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. 1988 Jan;395:401–418. doi: 10.1113/jphysiol.1988.sp016926

Three kinetically distinct potassium channels in mouse neuroblastoma cells.

F N Quandt 1
PMCID: PMC1192001  PMID: 2457680

Abstract

1. Mouse neuroblastoma cells were utilized to examine the electrical properties of single K+ channels which might underlie multiple components of outward current in vertebrate neurones. The conductance, kinetics of activation, inactivation, and pharmacology of three types of channels were compared. 2. Two types of voltage-dependent channels, primarily permeable to K+, were identified which did not require the presence of internal Ca2+. The first had gating kinetics best classified as a delayed rectifier. The conductance of the open channel was 35 pS (22 degrees C) in solutions having symmetrical 125 mM-K+ concentrations. 3. The second type of channel had a conductance of 14 pS under identical conditions. The gating kinetics of this type of channel were distinct from those of the delayed rectifier. The mean first latency, and lifetime of the open state at any voltage, were longer. The maximum probability of an open channel was smaller, so that this parameter appeared less sensitive to the membrane potential. The rate of inactivation of the channel was slower. Further, at the more negative membrane potentials tested, the level of steady-state inactivation was less for this type of channel. 4. The delayed rectifier channel was more sensitive to the blocking action of 4-aminopyridine than the channel with low conductance. 5. A Ca2+ -activated, voltage-dependent K+ channel, having a conductance of 140 pS, was also identified. The maximum probability of an open channel increased, and the voltage for half-maximal activation shifted to a more negative potential as the internal Ca2+ was increased. 6. The time course of inactivation of K+ currents recorded from the whole cell declined in two phases, probably due to the presence of the two types of voltage-dependent K+ channels.

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Selected References

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  1. Adams D. J., Smith S. J., Thompson S. H. Ionic currents in molluscan soma. Annu Rev Neurosci. 1980;3:141–167. doi: 10.1146/annurev.ne.03.030180.001041. [DOI] [PubMed] [Google Scholar]
  2. Aldrich R. W. Inactivation of voltage-gated delayed potassium current in molluscan neurons. A kinetic model. Biophys J. 1981 Dec;36(3):519–532. doi: 10.1016/S0006-3495(81)84750-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aldrich R. W., Jr, Getting P. A., Thompson S. H. Inactivation of delayed outward current in molluscan neurone somata. J Physiol. 1979 Jun;291:507–530. doi: 10.1113/jphysiol.1979.sp012828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Armstrong C. M., Swenson R. P., Jr, Taylor S. R. Block of squid axon K channels by internally and externally applied barium ions. J Gen Physiol. 1982 Nov;80(5):663–682. doi: 10.1085/jgp.80.5.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Chabala L. D. The kinetics of recovery and development of potassium channel inactivation in perfused squid (Loligo pealei) giant axons. J Physiol. 1984 Nov;356:193–220. doi: 10.1113/jphysiol.1984.sp015460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clay J. R. Potassium current in the squid giant axon. Int Rev Neurobiol. 1985;27:363–384. doi: 10.1016/s0074-7742(08)60562-0. [DOI] [PubMed] [Google Scholar]
  9. Conti F., Hille B., Nonner W. Non-stationary fluctuations of the potassium conductance at the node of ranvier of the frog. J Physiol. 1984 Aug;353:199–230. doi: 10.1113/jphysiol.1984.sp015332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Dubois J. M. Potassium currents in the frog node of Ranvier. Prog Biophys Mol Biol. 1983;42(1):1–20. doi: 10.1016/0079-6107(83)90002-0. [DOI] [PubMed] [Google Scholar]
  12. Ebihara L., Speers W. C. Ionic channels in a line of embryonal carcinoma cells induced to undergo neuronal differentiation. Biophys J. 1984 Dec;46(6):827–830. doi: 10.1016/S0006-3495(84)84081-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gardner P. I. Single-channel recordings of three K+-selective currents in cultured chick ciliary ganglion neurons. J Neurosci. 1986 Jul;6(7):2106–2116. doi: 10.1523/JNEUROSCI.06-07-02106.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Hugues M., Romey G., Duval D., Vincent J. P., Lazdunski M. Apamin as a selective blocker of the calcium-dependent potassium channel in neuroblastoma cells: voltage-clamp and biochemical characterization of the toxin receptor. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1308–1312. doi: 10.1073/pnas.79.4.1308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kimhi Y., Palfrey C., Spector I., Barak Y., Littauer U. Z. Maturation of neuroblastoma cells in the presence of dimethylsulfoxide. Proc Natl Acad Sci U S A. 1976 Feb;73(2):462–466. doi: 10.1073/pnas.73.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Latorre R., Coronado R., Vergara C. K+ channels gated by voltage and ions. Annu Rev Physiol. 1984;46:485–495. doi: 10.1146/annurev.ph.46.030184.002413. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lynch C., 3rd Biochemical separation of delayed rectifier currents in frog short skeletal muscle fibres. J Physiol. 1985 Nov;368:379–392. doi: 10.1113/jphysiol.1985.sp015863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marty A., Neher E. Potassium channels in cultured bovine adrenal chromaffin cells. J Physiol. 1985 Oct;367:117–141. doi: 10.1113/jphysiol.1985.sp015817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maruyama Y., Petersen O. H., Flanagan P., Pearson G. T. Quantification of Ca2+-activated K+ channels under hormonal control in pig pancreas acinar cells. Nature. 1983 Sep 15;305(5931):228–232. doi: 10.1038/305228a0. [DOI] [PubMed] [Google Scholar]
  22. Meves H., Pichon Y. The effect of internal and external 4-aminopyridine on the potassium currents in intracellularly perfused squid giant axons. J Physiol. 1977 Jun;268(2):511–532. doi: 10.1113/jphysiol.1977.sp011869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Moolenaar W. H., Spector I. Ionic currents in cultured mouse neuroblastoma cells under voltage-clamp conditions. J Physiol. 1978 May;278:265–286. doi: 10.1113/jphysiol.1978.sp012303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moolenaar W. H., Spector I. The calcium action potential and a prolonged calcium dependent after-hyperpolarization in mouse neuroblastoma cells. J Physiol. 1979 Jul;292:297–306. doi: 10.1113/jphysiol.1979.sp012851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moolenaar W. H., Spector I. The calcium current and the activation of a slow potassium conductance in voltage-clamped mouse neuroblastoma cells. J Physiol. 1979 Jul;292:307–323. doi: 10.1113/jphysiol.1979.sp012852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neher E., Steinbach J. H. Local anaesthetics transiently block currents through single acetylcholine-receptor channels. J Physiol. 1978 Apr;277:153–176. doi: 10.1113/jphysiol.1978.sp012267. [DOI] [PMC free article] [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]
  29. Petersen O. H., Maruyama Y. Calcium-activated potassium channels and their role in secretion. Nature. 1984 Feb 23;307(5953):693–696. doi: 10.1038/307693a0. [DOI] [PubMed] [Google Scholar]
  30. Quandt F. N., Narahashi T. Isolation and kinetic analysis of inward currents in neuroblastoma cells. Neuroscience. 1984 Sep;13(1):249–262. doi: 10.1016/0306-4522(84)90275-6. [DOI] [PubMed] [Google Scholar]
  31. Romey G., Hugues M., Schmid-Antomarchi H., Lazdunski M. Apamin: a specific toxin to study a class of Ca2+-dependent K+ channels. J Physiol (Paris) 1984;79(4):259–264. [PubMed] [Google Scholar]
  32. Schwarz W., Passow H. Ca2+-activated K+ channels in erythrocytes and excitable cells. Annu Rev Physiol. 1983;45:359–374. doi: 10.1146/annurev.ph.45.030183.002043. [DOI] [PubMed] [Google Scholar]
  33. Stanfield P. R. Tetraethylammonium ions and the potassium permeability of excitable cells. Rev Physiol Biochem Pharmacol. 1983;97:1–67. doi: 10.1007/BFb0035345. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. 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]
  37. Yellen G. Single Ca2+-activated nonselective cation channels in neuroblastoma. Nature. 1982 Mar 25;296(5855):357–359. doi: 10.1038/296357a0. [DOI] [PubMed] [Google Scholar]
  38. van Mastrigt R. Constant-step approximation of multi-exponential signals using a least-squares criterion. Comput Biol Med. 1977 Jul;7(3):231–247. doi: 10.1016/0010-4825(77)90027-0. [DOI] [PubMed] [Google Scholar]

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