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. 1991 Feb;433:241–257. doi: 10.1113/jphysiol.1991.sp018424

Conductance properties of the Na(+)-activated K+ channel in guinea-pig ventricular cells.

Z Wang 1, T Kimitsuki 1, A Noma 1
PMCID: PMC1181369  PMID: 1841940

Abstract

1. The Na(+)-activated K+ channel current was recorded from inside-out membrane patches excised from single ventricular cells of guinea-pig hearts. 2. The single channel current-voltage relations showed inward-going rectification with an asymptotic conductance of 180-210 pS for the inward current at 150 mM [K+]o, when [K+]i was changed between 5.4 and 150 mM. The reversal potential indicated the PNa/PK of about 0.02. 3. The amplitude of outward current was reduced by increasing [Mg2+]i or [Na+]i, but no obvious blocking noise was recorded. The outward current, which remained shortly after quick removal of both [Na+]i and [Mg2+]i, revealed an ohmic conductance of the K+ channel. 4. The [Mg2+]i and [Na+]i block was increased e-fold by depolarizing the membrane by 49 mV, while the inward current was not blocked. 5. The Na(+)-activated K+ channel showed frequent subconductance levels. The variance-mean analysis resolved at least ten major sublevels. The density distribution of the sublevels were measured by composing the conventional amplitude histogram, excluding clear closed state currents, and then dividing the histogram into five segments. The probability of staying in each segment (Pn) was almost always voltage independent, and the grand averages were P1 = 9.5 +/- 5.9%, P2 = 6.3 +/- 2.1%, P3 = 4.2 +/- 1.8%, P4 = 7.8 +/- 2.5%, and P5 = 39.3 +/- 5.6%, from the lowest segment, respectively. 6. The values of Pn in partially blocked conditions by Na+ and Mg2+ (outward current) were not clearly different from those without any channel block (inward current). The values of Pn, measured before and after applying Ba2+ in the pipette, were also very similar. 7. The above findings indicate that the inward-going rectification of the Na(+)-activated K+ channel is due to the Na+ and Mg2+ block. The subconductance of the channel is not due to any channel block by Na+ or Mg2+, but may be attributable to multiple open states of a single-barrel channel, which has a large conductance. The channel may be blocked from any open conformation with an equal probability and with very fast 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. Armstrong C. M. Inactivation of the potassium conductance and related phenomena caused by quaternary ammonium ion injection in squid axons. J Gen Physiol. 1969 Nov;54(5):553–575. doi: 10.1085/jgp.54.5.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong C. M. Time course of TEA(+)-induced anomalous rectification in squid giant axons. J Gen Physiol. 1966 Nov;50(2):491–503. doi: 10.1085/jgp.50.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Callewaert G., Vereecke J., Carmeliet E. Existence of a calcium-dependent potassium channel in the membrane of cow cardiac Purkinje cells. Pflugers Arch. 1986 Apr;406(4):424–426. doi: 10.1007/BF00590947. [DOI] [PubMed] [Google Scholar]
  4. Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979;75(5):463–505. [PubMed] [Google Scholar]
  5. Goldman D. E. POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. J Gen Physiol. 1943 Sep 20;27(1):37–60. doi: 10.1085/jgp.27.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Horie M., Irisawa H., Noma A. Voltage-dependent magnesium block of adenosine-triphosphate-sensitive potassium channel in guinea-pig ventricular cells. J Physiol. 1987 Jun;387:251–272. doi: 10.1113/jphysiol.1987.sp016572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Horie M., Irisawa H. Rectification of muscarinic K+ current by magnesium ion in guinea pig atrial cells. Am J Physiol. 1987 Jul;253(1 Pt 2):H210–H214. doi: 10.1152/ajpheart.1987.253.1.H210. [DOI] [PubMed] [Google Scholar]
  10. Hunter M., Giebisch G. Multi-barrelled K channels in renal tubules. Nature. 1987 Jun 11;327(6122):522–524. doi: 10.1038/327522a0. [DOI] [PubMed] [Google Scholar]
  11. Kakei M., Noma A., Shibasaki T. Properties of adenosine-triphosphate-regulated potassium channels in guinea-pig ventricular cells. J Physiol. 1985 Jun;363:441–462. doi: 10.1113/jphysiol.1985.sp015721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kameyama M., Kakei M., Sato R., Shibasaki T., Matsuda H., Irisawa H. Intracellular Na+ activates a K+ channel in mammalian cardiac cells. Nature. 1984 May 24;309(5966):354–356. doi: 10.1038/309354a0. [DOI] [PubMed] [Google Scholar]
  13. Kameyama M., Kiyosue T., Soejima M. Single channel analysis of the inward rectifier K current in the rabbit ventricular cells. Jpn J Physiol. 1983;33(6):1039–1056. doi: 10.2170/jjphysiol.33.1039. [DOI] [PubMed] [Google Scholar]
  14. Krouse M. E., Schneider G. T., Gage P. W. A large anion-selective channel has seven conductance levels. Nature. 1986 Jan 2;319(6048):58–60. doi: 10.1038/319058a0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Matsuda H., Matsuura H., Noma A. Triple-barrel structure of inwardly rectifying K+ channels revealed by Cs+ and Rb+ block in guinea-pig heart cells. J Physiol. 1989 Jun;413:139–157. doi: 10.1113/jphysiol.1989.sp017646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matsuda H. Open-state substructure of inwardly rectifying potassium channels revealed by magnesium block in guinea-pig heart cells. J Physiol. 1988 Mar;397:237–258. doi: 10.1113/jphysiol.1988.sp016998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Matsuda H., Saigusa A., Irisawa H. Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2+. Nature. 1987 Jan 8;325(7000):156–159. doi: 10.1038/325156a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8;305(5930):147–148. doi: 10.1038/305147a0. [DOI] [PubMed] [Google Scholar]
  21. Patlak J. B. Sodium channel subconductance levels measured with a new variance-mean analysis. J Gen Physiol. 1988 Oct;92(4):413–430. doi: 10.1085/jgp.92.4.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Powell T., Terrar D. A., Twist V. W. Electrical properties of individual cells isolated from adult rat ventricular myocardium. J Physiol. 1980 May;302:131–153. doi: 10.1113/jphysiol.1980.sp013234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sakmann B., Noma A., Trautwein W. Acetylcholine activation of single muscarinic K+ channels in isolated pacemaker cells of the mammalian heart. Nature. 1983 May 19;303(5914):250–253. doi: 10.1038/303250a0. [DOI] [PubMed] [Google Scholar]
  24. Sakmann B., Trube G. Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol. 1984 Feb;347:641–657. doi: 10.1113/jphysiol.1984.sp015088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shibasaki T. Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol. 1987 Jun;387:227–250. doi: 10.1113/jphysiol.1987.sp016571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Soejima M., Noma A. Mode of regulation of the ACh-sensitive K-channel by the muscarinic receptor in rabbit atrial cells. Pflugers Arch. 1984 Apr;400(4):424–431. doi: 10.1007/BF00587544. [DOI] [PubMed] [Google Scholar]
  27. Takano M., Qin D. Y., Noma A. ATP-dependent decay and recovery of K+ channels in guinea pig cardiac myocytes. Am J Physiol. 1990 Jan;258(1 Pt 2):H45–H50. doi: 10.1152/ajpheart.1990.258.1.H45. [DOI] [PubMed] [Google Scholar]
  28. Taniguchi J., Kokubun S., Noma A., Irisawa H. Spontaneously active cells isolated from the sino-atrial and atrio-ventricular nodes of the rabbit heart. Jpn J Physiol. 1981;31(4):547–558. doi: 10.2170/jjphysiol.31.547. [DOI] [PubMed] [Google Scholar]
  29. Tsien R. Y., Rink T. J. Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim Biophys Acta. 1980 Jul;599(2):623–638. doi: 10.1016/0005-2736(80)90205-9. [DOI] [PubMed] [Google Scholar]
  30. Vandenberg C. A. Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2560–2564. doi: 10.1073/pnas.84.8.2560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Woodhull A. M. Ionic blockage of sodium channels in nerve. J Gen Physiol. 1973 Jun;61(6):687–708. doi: 10.1085/jgp.61.6.687. [DOI] [PMC free article] [PubMed] [Google Scholar]

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