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Sodium channels contribute to action potential generation in canine and human pancreatic islet B cells

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Summary

Pancreatic islet B cells depolarize and display trains of action potentials in response to stimulatory concentrations of glucose. Based on data from rodent islets these action potentials are considered to be predominantly Ca2+ dependent. Here we describe Na+-dependent action potentials and Na+ currents recorded from canine and human pancreatic islet B cells. Current-clamp recording using the nystatin “perforated-patch” technique demonstrates that B cells from both species display tetrodotoxin-sensitive Na+ action potentials in response to modest glucose-induced depolarization. In companion “whole-cell” voltage-clamp experiments on canine B cells, the underlying Na+ current displays steep voltage-dependent activation and inactivation over the range of −50 to −40 mV. The Na+ current is sensitive to tetrodotoxin block with aK 1=3.2nm and has a reversal potential which changes with [Na+] o as predicted by the Nernst equation. These results suggest that a voltage-dependent Na+ current may contribute significantly to action potential generation in some species outside the rodent family.

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References

  • Eddlestone, G.T., Goncalves, A., Bangham, J.A., Rojas, E. 1984. Electrical coupling between cells in islets of Langerhans from mouse.J. Membrane Biol. 77: 1–14

    Google Scholar 

  • Falke, L.C., Gillis, K.D., Pressel, D.M., Misler, S. 1989. ‘Perforated patch recording’ allows long-term monitoring of metabolite-induced electrical activity and voltage-dependent Ca2+ currents in pancreatic islet B cells.FEBS Lett. 251: 167–172

    PubMed  Google Scholar 

  • Findlay, I., Ashcroft, F.M., Kelly, R.P., Rorsman, P., Petersen, O.H., Trube, G. 1989. Calcium currents in insulin-secreting B-cells.Ann. NY Acad. Sci. 560: 403–409

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hille, B. 1984. Ionic channels of excitable membranes. Sinauer Associates, Sunderland (MA)

    Google Scholar 

  • Hiriart, M., Matteson, D.R. 1988. Na channels and two types of Ca channels in rat pancreatic B cells identified with the reverse hemolytic plaque assay.J. Gen. Physiol. 67: 617–639

    Google Scholar 

  • Horn, R., Marty, A. 1988. Muscarinic activation of ionic currents measured by a new whole-cell recording method.J. Gen. Physiol. 92: 145–159

    PubMed  Google Scholar 

  • Llinas, R., Steinberg, I.Z., Walton, K. 1981. Presynaptic calcium currents in squid giant synapse.Biophys. J. 33: 289–322

    PubMed  Google Scholar 

  • McCleskey, E.W., Fox, A., Feldman, D., Tsien, R.W. 1986. Different types of calcium channels.J. Exp. Biol. 124: 177–190

    PubMed  Google Scholar 

  • Meissner, H.P., Preissler, H. 1980. Ionic mechanism of glucose-induced membrane potential changes in B cells.In: Biochemistry and Biophysics of the Pancreatic B-cell. W.J. Malaisse, and I.-B. Taljedal, editors. pp. 91–99. Thierne-Stratton, New York

    Google Scholar 

  • Misler, S., Falke, L. C., Gillis, K.D., McDaniel, M.L. 1986. A metabolite-regulated potassium channel in rat pancreatic B cells.Proc. Natl. Acad. Sci. USA 83: 7119–7123

    PubMed  Google Scholar 

  • Misler, S., Gee, W.M., Gillis, K.D., Scharp, D.W., Falke, L.C. 1989. Metabolite-regulated ATP-sensitive K+ channel in human pancreatic islet cells.Diabetes 38: 422–427

    PubMed  Google Scholar 

  • Pace, C.S. 1979. Activation of Na+ channels in islet cells: Metabolic and secretory effects.Am. J. Physiol. 237: 130–135

    Google Scholar 

  • Petersen, O.H., Findlay, I. 1987. Electrophysiology of the pancreas.Physiol. Rev. 67: 1054–1116

    PubMed  Google Scholar 

  • Plant, T.D. 1988. Na+ currents in cultured mouse pancreatic B-cells.Pfluegers Arch. 411: 429–435

    Google Scholar 

  • Pressel, D.M., Misler, S. 1989. Ion channel currents in canine pancreatic islet B cells.Biophys. J. 55: 540a

    Google Scholar 

  • Pressel, D.M., Misler, S. 1990. Sodium currents in pancreatic islet B cells.Biophys. J. 57: 104a

    Google Scholar 

  • Ribalet, B., Beigelman, P.M. 1981. Effect of sodium on beta-cell electrical activity.Am. J. Physiol. 242: 296–303

    Google Scholar 

  • Ricordi, C., Lacy, P.E., Finke, E.H., Olack, B.J., Scharp, D.W. 1988. Automated method for isolation of human pancreatic islets.Diabetes 37: 413–420

    PubMed  Google Scholar 

  • Rorsman, P., Arkhammar, P., Berggren, P.O. 1986. Voltage-activated Na+ currents and their suppression by phorbol ester in clonal insulin producing RINm5F cells.Am. J. Physiol. 251: 912–919

    Google Scholar 

  • Rorsman, P., Ashcroft, F.M., Trube, G. 1988. Single Ca2+ channel currents in mouse pancreatic B-cells.Pfluegers Arch. 412: 597–603

    Google Scholar 

  • Rorsman, P., Hellman, B. 1988. Voltage-activated currents in guinea pig pancreatic alpha 2 cells.J. Gen. Physiol. 91: 223–242

    PubMed  Google Scholar 

  • Rorsman, P., Trube, G. 1986. Calcium and delayed potassium currents in mouse pancreatic B-cells under voltage-clamp conditions.J. Physiol. (London) 374: 531–550

    Google Scholar 

  • Satin, L.S., Cook, D.L. 1988. Evidence for two calcium currents in insulin-secreting cells.Pfluegers Arch. 411: 401–409

    Google Scholar 

  • Tabcharani, J., Falke, L., Misler, S. 1988. Interaction of ions with a metabolically regulated K+ channel in pancreatic islet B cells.Biophys. J. 53: 157a

    Google Scholar 

  • Tarvin, J.T., Pace, C.S. 1981. Glucose-induced electrical activity in pancreatic B cell: Effect of veratridine.Am. J. Physiol. 240: C127–134

    PubMed  Google Scholar 

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Pressel, D.M., Misler, S. Sodium channels contribute to action potential generation in canine and human pancreatic islet B cells. J. Membrain Biol. 116, 273–280 (1990). https://doi.org/10.1007/BF01868466

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