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. 1997 Aug 1;502(Pt 3):497–508. doi: 10.1111/j.1469-7793.1997.497bj.x

Activation of small conductance Ca(2+)-dependent K+ channels by purinergic agonists in smooth muscle cells of the mouse ileum.

F Vogalis 1, R K Goyal 1
PMCID: PMC1159523  PMID: 9279803

Abstract

1. Whole-cell and single-channel K+ currents were recorded at room temperature (22-24 degrees C), from smooth muscle cells enzymatically dispersed from the mouse ileum, using variations of the patch-clamp technique. 2. Net outward K+ currents recorded through amphotericin-B-perforated patches in response to step depolarizations positive to -50 mV from a holding potential of -80 mV were decreased by up to 70% by external apamin (0.5 microM). Apamin-sensitive whole-cell currents were also recorded from cells perfused internally with 150 nM Ca2+ but not from cells perfused internally with 85 nM Ca2+. 3. Three types of non-inactivating Ca(2+)-sensitive K+ channels were identified in cell-attached and excised patches under an asymmetrical K+ gradient: (i) large conductance (BKCa; approximately 200 pS) channels blocked by 2 mM external TEA; (ii) intermediate conductance (IKCa; approximately 39 pS) channels blocked by 2 mM external TEA and inhibited by external apamin (0.5 microM); and (iii) small conductance (SKCa; approximately 10 pS) channels that were not blocked by 5 mM external TEA but were sensitive to extracellular apamin (0.5 microM). 4. The TEA-resistant SKCa channels were activated by an increase in [Ca2+]i with an EC50 of 1.5 microM and a Hill coefficient of 1.3. 5. P2 purinoceptor agonists 2-methylthioATP (2-MeSATP), 2-chloroATP and ATP (10-50 microM) increased an apamin-sensitive whole-cell outward K+ current. Extrapatch application of 2-MeSATP (20-100 microM) stimulated the apamin-sensitive IKCa and SKCa channels and activated an apamin-sensitive steady outward current at 0 mV. 6. Smooth muscle cells from the mouse ileum possess two apamin-sensitive K+ channels (IKCa and SKCa); of these, the IKCa channels are TEA sensitive while the SKCa channels are TEA resistant. These channels, along with an apamin-sensitive but TEA-resistant steady outward current, may mediate membrane hyperpolarization elicited by purinergic agonists.

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Selected References

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  1. Auguste P., Hugues M., Borsotto M., Thibault J., Romey G., Coppola T., Lazdunski M. Characterization and partial purification from pheochromocytoma cells of an endogenous equivalent of scyllatoxin, a scorpion toxin which blocks small conductance Ca(2+)-activated K+ channels. Brain Res. 1992 Dec 25;599(2):230–236. doi: 10.1016/0006-8993(92)90396-q. [DOI] [PubMed] [Google Scholar]
  2. Banks B. E., Brown C., Burgess G. M., Burnstock G., Claret M., Cocks T. M., Jenkinson D. H. Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Nature. 1979 Nov 22;282(5737):415–417. doi: 10.1038/282415a0. [DOI] [PubMed] [Google Scholar]
  3. Bauer V., Kuriyama H. The nature of non-cholinergic, non-adrenergic transmission in longitudinal and circular muscles of the guinea-pig ileum. J Physiol. 1982 Nov;332:375–391. doi: 10.1113/jphysiol.1982.sp014419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benham C. D., Bolton T. B., Lang R. J., Takewaki T. The mechanism of action of Ba2+ and TEA on single Ca2+-activated K+ -channels in arterial and intestinal smooth muscle cell membranes. Pflugers Arch. 1985 Feb;403(2):120–127. doi: 10.1007/BF00584088. [DOI] [PubMed] [Google Scholar]
  5. Bennett M. R., Burnstock G., Holman M. E. Transmission from perivascular inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol. 1966 Feb;182(3):527–540. doi: 10.1113/jphysiol.1966.sp007835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blatz A. L., Magleby K. L. Single apamin-blocked Ca-activated K+ channels of small conductance in cultured rat skeletal muscle. Nature. 1986 Oct 23;323(6090):718–720. doi: 10.1038/323718a0. [DOI] [PubMed] [Google Scholar]
  7. Boarder M. R., Weisman G. A., Turner J. T., Wilkinson G. F. G protein-coupled P2 purinoceptors: from molecular biology to functional responses. Trends Pharmacol Sci. 1995 Apr;16(4):133–139. doi: 10.1016/s0165-6147(00)89001-x. [DOI] [PubMed] [Google Scholar]
  8. Bywater R. A., Taylor G. S. Non-cholinergic excitatory and inhibitory junction potentials in the circular smooth muscle of the guinea-pig ileum. J Physiol. 1986 May;374:153–164. doi: 10.1113/jphysiol.1986.sp016072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Capiod T., Ogden D. C. The properties of calcium-activated potassium ion channels in guinea-pig isolated hepatocytes. J Physiol. 1989 Feb;409:285–295. doi: 10.1113/jphysiol.1989.sp017497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carl A., Sanders K. M. Ca2+-activated K channels of canine colonic myocytes. Am J Physiol. 1989 Sep;257(3 Pt 1):C470–C480. doi: 10.1152/ajpcell.1989.257.3.C470. [DOI] [PubMed] [Google Scholar]
  11. Crist J. R., He X. D., Goyal R. K. Both ATP and the peptide VIP are inhibitory neurotransmitters in guinea-pig ileum circular muscle. J Physiol. 1992 Feb;447:119–131. doi: 10.1113/jphysiol.1992.sp018994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gebremedhin D., Kaldunski M., Jacobs E. R., Harder D. R., Roman R. J. Coexistence of two types of Ca(2+)-activated K+ channels in rat renal arterioles. Am J Physiol. 1996 Jan;270(1 Pt 2):F69–F81. doi: 10.1152/ajprenal.1996.270.1.F69. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. He X. D., Goyal R. K. Nitric oxide involvement in the peptide VIP-associated inhibitory junction potential in the guinea-pig ileum. J Physiol. 1993 Feb;461:485–499. doi: 10.1113/jphysiol.1993.sp019524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hugues M., Duval D., Kitabgi P., Lazdunski M., Vincent J. P. Preparation of a pure monoiodo derivative of the bee venom neurotoxin apamin and its binding properties to rat brain synaptosomes. J Biol Chem. 1982 Mar 25;257(6):2762–2769. [PubMed] [Google Scholar]
  16. Jury J., Boev K. R., Daniel E. E. Nitric oxide mediates outward potassium currents in opossum esophageal circular smooth muscle. Am J Physiol. 1996 Jun;270(6 Pt 1):G932–G938. doi: 10.1152/ajpgi.1996.270.6.G932. [DOI] [PubMed] [Google Scholar]
  17. Koumi S., Sato R., Hayakawa H. Modulation of the delayed rectifier K+ current by apamin in guinea-pig heart. Eur J Pharmacol. 1994 Aug 11;261(1-2):213–216. doi: 10.1016/0014-2999(94)90322-0. [DOI] [PubMed] [Google Scholar]
  18. Koumi S., Sato R., Horikawa T., Aramaki T., Okumura H. Characterization of the calcium-sensitive voltage-gated delayed rectifier potassium channel in isolated guinea pig hepatocytes. J Gen Physiol. 1994 Jul;104(1):147–171. doi: 10.1085/jgp.104.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Köhler M., Hirschberg B., Bond C. T., Kinzie J. M., Marrion N. V., Maylie J., Adelman J. P. Small-conductance, calcium-activated potassium channels from mammalian brain. Science. 1996 Sep 20;273(5282):1709–1714. doi: 10.1126/science.273.5282.1709. [DOI] [PubMed] [Google Scholar]
  20. Latorre R., Oberhauser A., Labarca P., Alvarez O. Varieties of calcium-activated potassium channels. Annu Rev Physiol. 1989;51:385–399. doi: 10.1146/annurev.ph.51.030189.002125. [DOI] [PubMed] [Google Scholar]
  21. Leinders T., Vijverberg H. P. Ca2+ dependence of small Ca(2+)-activated K+ channels in cultured N1E-115 mouse neuroblastoma cells. Pflugers Arch. 1992 Dec;422(3):223–232. doi: 10.1007/BF00376206. [DOI] [PubMed] [Google Scholar]
  22. Merot J., Bidet M., Le Maout S., Tauc M., Poujeol P. Two types of K+ channels in the apical membrane of rabbit proximal tubule in primary culture. Biochim Biophys Acta. 1989 Jan 16;978(1):134–144. doi: 10.1016/0005-2736(89)90508-7. [DOI] [PubMed] [Google Scholar]
  23. Park Y. B. Ion selectivity and gating of small conductance Ca(2+)-activated K+ channels in cultured rat adrenal chromaffin cells. J Physiol. 1994 Dec 15;481(Pt 3):555–570. doi: 10.1113/jphysiol.1994.sp020463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shuba M. F., Vladimirova I. A. Effect of apamin on the electrical responses of smooth muscle to adenosine 5'-triphosphate and to non-adrenergic, non-cholinergic nerve stimulation. Neuroscience. 1980;5(5):853–859. doi: 10.1016/0306-4522(80)90154-2. [DOI] [PubMed] [Google Scholar]
  25. Vogalis F., Sanders K. M. Excitatory and inhibitory neural regulation of canine pyloric smooth muscle. Am J Physiol. 1990 Jul;259(1 Pt 1):G125–G133. doi: 10.1152/ajpgi.1990.259.1.G125. [DOI] [PubMed] [Google Scholar]
  26. Yamashita Y., Ogawa H., Akaike N. ATP-induced rise in apamin-sensitive Ca(2+)-dependent K+ conductance in adult rat hepatocytes. Am J Physiol. 1996 Feb;270(2 Pt 1):G307–G313. doi: 10.1152/ajpgi.1996.270.2.G307. [DOI] [PubMed] [Google Scholar]
  27. den Hertog A., Jager L. P. Ion fluxes during the inhibitory junction potential in the guinea-pig taenia coli. J Physiol. 1975 Sep;250(3):681–691. doi: 10.1113/jphysiol.1975.sp011077. [DOI] [PMC free article] [PubMed] [Google Scholar]

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