Skip to main content
SpringerLink
Log in

Tolbutamide-sensitive potassium conductance in the basolateral membrane of A6 cells

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

K+ channels sensitive to intracellular ATP (KATP channels) have been described in a number of cell types and are selectively inhibited by sulfonylurea drugs. To look for the presence of this type of K+ channel in the basolateral membrane of tight epithelia, we have used an amphibian renal cell line, the A6 cells, grown on filters. After the selective permeabilization of the apical membrane with amphotericin B, the basolateral conductance was studied under voltage-clamp conditions. Tolbutamide inhibited 65.8 ± 6.3% of the barium-sensitive current. The tolbutamide-sensitive conductance had an equilibrium potential of −83 ± 1 mV and was inward rectifying in spite of the outwardly directed K+ gradient. Similar results were obtained with glibenclamide. The half-inhibition constants were 25.7 ± 3.0 μm and 0.114 ± 0.018 μm for tolbutamide and glibenclamide respectively. To study the relation between cellular ATP and the activity of this conductance, A6 cells were treated with glucose (5 mm) and insulin (250 μU/ml). This maneuver significantly increased the cellular ATP and abolished the tolbutamide-sensitive conductance. A sulfonylurea-sensitive K+ conductance is present and active in the basolateral membrane of A6 cells. This conductance appears to be modulated by physiological changes of intracellular ATP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ashcroft, F.M., Harrison, D.E., Ashcroft, S.J.H. 1984. Glucose induces closure of single potassium channels in isolated rat pancreatic β-cells. Nature 312:446–448

    Google Scholar 

  • Ashford, M.L.J., Sturgess, N.C., Trout, N.J., Gardner, N.J., Hales, C.N. 1988. Adenosine 5'-triphosphate-sensitive ion channels in neonatal rat cultured central neurons. Pfluegers Arch. 412:297–304

    Google Scholar 

  • Beech, D.J., Bolton, T.B. 1989. Properties of the cromakalim-induced potassium conductance in smooth muscle cells isolated from the rabbit portal vein. Br. J. Pharmacol. 98:851–864

    Google Scholar 

  • Belles, B., Hescheler, J., Trube, G. 1987. Changes of membrane currents in cardiac cells induced by long whole-cell recordings and tolbutamide. Pfluegers Arch. 409:582–588

    Google Scholar 

  • Broillet, M.-C., Horisberger, J.-D. 1991. Basolateral membrane potassium conductance of A6 cells. J. Membrane Biol. 124:1–12

    Google Scholar 

  • Castle, N.A., Haylett, D.G. 1987. Effect of channel blockers on potassium efflux from metabolically exhausted frog skeletal muscle. J. Physiol. 383:31–43

    Google Scholar 

  • Cook, D.L., Hales, C.N. 1984. Intracellular ATP directly blocks K+ channels in pancreatic β-cells. Nature 311:271–273

    Google Scholar 

  • Davies, N.W., Standen, N.B., Stanfield, P.R. 1991. ATP-dependent potassium channels of muscle cells: Their properties, regulation, and possible functions. J. Bioenerg. Biomembr. 23:509–535

    Google Scholar 

  • Dawson, D.C. 1987. Properties of epithelial potassium channels. Curr. Topics Membr. Trans. 28:41–71

    Google Scholar 

  • Eveloff, J.L., Warnock, D.G. 1987. Activation of ion transport systems during cell volume regulation. Am. J. Physiol. 252:F1-F10

    Google Scholar 

  • Fidelman, M.L., May, J.M., Biber, T.U.L., Watlington, C.O. 1982. Insulin Stimulation of Na transport and glucose metabolism in cultured kidney cells. Am. J. Physiol. 242:C121-C123

    Google Scholar 

  • Findlay, I. 1987. ATP-sensitive K+ channels in rat ventricular myocytes are blocked and inactivated by internal divalent cations. Pfluegers Arch. 410:313–320

    Google Scholar 

  • Germann, W.J., Ernst, S.A., Dawson, D.C. 1986. Resting and osmotically induced basolateral K conductances in turtle colon. J. Gen. Physiol. 88:253–274

    Google Scholar 

  • Handler, J.S., Steele, R.E., Sahib, M.K., Wade, J.B., Preston, A.S., Lawson, N.L., Johnson, J.P. 1979. Toad urinary bladder epithelial cells in culture: maintenance of epithelial structure, sodium transport, and response to hormones. Proc. Natl. Acad. Sci. USA 76:4151–4155

    Google Scholar 

  • Kovacs, R.J., Nelson, M.T. 1991. ATP-sensitive K+ channels from aortic smooth muscle incorporated into planar lipid bilayers. Am. J. Physiol. 261:H604-H609

    Google Scholar 

  • Lowry, O.H., Rosebrough, A.L., Farr, A.L., Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275

    CAS  PubMed  Google Scholar 

  • Misler, S., Gillis, K., Tabcharani, J. 1989. Modulation of gating of a metabolically regulated, ATP-dependent K+ channel by intracellular pH in β cells of the pancreatic islet. J. Membrane Biol. 109:135–143

    Google Scholar 

  • Mourre, C., Widmann, C., Lazdunski, M. 1990. Sulfonylurea binding sites associated with ATP-regulated K+ channels in the central nervous system: Autoradiographic analysis of their distribution and ontogenesis, and of their localization in mutant mice cerebellum. Brain Res. 519:29–43

    Google Scholar 

  • Nelder, J.A., Mead, R. 1965. A simplex method for function minimization. Comput. J. 7:308–313

    Google Scholar 

  • Nichols, C.G., Lederer, W.J. 1991. Adenosine triphosphatesensitive potassium channels in the cardiovascular system. Am. J. Physiol. 261:H1675-H1686

    Google Scholar 

  • Nichols, C.G., Ripoll, C., Lederer, W.J. 1991. ATP-sensitive potassium channel modulation of the guinea pig ventricular action potential and contraction. Circ. Res. 68:280–287

    Google Scholar 

  • Nielsen, R. 1979. A 3 to 2 coupling of the Na-K pump responsible for the transepithelial Na transport in frog skin disclosed by the effect of Ba. Acta Physiol. Scand. 107:189–191

    Google Scholar 

  • Noma, A. 1983. ATP-regulated K+ channels in cardiac muscle. Nature 305:147–148

    Google Scholar 

  • Pfaller, W., Guder, W.G., Gstraunthaler, G., Kotanko, P., Jehart, I., Pürschel, S. 1984. Compartmentation of ATP within renal proximal tubular cells. Biochim. Biophys. Acta 805:152–157

    Google Scholar 

  • Ribalet, B., Ciani, S. 1987. Regulation by cell metabolism and adenine nucleotides of a K channel in insulin-secreting β cells (RIN m5F). Proc. Natl. Acad. Sci. USA 84:1721–1725

    Google Scholar 

  • Satoh, K., Yamada, H., Taira, N. 1991. Differential antagonism by glibenclamide of the relaxant effects of cromakalim, pinacidil and nicorandil on canine large coronary arteries. Naunyn Schmiedebergs Arch. Pharmacol. 343:76–82

    Google Scholar 

  • Standen, N.B., Quayle, J.M., Davies, N.W., Brayden, J.E., Huang, Y., Nelson, M.T. 1989. Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science 245:177–180

    Google Scholar 

  • Sturgess, N.C., Ashford, M.L.J., Cook, D.L., Hales, C.N. 1985. The sulfonylurea receptor may be an ATP-sensitive potassium channel. Lancet ii:474–475

    Google Scholar 

  • Thore, A. 1979. Technical aspects of the bioluminescent firefly luciferase assay of ATP. Science Tools 26(2):30–35

    Google Scholar 

  • Tousson, A., Alley, C.D., Sorscher, E.J., Brinkley, B.R., Benos, D.J. 1989. Immunochemical localization of amiloride-sensitive sodium channels in sodium-transporting epithelia. J. Cell. Sci. 93:349–362

    Google Scholar 

  • Trube, G.P., Hescheler, J. 1984. Inward-rectifying channels in isolated patches of heart cell membrane: ATP-dependence and comparison with cell-attached patches. Pfluegers Arch. 401:178–184

    Google Scholar 

  • Trube, G.P., Rorsman, P., Ohno-Shoshaku, T. 1986. Opposite effects of tolbutamide and diazoxide on ATP-dependent K+ channel in mouse pancreatic β-cells. Pfluegers Arch. 407:493–499

    Google Scholar 

  • Tsuchiya, K., Wang, W., Giebisch, G., Welling, P.A. 1992. ATP is a coupling-modulator of parallel Na/K ATPase-K channel activity in the renal proximal tubule. Proc. Natl. Acad. Sci. USA 89:6418–6422

    Google Scholar 

  • Uchida, S., Endou, H. 1988. Substrate specificity to maintain cellular ATP along the mouse nephron. Am. J. Physiol. 24:F977-F983

    Google Scholar 

  • Verrey, F., Schaerer, E., Zoerkler, P., Paccolat, M.P., Geering, K., Kraehenbuhl, J.-P., Rossier, B.C. 1987. Regulation by aldosterone of Na+, K+-ATPase mRNAs, protein synthesis, and sodium transport in cultured kidney cells. J. Cell. Biol. 104:1231–1237

    Google Scholar 

  • Wang, W., Schwab, A., Giebisch, G. 1990. Regulation of smallconductance K+ channel in apical membrane of rat cortical collecting tubule. Am. J. Physiol. 259:F494-F502

    Google Scholar 

  • Wang, W., White, S., Geibel, J., Giebisch, G. 1990. A potassium channel in the apical membrane of rabbit thick ascending limb of Henle's loop. Am. J. Physiol. 258:F244-F253

    Google Scholar 

  • Wang, W., Sackin, H., Giebisch, G. 1992. Renal potassium channels and their regulation. Annu. Rev. Physiol. 54:81–96

    Google Scholar 

  • Woll, K.H., Lönnendonker, U., Neumcke, B. 1989. ATP-sensitive potassium channels in adult mouse skeletal muscle: Different modes of blockage by internal cations, ATP and tolbutamide. Pfluegers Arch. 414:622–628

    Google Scholar 

  • Zünkler, B.J., Lenzen, S., Männer, K., Panten, U., Trube, G. 1988. Concentration-dependent effects of tolbutamide, meglitinide, glipizide, glibenclamide and diazoxide on ATP-regulated K+-current in pancreatic B-cells. Naunyn-Schmiedbergs Arch. Pharmacol. 337:225–230

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Pharmacologie, Université de Lausanne, Lausanne, Switzerland

    Marie-Christine Broillet & Jean-Daniel Horisberger

Authors
  1. Marie-Christine Broillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Daniel Horisberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

We are very grateful to Prof. Dr. B.C. Rossier, Dr. L. Schild and Dr. P. Matthews for their careful reading of the manuscript. This work was supported by the Swiss Science Foundation, Grant 31-27798.89.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Broillet, MC., Horisberger, JD. Tolbutamide-sensitive potassium conductance in the basolateral membrane of A6 cells. J. Membarin Biol. 134, 181–188 (1993). https://doi.org/10.1007/BF00234499

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00234499

Key words

Search

Navigation