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Neurophysiology

, Volume 32, Issue 1, pp 1–7 | Cite as

Properties of the charibdotoxin-sensitive component of Ca2+-dependent K+ current in smooth muscle cells of the guinea pigTaenia Coli

  • A. V. Povtyan
  • A. V. Zima
  • M. I. Harhun
  • M. F. Shuba
Article

Abstract

Using the voltage-clamp technique, we investigated transmembrane ion currents in isolated smooth muscle cells of the guinea pigtaenia coli. In our study, we identified and studied a charibdotoxin-sensitive component of Ca2+-dependent K+ current carried through the channels of high conductance (in most publications called “big conductance,”I BK(Ca)). This component was completely blocked by 100 nM charibdotoxin and by tetraethylammonium in concentrations as low as 1 mM.I BK(Ca) demonstrated fast kinetics of inactivation, which nearly coincided with that of Ca2+ current. In addition to the dependence on Ca2+ concentration, this current also showed voltage-dependent properties: with a rise in the level of depolarization its amplitude increased. In many cells, depolarizing shifts in the membrane potential evoke spontaneous outward currents. Such currents probably represent the secondary effect of cyclic Ca2+ release from the caffeine-sensitive intracellular stores that result in short-term activation of charibdotoxin-sensitive Ca2+-dependent K+ channels.

Keywords

smooth muscle cells Ca2+-dependent K+ channels charibdotoxin spontaneous outward currents 

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References

  1. 1.
    V. I. Skok and M. F. Shuba,Neuromuscular Physiology [in Russian], Vyshcha Shkola, Kyiv (1986).Google Scholar
  2. 2.
    E. I. Nikitina, N. G. Kochemasova, V. M. Taranenko, and M. F. Shuba, “On the mechanism of the relaxing effect of noradrenaline on smooth muscle cells of the coronary arteries,”Byull. Éksp. Biol. Med.,91, No. 5, 517–520 (1981).Google Scholar
  3. 3.
    H. Kolb, “Potassium channels in excitable and non-excitable cells,”Rev. Physiol. Biochem. Pharmacol.,115, 52–91 (1990).Google Scholar
  4. 4.
    A. V. Zholos, V. A. Bouryi, and M. F. Shuba “Components of transmembrane ion current of the electroexcitable membrane of smooth muscle cells,”Biol. Membrany,3, No. 8, 804–815 (1986).Google Scholar
  5. 5.
    Y. Yamamoto, S. L. Hu, and C. Y. Kao, “Outward current in single smooth muscle cells of the guinea pigtaenia coli,”Gen. J. Physiol.,93, No. 3, 551–564 (1989).CrossRefGoogle Scholar
  6. 6.
    S. H. P. Alexander and J. A. Peters,TiPS Receptor and Ion Channel Nomenclature Supplement (1997), pp. 1-84.Google Scholar
  7. 7.
    C. Miller, E. Moczydlowski, R. Latorre, and M. Phillips, “Charybdotoxin a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle,”Nature,313, 316–318 (1985).PubMedCrossRefGoogle Scholar
  8. 8.
    H. Meves, “Potassium channel toxins,” in:Handbook of Experimental Pharmacology, Sec. Selective Neurotoxicity, Vol. 102, H. Herken and F. Hucho (eds.), Springer-Verlag, Berlin (1992), pp. 739–774.Google Scholar
  9. 9.
    M. L. Garcia, H. -G. Knaus, P. Munujos, et al., “Charibdotoxin and its effects on potassium channels,”Am. J. Physiol., 269 (Cell Physiol., 38), C1-C10 (1995).PubMedGoogle Scholar
  10. 10.
    M. Hugues, H. Schmid, G. Romey, et al., “The Ca2+-dependent slow K+ conductance in cultured rat muscle cells: characterization with apamin,”EMBO J.,1, 1039–1042 (1982).PubMedGoogle Scholar
  11. 11.
    A. L. Blatz, and K. L. Magleby, “Single apamin-blocked Ca-activated K+ channels of low conductance in cultured rat skeletal muscle,”Nature,323, 718–720 (1986).PubMedCrossRefGoogle Scholar
  12. 12.
    T. Capiod, and D. C. Ogden, “The properties of calcium-activated potassium ion channels in guinea-pig isolated hepatocytes,”J. Physiol.,409, 285–295 (1989).PubMedGoogle Scholar
  13. 13.
    F. Vogalis, Y. Zhang, and R. K. Goyal, “An intermediate conductance K+ channel in the cell membrane of mouse intestinal smooth muscle,”Biochim. Biophys. Acta,1371, No. 2, 309–316 (1998).PubMedCrossRefGoogle Scholar
  14. 14.
    A. V. Povstyan, A. V. Zima, and V. L. Reznikov, “Components of depolarization-induced transmembrane ion current in isolated smooth muscle cells of the guinea pigtaenia coli,”Neirofiziologiya/Neurophysiology,29, Nos. 4/5, 340–350 (1997).Google Scholar
  15. 15.
    C. D. Benham, and T. B. Bolton, “Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit,”J. Physiol.,381, 385–406 (1986).PubMedGoogle Scholar
  16. 16.
    Y. Ohya, K. Kitamura, and H. Kuriyama, “Cellular calcium regulates outward currents in rabbit intestinal smooth muscle cell,”Am. J. Physiol.,252, No. 4, C401-C410 (1987).PubMedGoogle Scholar
  17. 17.
    W. C. Cole, and K. M. Sanders, “Characterization of macroscopic outward currents of canine colonic myocytes,”Am. J. Physiol.,26, No. 3, C461-C469 (1989).Google Scholar
  18. 18.
    M. Ya. Ganitkevich, and M. F. Shuba, “Spontaneous outward currents in the membrane of isolated smooth muscle cells of the coronary artery,”Biol. Membrany,5, No. 12, 1312–1320 (1988).Google Scholar
  19. 19.
    V. A. Bouryi, D. V. Gordienko, and M. F. Shuba, “Characteristics of the K+ conductance of the membrane of isolated smooth muscle cells of mesenteric artery,”Biol. Membrany,9, No. 2, 595–601 (1992).Google Scholar
  20. 20.
    O. P. Hamill, A. Marty, E. Neher, et al., “Improved patch-clamp techniques for high-resolution current recording from cell-free membrane patches,”Pflügers Arch.,391, No. 1, 85–100 (1981).PubMedCrossRefGoogle Scholar
  21. 21.
    A. V. Zholos, L. V. Baidan, and M. F. Shuba, “Some properties of Ca2+-induced Ca2+ release mechanism in single visceral smooth muscle cell of the guinea-pig,”J. Physiol.,457, 1–25 (1992).PubMedGoogle Scholar
  22. 22.
    V. V. Rekalov, and A. M. Tsugorka, “Inactivation of Ca2+ current in isolated smooth muscle cells of the guinea pig stomach,”Biol. Membrany,6, No. 1, 59–66 (1989).Google Scholar
  23. 23.
    V. Ya. Ganitkevich, S. V. Smirnov, and M. F. Shuba, “On the nature of inactivation of inward Ca2+ current in isolated single smooth muscle cell,”Biol. Membrany,2, No. 12, 1235–1241 (1985).Google Scholar
  24. 24.
    A. L. Blatz, and K. L. Magleby, “Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle,”J. Gen. Physiol.,84, No. 1, 1–23 (1984).PubMedCrossRefGoogle Scholar
  25. 25.
    R. Latorre, and C. Miller, “Conduction and selectivity in potassium channels,”J. Membrane Biol.,71, Nos. 1/2, 11–30 (1983).CrossRefGoogle Scholar
  26. 26.
    C. D. Benham, T. B. Bolton, J. Lang, and T. Takewaki, “The mechanism of action of Ba2+ and TEA on single Ca2+-activated K+ channels in arterial and intestinal smooth muscle cell membranes,”Pflügers Arch.,403, No. 2, 120–127 (1985).PubMedCrossRefGoogle Scholar
  27. 27.
    A. V. Zima, A. V. Povstyan, and M. F. Shuba, “Ca2+-dependent K+ channels of high conductance in the membrane of smooth muscle cells of the guinea pigtaenia coli,”Vestn. Khar’kov Univ., Ser. Biophs. Vestn, No. 466, Issue 5, 47–51 (1999).Google Scholar
  28. 28.
    A. V. Zima, A. E. Belevich, Ya. D. Tsitsyura, and M. F. Shuba, “Effect of nitric oxide on Ca2+ and Ca2+-activated K+ channels in smooth muscle cells of the guinea pigtaenia coli,”Fiz. Zhivogo,4, No. 1, 67–72 (1996).Google Scholar
  29. 29.
    A. Marty, “Ca-dependent K channels with large unitary conductance in chromaffin cell membranes,”Nature,291, 497–500 (1981).PubMedCrossRefGoogle Scholar
  30. 30.
    H. G. Knaus, M. Garcia-Calvo, G. J. Kaczorowski, and M. L. Garcia, “Subunit composition of the high conductance calcium-activated potassium channel from smooth muscle, a representative of the mSlo and slowpoke family of potassium channels,”J. Biol. Chem.,269, 3921–3924 (1994).PubMedGoogle Scholar
  31. 31.
    P. Meera, M. Wallner, Z. Jiang, and L. Toro, “A calcium switch for the functional coupling between α (hslo) and β subunits (KV,Caβ) of maxi K channels,”FEBS,382, 84–88 (1996).CrossRefGoogle Scholar
  32. 32.
    M. Wallner, P. Meera, M. Ottolia, et al., “Characterization of and modulation by a β-subunit of a human maxi KCa channel cloned from myometrium,”Receptors Channels,3, 185–199 (1995).PubMedGoogle Scholar
  33. 33.
    Y. Tanaka, P. Meera, M. Song, et al., “Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant α+β subunit complexes,”J. Physiol.,502, No. 3, 545–557 (1997).PubMedCrossRefGoogle Scholar
  34. 34.
    B. P. Bean, M. Sturek, A. Puga, and K. Hermsmeyer “Calcium channels in muscle cells isolated from rat mesenteric arteries: modulation by dihydropyridine drugs,”Circ. Res.,59, No. 2, 229–235 (1986).PubMedGoogle Scholar
  35. 35.
    N. Akaike, H. Kanaide, T. Kuga, et al., “Low-voltage-activated calcium current in rat aorta smooth muscle cells in primary culture,”J. Physiol.,416, 141–160 (1989).PubMedGoogle Scholar
  36. 36.
    Y. Yamamoto, S. L. Hu, and C. Y. Kao, “Inward current in single smooth muscle cells of the guinea pigtaenia coli,”Gen. J. Physiol.,93, No. 3, 521–550 (1989).CrossRefGoogle Scholar
  37. 37.
    P. D. Langton, E. P. Burke, and K. M. Sanders, “Participation of Ca currents in colonic electrical activity,”Am. J. Physiol.,257, C451-C460 (1989).PubMedGoogle Scholar
  38. 38.
    A. V. Zima, A. É. Belevich, A. M. Tsugorka, and M. F. Shuba, “Depressing action of nitroglycerin on voltage-activated, calcium current in isolated smooth muscle cells of the guinea pig,”Neirofiziologiya/Neurophysiology26, No. 3. 218–222 (1994).Google Scholar
  39. 39.
    G. Yellen, “Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells,”J. Gen. Physiol.,84, 157–186 (1984).PubMedCrossRefGoogle Scholar
  40. 40.
    D. V. Gordienko, V. A. Bouryi, and M. F. Shuba, “Effect of caffeine on transmembrane K+ currents in isolated smooth muscle cells of the guinea pig mesenteric artery,”Biol. Membrany,12, No. 2, 129–137 (1995)Google Scholar

Copyright information

© Kluwer Academic/Plenum Publishers 2000

Authors and Affiliations

  • A. V. Povtyan
    • 1
  • A. V. Zima
    • 1
  • M. I. Harhun
    • 1
  • M. F. Shuba
    • 1
  1. 1.Bogomolets Institute of PhysiologyNational Academy of Sciences of UkraineKyivUkraine

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