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Characterization of a 25-pS nonselective cation channel in a cultured secretory epithelial cell line

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We have studied a 25-pS nonselective cation channel from the apical membranes of cell line ST885, derived from neonatal mouse mandibular glands. Its Cl− permeability was not significantly different from zero. The permeabilities (relative to Na+) for inorganic cations were NH +4 (1.87)>K+(1.12)>Li+ (1.02)>Na+(1)>Rb+(0.81)>Mg2+(0.07)>Ca2+(0.002), and for organic cations, guanidinium (1.61)<ethanolamine (0.70)>4-aminopyridine (0.66)>diethylamine (0.54)>piperazine (0.25)>Tris (0.18)>N-methylglucamine (0.12). The Tris and N-methylglucamine permeabilities differed significantly from zero. Fitting the Renkin equation indicated that the channel had an equivalent pore radius of 0.49 nm. The channel was activated by Ca2+ on the cytosolic surface (>0.1 mmol/liter) with a Hill coefficient of 1.2; it was also activated by depolarization. Open- and closed-time histograms indicated that it had at least two open and two closed states. The channel was blocked by cytosolic AMP or ATP (0.1 mmol/liter). It was also blocked by the Cl− channel blocker, diphenylamine-2-carboxylate (DPC; 0.1 mmol/liter), applied to the extracellular but not the cytosolic surface. 4-Aminopyridine, which permeated the channel when applied to the extracellular surface, blocked it when applied in low concentrations (5 mmol/liter) to the cytosolic surface. Quinine (0.1 mmol/liter) blocked from both the extracellular and cytosolic surfaces, blockade from either side being enhanced by depolarization. The channel was held open by application of SITS (0.1 mmol/liter) to the cytosolic surface. The channel shows striking similarities to the nicotinic acetylcholine receptor channel,viz., both channel types are abnormally permeable to 4-aminopyridine applied externally, and their selectivity sequences for inorganic ions are similar and for organic cations are identical.

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References

  1. Adams, D.J., Dwyer, T.M., Hille, B. 1980. The permeability of endplate channels to monovalent and divalent metal cations.J. Gen. Physiol. 75:493–510

    Google Scholar 

  2. Barry, P.H., Gage, P.W. 1984. Ionic selectivity of channels at the end plate.In: Ion Channels: Molecular and Physiological AspectsCurr. Topics Membr. Transport 21:1–51

  3. Bevan, S., Gray, P.T.A., Ritchie, J.M. 1984. A calcium-activated cation-selective channel in rat cultured Schwann cells.Proc. R. Soc. Lond. [Biol.] 222:349–355

    Google Scholar 

  4. Bezanilla, F. 1985. A high capacity data recording device based on a digital audio processor and a video cassette recorder.Biophys. J. 47:437–441

    Google Scholar 

  5. Colquhoun, D., Hawkes, A.G. 1983. The principles of the stochastic interpretation of ion-channel mechanisms.In: Single-Channel Recording. B. Sakmann and E. Neher, editors. pp. 135–175. Plenum, New York

    Google Scholar 

  6. Colquhoun, D., Neher, E., Reuter, H., Stevens, C.F. 1981. Inward current channels activated by intracellular Ca in cultured cardiac cells.Nature (London) 294:752–754

    Google Scholar 

  7. Cook, D.I., Towner, S.P., Young, J.A. 1986. Patch-clamp studies of cultured salivary cells.Biomed. Res. 7 (Suppl. 2):203–207

    Google Scholar 

  8. Cook, D.I., Young, J.A. 1989. The effect of K+ channels in the apical plasma membrane on epithelial secretion based on secondary active Cl− transport.J. Membrane Biol. 110:139–146

    Google Scholar 

  9. Dwyer, T.M., Adams, D.J., Hille, B. 1980. The permeability of the endplate channel to organic cations in frog muscle.J. Gen. Physiol. 75:469–492

    Google Scholar 

  10. Ehara, T., Noma, A., Ono, K. 1988. Calcium-activated non-selective cation channel in ventricular cells isolated from adult guinea-pig hearts.J. Physiol. (London) 403:117–134

    Google Scholar 

  11. Gögelein, H., Pfannmüller, B. 1988. The nonselective cation channel in the basolateral membrane of rat exocrine pancreas. Inhibition by 3′,5′-dichlorodiphenylamine-2-carboxylic acid (DCDPC).Pfluegers Arch. 413:287–298

    Google Scholar 

  12. Gray, M.A., Greenwell, J.R., Argent, B.E. 1988. Ion channels in pancreatic duct cells and their role in bicarbonate secretion.In: Exocrine Secretion. P.Y.D. Wong and J.A. Young, editors. pp. 77–80. Hong Kong University Press, Hong Kong

    Google Scholar 

  13. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.S. 1981. Improved patch-clamp techniques for high resolution current recording from cells and cell free membrane patches.Pfluegers Arch. 391:85–100

    Google Scholar 

  14. Krouse, M.E., Hagiwara, G., Chen, J., Lewiston, N.L., Wine, J.J. 1988. Ion channels in normal and cystic fibrosis cultured sweat gland cells.In: Exocrine Secretion. P.Y.D. Wong and J.A. Young, editors. pp. 99–102. Hong Kong University Press, Hong Kong

    Google Scholar 

  15. Martin, D.K., Cook, D.I., Young, J.A. 1989. A direct-reading device for measurement of micropipette diameters.Proc. Aust. Physiol. Pharmacol. Soc. 20:171P

    Google Scholar 

  16. Marty, A., Tan, Y.P., Trautmann, A. 1984. Three types of calcium-dependent channels in rat lacrimal glands.J. Physiol. (London) 357:293–325

    Google Scholar 

  17. Maruyama, Y., Gallacher, D.V., Petersen, O.H. 1983. Voltage and Ca2+-activated K+ channel in basolateral acinar cell membranes in mammalian salivary glands.Nature (London) 302:827–829

    Google Scholar 

  18. Maruyama, Y., Moore, D., Petersen, O.H. 1985. Calcium-activated cation channel in rat thyroid follicular cells.Biochim. Biophys. Acta 821:229–232

    Google Scholar 

  19. Maruyama, Y., Petersen, O.H. 1982. Cholecystokinin activation of single-channel currents is mediated by an internal messenger in pancreatic acinar cells.Nature (London) 300:61–63

    Google Scholar 

  20. Maruyama, Y., Peterson, O.H. 1982. Single-channel currents in isolated patches of plasma membrane from basal surface of pancreatic acini.Nature (London) 299:159–161

    Google Scholar 

  21. Maruyama, Y., Petersen, O.H. 1984. Single calcium-dependent cation channels in mouse pancreatic acinar cells.J. Membrane Biol. 81:83–87

    Google Scholar 

  22. Mittman, S., Flaming, D.G., Copenhagen, D.R., Belgum, J.H. 1987. Bubble pressure measurement of micropipette tip outer diameter.J. Neurosci. Methods 22:161–166

    Google Scholar 

  23. Neter, J., Wasserman, W. 1974. Applied Linear Statistical Models. Regression, Analysis of Variance, and Experimental Designs. Richard D. Irwin, Homewood (IL)

    Google Scholar 

  24. Partridge, L.D., Swandulla, D. 1987. Single Ca-activated cation channels in bursting neurone ofHelix.Pfluegers Arch. 410:627–631

    Google Scholar 

  25. Partridge, L.D., Swandulla, D. 1988. Calcium-activated non-specific cation channels.Trends Neurosci. 11:69–72

    Google Scholar 

  26. Petersen, O.H., Maruyama, Y. 1983. What is the mechanism of the calcium influx to pancreatic acinar cells evoked by secretagogues.Pfluegers Arch. 396:82–84

    Google Scholar 

  27. Petersen, O.H., Maruyama, Y. 1984. Calcium-activated potassium channels and their role in secretion.Nature (London) 307:693–696

    Google Scholar 

  28. Poronnik, P., Cook, D.I., Young, J.A. 1988. The use of Cytodex® microcarrier beads in patch-clamp studies on cultured epithelial cells.Pfluegers Arch. 413:90–92

    Google Scholar 

  29. Renkin, E.M., Curry, F.E. 1979. Transport of water and solutes across capillary endothelium.In: Membrane Transport in Biology. G. Giebisch, editor. Vol. IVA (Transport Organs). pp. 1–45. Springer-Verlag, Berlin

    Google Scholar 

  30. Robinson, R.A., Stokes, R.H. 1965. Electrolyte Solutions. (2nd Ed. Butterworths, London

    Google Scholar 

  31. Sachs, F., Neil, J., Barkakati, N. 1982. The automated analysis of data from single ionic channels.Pfluegers Arch. 395:331–340

    Google Scholar 

  32. Sanchez, J.G., Dani, J.A., Siemen, D., Hille, B. 1986. Slow permeation of organic cations in acetylcholine receptor channels.J. Gen. Physiol. 87:985–1001

    Google Scholar 

  33. Siemen, D., Reuhl, T. 1987. Non-selective cationic channel in primary cultured cells of brown adipose tissue.Pfluegers Arch. 408:534–536

    Google Scholar 

  34. Silva, P., Stoff, J., Field, M., Fine, L., Forrest, J.N., Epstein, F.J. 1977. Mechanism of active chloride secretion by shark rectal gland: Role of Na−K-ATPase in chloride transport.Am. J. Physiol. 233:F298-F306

    Google Scholar 

  35. Sturgess, N.C., Hales, C.N., Ashford, M.L.J. 1987 Calcium and ATP regulate the activity of a non-selective cation channel in a rat insulinoma cell line.Pfluegers Arch. 409:607–615

    Google Scholar 

  36. Suzuki, K., Petersen, O.H. 1988. Patch-clamp study of single channel and whole cell K+ currents in guinea pig pancreatic acinar cells.Am. J. Physiol. 255:G275-G285

    Google Scholar 

  37. Takeda, K., Gage, P.W., Barry, P.H. 1982. Effects of divalent cations on toad end-plate channels.J. Membrane Biol. 64:55–66

    Google Scholar 

  38. Von Tscharner, V., Prod'hon, B., Baggiolini, B., Reuter, H. 1986. Ion channels in human neutrophils activated by a rise in cytosolic calcium concentration.Nature (London) 324:369–372

    Google Scholar 

  39. Yellen, G. 1982. Single Ca2+-activated nonselective cation channels in neuroblastoma.Nature (London) 296:357–359

    Google Scholar 

  40. Young, J.A., Cook, D.I., Van Lennep, E.W., Roberts, M.L. 1987. Secretion by the major salivary glands.In: Physiology of the Gastrointestinal Tract. (2nd Ed.) L. Johnson, J. Christensen, M. Jackson, E. Jacobson, and J. Walsh, editors, Vol. 2, pp. 773–815. Raven, New York

    Google Scholar 

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  1. Department of Physiology, University of Sydney, 2006, NSW, Australia

    D. I. Cook, P. Poronnik & J. A. Young

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Cook, D.I., Poronnik, P. & Young, J.A. Characterization of a 25-pS nonselective cation channel in a cultured secretory epithelial cell line. J. Membrain Biol. 114, 37–52 (1990). https://doi.org/10.1007/BF01869383

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