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. 1989 Nov;418:293–309. doi: 10.1113/jphysiol.1989.sp017841

Two components of potassium current activated by depolarization of single smooth muscle cells from the rabbit portal vein.

D J Beech 1, T B Bolton 1
PMCID: PMC1189972  PMID: 2621620

Abstract

1. Using the patch-clamp technique at 20-23 degrees C membrane currents were recorded from single smooth muscle cells enzymatically isolated from the rabbit portal vein. Single-channel currents were observed in outside-out patches excised from these. 2. Outward current elicited upon depolarization from -70 mV was not activated as a result of Ca2+ influx. It could be divided into two components: an inactivating, 4-aminopyridine- and phencyclidine-sensitive low-noise current (IdK), and a non-inactivating, tetraethylammonium (TEA)- and charybdotoxin-sensitive high-noise current (IcK). 3. IdK activated with a threshold around -40 mV and was carried by K+. It was substantially inhibited by 4-aminopyridine (5 mM) or phencyclidine (0.1 mM) but was insensitive to TEA+ (4 mM), charybdotoxin (0.1 microM) or apamin (0.1 microM). Upon stepping to 0 mV it reached a maximum within about 0.2 s. The time course of its activation could be described by a fourth-order single exponential; the time constants of these exponentials changed e-fold every 56 mV. It inactivated in a time- and voltage-dependent manner with a fast and slow component, and was about 50% available at -30 mV. From single-channel recordings in isolated patches single channels underlying this current have a small unitary conductance (around 5 pS). 4. IcK did not inactivate significantly over 6 s. It activated with a less negative threshold than IdK, usually near 0 mV when the pipette solution contained 0.8 mM-EGTA with no added calcium. It was blocked by TEA (4 mM) or charybdotoxin (0.1 microM), but not by 4-aminopyridine (5 mM), phencyclidine (0.1 mM) or apamin (0.1 microM). Estimates of the single-channel conductance from the noise variance of the whole-cell current IcK indicated a value at +80 mV of 115 pS, very similar to that of the large-conductance Ca2(+)-activated K+ channels studied in these cells using single-channel recording. 5. The results suggest that outward current evoked by depolarization from the resting potential can be carried by 100 pS Ca2(+)-activated K+ channels and by small-conductance delayed-rectifier K+ channels. It is likely that opening of both types of channel contributes to the repolarization phase of the action potential in this smooth muscle.

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Selected References

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  1. Adrian R. H., Chandler W. K., Hodgkin A. L. Voltage clamp experiments in striated muscle fibres. J Physiol. 1970 Jul;208(3):607–644. doi: 10.1113/jphysiol.1970.sp009139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beech D. J., Bolton T. B. A voltage-dependent outward current with fast kinetics in single smooth muscle cells isolated from rabbit portal vein. J Physiol. 1989 May;412:397–414. doi: 10.1113/jphysiol.1989.sp017623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benham C. D., Bolton T. B., Lang R. J., Takewaki T. Calcium-activated potassium channels in single smooth muscle cells of rabbit jejunum and guinea-pig mesenteric artery. J Physiol. 1986 Feb;371:45–67. doi: 10.1113/jphysiol.1986.sp015961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benham C. D., Bolton T. B. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986 Dec;381:385–406. doi: 10.1113/jphysiol.1986.sp016333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Castle N. A., Strong P. N. Identification of two toxins from scorpion (Leiurus quinquestriatus) venom which block distinct classes of calcium-activated potassium channel. FEBS Lett. 1986 Dec 1;209(1):117–121. doi: 10.1016/0014-5793(86)81095-x. [DOI] [PubMed] [Google Scholar]
  6. Conti F., Neher E. Single channel recordings of K+ currents in squid axons. Nature. 1980 May 15;285(5761):140–143. doi: 10.1038/285140a0. [DOI] [PubMed] [Google Scholar]
  7. Dubois J. M. Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J Physiol. 1981 Sep;318:297–316. doi: 10.1113/jphysiol.1981.sp013865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Galvan M., Sedlmeir C. Outward currents in voltage-clamped rat sympathetic neurones. J Physiol. 1984 Nov;356:115–133. doi: 10.1113/jphysiol.1984.sp015456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [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. Hara Y., Kitamura K., Kuriyama H. Actions of 4-aminopyridine on vascular smooth muscle tissues of the guinea-pig. Br J Pharmacol. 1980 Jan;68(1):99–106. doi: 10.1111/j.1476-5381.1980.tb10704.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holman M. E., Kasby C. B., Suthers M. B., Wilson J. A. Some properties of the smooth muscle of rabbit portal vein. J Physiol. 1968 May;196(1):111–132. doi: 10.1113/jphysiol.1968.sp008498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Inoue R., Kitamura K., Kuriyama H. Two Ca-dependent K-channels classified by the application of tetraethylammonium distribute to smooth muscle membranes of the rabbit portal vein. Pflugers Arch. 1985 Oct;405(3):173–179. doi: 10.1007/BF00582557. [DOI] [PubMed] [Google Scholar]
  14. Klöckner U., Isenberg G. Action potentials and net membrane currents of isolated smooth muscle cells (urinary bladder of the guinea-pig). Pflugers Arch. 1985 Dec;405(4):329–339. doi: 10.1007/BF00595685. [DOI] [PubMed] [Google Scholar]
  15. Kuriyama H., Oshima K., Sakamoto Y. The membrane properties of the smooth muscle of the guinea-pig portal vein in isotonic and hypertonic solutions. J Physiol. 1971 Aug;217(1):179–199. doi: 10.1113/jphysiol.1971.sp009565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marchetti C., Premont R. T., Brown A. M. A whole-cell and single-channel study of the voltage-dependent outward potassium current in avian hepatocytes. J Gen Physiol. 1988 Feb;91(2):255–274. doi: 10.1085/jgp.91.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Miller C., Moczydlowski E., Latorre R., Phillips M. Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle. Nature. 1985 Jan 24;313(6000):316–318. doi: 10.1038/313316a0. [DOI] [PubMed] [Google Scholar]
  18. Mironneau J., Savineau J. P. Effects of calcium ions on outward membrane currents in rat uterine smooth muscle. J Physiol. 1980 May;302:411–425. doi: 10.1113/jphysiol.1980.sp013253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mitra R., Morad M. Ca2+ and Ca2+-activated K+ currents in mammalian gastric smooth muscle cells. Science. 1985 Jul 19;229(4710):269–272. doi: 10.1126/science.2409600. [DOI] [PubMed] [Google Scholar]
  20. Ohya Y., Kitamura K., Kuriyama H. Cellular calcium regulates outward currents in rabbit intestinal smooth muscle cell. Am J Physiol. 1987 Apr;252(4 Pt 1):C401–C410. doi: 10.1152/ajpcell.1987.252.4.C401. [DOI] [PubMed] [Google Scholar]
  21. Ohya Y., Kitamura K., Kuriyama H. Regulation of calcium current by intracellular calcium in smooth muscle cells of rabbit portal vein. Circ Res. 1988 Feb;62(2):375–383. doi: 10.1161/01.res.62.2.375. [DOI] [PubMed] [Google Scholar]
  22. Ohya Y., Terada K., Kitamura K., Kuriyama H. Membrane currents recorded from a fragment of rabbit intestinal smooth muscle cell. Am J Physiol. 1986 Sep;251(3 Pt 1):C335–C346. doi: 10.1152/ajpcell.1986.251.3.C335. [DOI] [PubMed] [Google Scholar]
  23. Okabe K., Kitamura K., Kuriyama H. Features of 4-aminopyridine sensitive outward current observed in single smooth muscle cells from the rabbit pulmonary artery. Pflugers Arch. 1987 Aug;409(6):561–568. doi: 10.1007/BF00584654. [DOI] [PubMed] [Google Scholar]
  24. Osa T. Effects of tetraethylammonium on the electrical activity of pregnant mouse myometrium and the interaction with manganese and cadmium. Jpn J Physiol. 1974 Feb;24(1):119–133. doi: 10.2170/jjphysiol.24.119. [DOI] [PubMed] [Google Scholar]
  25. Pallotta B. S. Calcium-activated potassium channels in rat muscle inactivate from a short-duration open state. J Physiol. 1985 Jun;363:501–516. doi: 10.1113/jphysiol.1985.sp015724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. SUZUKI T., NISHIYAMA A., INOMATA H. Effect of tetraethyl ammonium ion on the electrical activity of smooth muscle cell. Nature. 1963 Mar 2;197:908–909. doi: 10.1038/197908a0. [DOI] [PubMed] [Google Scholar]
  27. Schwarz J. R., Vogel W. Potassium inactivation in single myelinated nerve fibres of Xenopus laevis. Pflugers Arch. 1971;330(1):61–73. doi: 10.1007/BF00588735. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Somlyo A. V., Vinall P., Somlyo A. P. Excitation-contraction coupling and electrical events in two types of vascular smooth muscle. Microvasc Res. 1969 Oct;1(4):354–373. doi: 10.1016/0026-2862(69)90014-4. [DOI] [PubMed] [Google Scholar]
  30. Suzuki T., Inomata H. The ionic mechanism of excitation in intestinal smooth muscle cells. Adv Biophys. 1981;14:239–256. [PubMed] [Google Scholar]
  31. Terada K., Kitamura K., Kuriyama H. Different inhibitions of the voltage-dependent K+ current by Ca2+ antagonists in the smooth muscle cell membrane of rabbit small intestine. Pflugers Arch. 1987 May;408(6):558–564. doi: 10.1007/BF00581156. [DOI] [PubMed] [Google Scholar]
  32. Walsh J. V., Jr, Singer J. J. Voltage clamp of single freshly dissociated smooth muscle cells: current-voltage relationships for three currents. Pflugers Arch. 1981 May;390(2):207–210. doi: 10.1007/BF00590209. [DOI] [PubMed] [Google Scholar]
  33. Weigel R. J., Connor J. A., Prosser C. L. Two roles of calcium during the spike in circular muscle of small intestine in cat. Am J Physiol. 1979 Nov;237(5):C247–C256. doi: 10.1152/ajpcell.1979.237.5.C247. [DOI] [PubMed] [Google Scholar]
  34. Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Dynamics of aminopyridine block of potassium channels in squid axon membrane. J Gen Physiol. 1976 Nov;68(5):519–535. doi: 10.1085/jgp.68.5.519. [DOI] [PMC free article] [PubMed] [Google Scholar]

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