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. 1993 Jan;460:311–326. doi: 10.1113/jphysiol.1993.sp019473

Effects of internal and external Na+ ions on inwardly rectifying K+ channels in guinea-pig ventricular cells.

H Matsuda 1
PMCID: PMC1175215  PMID: 8487197

Abstract

1. The effects of internal and external Na+ ions on the inwardly rectifying K+ channel were studied in guinea-pig ventricular cells. 2. Single-channel currents through the inwardly rectifying K+ channel were recorded in the open cell-attached or inside-out configuration at 150 mM internal K+ and either 150 or 25 mM external K+. Internal Na+, at a concentration of 5-40 mM, reduced the unitary amplitude of the outward current. No increase in open-channel current noise was detected with the filter cut-off frequency of 3 kHz. Substate behaviour seen with internal Mg2+ at a micromolar level was not observed. The inward currents were little affected by internal Na+. 3. The unitary current-voltage relation rectified inwardly in the presence of internal Na+ in a concentration-dependent manner. 4. Outward unitary currents were normalized to those measured in the absence of Na+. The normalized current-voltage relation was shifted in the negative direction by 20-25 mV by decreasing external K+ from 150 to 25 mM, indicating that the blocking effect increases with low external K+ when compared at a fixed voltage. 5. The normalized current-Na+ concentration curve was fitted by a one-to-one binding curve at each voltage. In a semi-logarithmic plot of dissociation constant versus membrane potential, data points for 150 and 25 mM external K+ were fitted by straight lines with nearly the same slope. The dissociation constant at 0 mV is 154 mM in 150 mM external K+ and 89 mM in 25 mM external K+. The voltage dependence of dissociation constants gives a value for the effective valency of the Na+ ion of around 0.5. 6. To study effects of external Na+, single-channel currents were recorded with pipette solutions containing 125 mM Na+, 125 mM choline or 125 mM N-methyl-D-glucamine (NMDG) in addition to 25 mM K+. Current amplitude was smaller with choline than with Na+ or NMDG. The reduction in current amplitude with choline was more evident in the inward current, resulting in a stronger outward rectification of the current-voltage relation. This finding and prolonged mean open time (see Summary point 7) was interpreted by assuming that choline is an open-channel blocker. 7. The lifetimes of the openings in the inward currents were distributed according to a single exponential. The mean open time with Na+ was similar to that with NMDG, which decreased with hyperpolarization. The mean open time with choline was much longer and less voltage dependent.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Biermans G., Vereecke J., Carmeliet E. The mechanism of the inactivation of the inward-rectifying K current during hyperpolarizing steps in guinea-pig ventricular myocytes. Pflugers Arch. 1987 Dec;410(6):604–613. doi: 10.1007/BF00581320. [DOI] [PubMed] [Google Scholar]
  2. Blatter L. A., McGuigan J. A. Intracellular pH regulation in ferret ventricular muscle. The role of Na-H exchange and the influence of metabolic substrates. Circ Res. 1991 Jan;68(1):150–161. doi: 10.1161/01.res.68.1.150. [DOI] [PubMed] [Google Scholar]
  3. Chapman R. A., Coray A., McGuigan J. A. Sodium/calcium exchange in mammalian ventricular muscle: a study with sodium-sensitive micro-electrodes. J Physiol. 1983 Oct;343:253–276. doi: 10.1113/jphysiol.1983.sp014891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ciani S., Ribalet B. Ion permeation and rectification in ATP-sensitive channels from insulin-secreting cells (RINm5F): effects of K+, Na+ and Mg2+. J Membr Biol. 1988 Jul;103(2):171–180. doi: 10.1007/BF01870947. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Findlay I. ATP-sensitive K+ channels in rat ventricular myocytes are blocked and inactivated by internal divalent cations. Pflugers Arch. 1987 Oct;410(3):313–320. doi: 10.1007/BF00580282. [DOI] [PubMed] [Google Scholar]
  7. Fukushima Y. Blocking kinetics of the anomalous potassium rectifier of tunicate egg studied by single channel recording. J Physiol. 1982 Oct;331:311–331. doi: 10.1113/jphysiol.1982.sp014374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Harvey R. D., Ten Eick R. E. Characterization of the inward-rectifying potassium current in cat ventricular myocytes. J Gen Physiol. 1988 Apr;91(4):593–615. doi: 10.1085/jgp.91.4.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harvey R. D., Ten Eick R. E. On the role of sodium ions in the regulation of the inward-rectifying potassium conductance in cat ventricular myocytes. J Gen Physiol. 1989 Aug;94(2):329–348. doi: 10.1085/jgp.94.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harvey R. D., Ten Eick R. E. Voltage-dependent block of cardiac inward-rectifying potassium current by monovalent cations. J Gen Physiol. 1989 Aug;94(2):349–361. doi: 10.1085/jgp.94.2.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Horie M., Irisawa H. Dual effects of intracellular magnesium on muscarinic potassium channel current in single guinea-pig atrial cells. J Physiol. 1989 Jan;408:313–332. doi: 10.1113/jphysiol.1989.sp017461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. Matsuda H. Effects of external and internal K+ ions on magnesium block of inwardly rectifying K+ channels in guinea-pig heart cells. J Physiol. 1991 Apr;435:83–99. doi: 10.1113/jphysiol.1991.sp018499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. 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]
  23. Matsuda H., Stanfield P. R. Single inwardly rectifying potassium channels in cultured muscle cells from rat and mouse. J Physiol. 1989 Jul;414:111–124. doi: 10.1113/jphysiol.1989.sp017679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Ohmori H. Inactivation kinetics and steady-state current noise in the anomalous rectifier of tunicate egg cell membranes. J Physiol. 1978 Aug;281:77–99. doi: 10.1113/jphysiol.1978.sp012410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Payet M. D., Rousseau E., Sauvé R. Single-channel analysis of a potassium inward rectifier in myocytes of newborn rat heart. J Membr Biol. 1985;86(2):79–88. doi: 10.1007/BF01870774. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Sakmann B., Trube G. Voltage-dependent inactivation of inward-rectifying single-channel currents in the guinea-pig heart cell membrane. J Physiol. 1984 Feb;347:659–683. doi: 10.1113/jphysiol.1984.sp015089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sheu S. S., Fozzard H. A. Transmembrane Na+ and Ca2+ electrochemical gradients in cardiac muscle and their relationship to force development. J Gen Physiol. 1982 Sep;80(3):325–351. doi: 10.1085/jgp.80.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Standen N. B., Stanfield P. R. Potassium depletion and sodium block of potassium currents under hyperpolarization in frog sartorius muscle. J Physiol. 1979 Sep;294:497–520. doi: 10.1113/jphysiol.1979.sp012943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. Wang Z., Kimitsuki T., Noma A. Conductance properties of the Na(+)-activated K+ channel in guinea-pig ventricular cells. J Physiol. 1991 Feb;433:241–257. doi: 10.1113/jphysiol.1991.sp018424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. Yellen G. Relief of Na+ block of Ca2+-activated K+ channels by external cations. J Gen Physiol. 1984 Aug;84(2):187–199. doi: 10.1085/jgp.84.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]

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