066212. [DOI] [PubMed] [Google Scholar]
  26. Mallart A., Martin A. R. The relation between quantum content and facilitation at the neuromuscular junction of the frog. J Physiol. 1968 Jun;196(3):593–604. doi: 10.1113/jphysiol.1968.sp008525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McFarlane S., Cooper E. Kinetics and voltage dependence of A-type currents on neonatal rat sensory neurons. J Neurophysiol. 1991 Oct;66(4):1380–1391. doi: 10.1152/jn.1991.66.4.1380. [DOI] [PubMed] [Google Scholar]
  28. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. doi: 10.1085/jgp.58.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nilius B. Modal gating behavior of cardiac sodium channels in cell-free membrane patches. Biophys J. 1988 Jun;53(6):857–862. doi: 10.1016/S0006-3495(88)83166-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nordmann J. J., Stuenkel E. L. Electrical properties of axons and neurohypophysial nerve terminals and their relationship to secretion in the rat. J Physiol. 1986 Nov;380:521–539. doi: 10.1113/jphysiol.1986.sp016300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Premack B. A., Thompson S., Coombs-Hahn J. Clustered distribution and variability in kinetics of transient K channels in molluscan neuron cell bodies. J Neurosci. 1989 Nov;9(11):4089–4099. doi: 10.1523/JNEUROSCI.09-11-04089.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rahamimoff R. A dual effect of calcium ions on neuromuscular facilitation. J Physiol. 1968 Mar;195(2):471–480. doi: 10.1113/jphysiol.1968.sp008468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rahamimoff R., DeRiemer S. A., Ginsburg S., Kaiserman I., Sakmann B., Shapira R., Stadler H., Yakir N. Ionic channels in synaptic vesicles: are they involved in transmitter release? Q J Exp Physiol. 1989 Dec;74(7):1019–1031. doi: 10.1113/expphysiol.1989.sp003330. [DOI] [PubMed] [Google Scholar]
  34. Rahamimoff R., DeRiemer S. A., Sakmann B., Stadler H., Yakir N. Ion channels in synaptic vesicles from Torpedo electric organ. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5310–5314. doi: 10.1073/pnas.85.14.5310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rogawski M. A., Barker J. L. Effects of 4-aminopyridine on calcium action potentials and calcium current under voltage clamp in spinal neurons. Brain Res. 1983 Nov 28;280(1):180–185. doi: 10.1016/0006-8993(83)91190-3. [DOI] [PubMed] [Google Scholar]
  36. Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988 Jun;25(3):729–749. doi: 10.1016/0306-4522(88)90033-4. [DOI] [PubMed] [Google Scholar]
  37. Ruppersberg J. P., Stocker M., Pongs O., Heinemann S. H., Frank R., Koenen M. Regulation of fast inactivation of cloned mammalian IK(A) channels by cysteine oxidation. Nature. 1991 Aug 22;352(6337):711–714. doi: 10.1038/352711a0. [DOI] [PubMed] [Google Scholar]
  38. Salzberg B. M., Obaid A. L. Optical studies of the secretory event at vertebrate nerve terminals. J Exp Biol. 1988 Sep;139:195–231. doi: 10.1242/jeb.139.1.195. [DOI] [PubMed] [Google Scholar]
  39. Solc C. K., Zagotta W. N., Aldrich R. W. Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. Science. 1987 May 29;236(4805):1094–1098. doi: 10.1126/science.2437657. [DOI] [PubMed] [Google Scholar]
  40. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Thorn P. J., Wang X. M., Lemos J. R. A fast, transient K+ current in neurohypophysial nerve terminals of the rat. J Physiol. 1991 Jan;432:313–326. doi: 10.1113/jphysiol.1991.sp018386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zagotta W. N., Aldrich R. W. Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle. J Gen Physiol. 1990 Jan;95(1):29–60. doi: 10.1085/jgp.95.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zbicz K. L., Weight F. F. Transient voltage and calcium-dependent outward currents in hippocampal CA3 pyramidal neurons. J Neurophysiol. 1985 Apr;53(4):1038–1058. doi: 10.1152/jn.1985.53.4.1038. [DOI] [PubMed] [Google Scholar]

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