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Effects of internal ph on the nonselective cation channel from the mouse collecting tubule

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Abstract

We investigated the effects of internal pH on Ca-activated, nucleotide-inhibited nonselective cation channels in the basolateral membranes of mouse collecting tubules, using the inside-out variant of the patch clamp technique. pH modulated the channel open probability (P o ), giving a bell-shaped curve peaking at pH 6.8/7.0: P o at pH 6.0 was 11±6% of P o at pH 7.2 and 32 ±7% at pH 8.0. The open and closed time distributions, best fitted to the sum of two exponentials, were differently sensitive to acid and alkaline conditions. Low pH reduced the short and long open times to 38 and 24% of their pH 7.2 values, while high pH produced a 4-fold increase in the long closed time. As previously reported, 4-acetamido-4′-isothiocyanatostilbene-2,2′-disulfonic acid (SITS) induced a quasi-permanent opening of the channel. The inhibition of the channel produced by high pH disappeared in the presence of SITS, while the inhibition produced by low pH was unaffected. These results suggest that the pH dependence of the channel is due to two separate mechanisms. pH was without effect on the ATP-evoked inhibition of the channel, while high pH profoundly reduced the steepness of the AMP inhibition curve, without altering the half-maximal inhibitory AMP concentration.

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References

  1. 1.

    Bleich, M., Schlatter, E., Greger, R. 1991. The luminal K+ channel of the thick ascending limb of Henle's loop. Pfluegers Arch. 415:449–460

  2. 2.

    Chraïbi, A., Van Den Abbeele, T., Guinamard, R., Teulon, J. 1994. A ubiquitous non-selective cation channel in the mouse renal tubule with variable sensitivity to calcium. Pfluegers Arch. 429:90–97

  3. 3.

    Christensen, O., Zeuthen, T. 1987. Maxi K+ channels in leaky epithelia are regulated by intracellular Ca-2+, pH and membrane potential. Pfluegers Arch. 408:249–259

  4. 4.

    Colquhoun, D., Neher, E., Reuter, H., Stevens, C.F. 1981. Inward current channels activated by intracellular Ca in cultured cardiac cells. Nature 314:752–754

  5. 5.

    Cook, D.L., Ikenchi, M., Fujimoto, W.Y. 1984. Lowering of pH; inhibits Ca-2+-activated K+ channel in pancreatic β-cells. Nature 311:269–273

  6. 6.

    Cook, D.I., Poronnick, P., Young, J.A. 1990. Characterization of a 25-pS non selective cation channel in a cultured secretory epithelial cell line. J. Membrane Biol. 114:37–52

  7. 7.

    Davies, N.N. 1990. Modulation of ATP-sensitive K+ channels in skeletal muscle by intracellular protons. Nature 343:375–368

  8. 8.

    Davies, N.N., Standen, N.B., Stanfield, P.R. 1992. The effect of intracellular pH on ATP-dependent potassium channels of frog skeletal muscle. J. Physiol. 445:549–568

  9. 9.

    Fabiato, A. 1981. Myoplasmic free calcium concentration reached during the twitch of an intact-isolated cardiac cell and during calcium-induced released from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricule. J. Gen. Physiol 78:457–497

  10. 10.

    Gögelein, H., Pfanmüller, B. 1989. The nonselective cation channel in the basolateral membrane of rat exocrine pancreas: inhibition by 3′,5-dichlorodiphenylamine-2-carbolxylic acid (DCDPC) and activation by the stilbene disulfonate. Pfluegers Arch. 413:289–298

  11. 11.

    Gray, M.A., Argent, B.E. 1990. Non-selective cation channel pancreatic duct cells. Biochim. Biophys. Acta 1029:33–42

  12. 12.

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

  13. 13.

    Lederer, W.J., Nichols, G.G. 1989. Nucleotide modulation of the activity of rat heart ATP-sensitive K+ channels in isolated membrane patches. J. Physiol. 419:193–211

  14. 14.

    Martell, A.E., Smith, R.L. 1974. Critical stability constants. Vol 1. Plenum Press, New York

  15. 15.

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

  16. 16.

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

  17. 17.

    Mérot, J., Bidet M., Gachot, B., Le Maout, S., Tauc, M., Poujeol, P. 1988. Patch-clamp study on primary culture of isolated proximal convoluted tubules. Pfluegers Arch. 413:51–61

  18. 18.

    Miller, C., White, M.M. 1980. A voltage-dependent chloride conductance channel from torpedo electroplax membrane. Ann NY Acad. Sci. 341:534–551

  19. 19.

    Palmer, L.G., Frindt, G. 1987. Effects of cell Ca and pH on Na channels from rat cortical collecting tubule. Am. J. Physiol. 253:F333-F339

  20. 20.

    Ohno-Shosaku, T., Kubota, T., Yamaguchi, J., Fujimoto, M. 1990. Regulation of inwardly rectifying K+ channels by intracellular pH in opossum kidney cells. Pfluegers Arch. 416:138–143

  21. 21.

    Paulais, M., Teulon, J. 1989. A cation channel in the thick ascending limb of Henle's loop of the mouse kidney: inhibition by adenine nucleotides. J. Physiol. 413:315–327

  22. 22.

    Razani-Boroujerdi, S., Partridge, L.D. 1993. Activation and modulation of calcium-activated non-selective cation channels from ambryom'c chick sensory neurons. Brain Res. 623:195–200

  23. 23.

    Reale, V., Hales, C.N., Ashford, M.L.J. 1994. Nucleotide regulation of a calcium-activated cation channel in the rat insulinoma cell line, CR1-G1. J. Membrane Biol. 141:631–640

  24. 24.

    Sasaki, T., Gallacher, D.V. 1990. Extracellular ATP activates receptor-operated cation channels in mouse lacrimal cells to promote calcium influx in the absence of phosphoinositide metabolism. FEBS Lett. 264:130–134

  25. 25.

    Schlatter, E., Haxelmans, S., Hirsch, J., Leipziger, J. 1994. pH dependence of K+ conductances if rat corical collecting duct principal cells. Pfluegers Arch. 428:631–640

  26. 26.

    Siemen, D. 1993. Nonselective cation channels. In: Nonselective cation channels. Pharmacology, Physiology and Biophysics. D. Siemen and J. Hescheler editors, pp. 3–25 Birkhaüser Verlag, Basel

  27. 27.

    Sturgess, N.C., Hales, C.N., Ashford, M.L.J. 1986. Inhibition of a calcium-activated, non-selective cation channel, in a rat insulinoma cells line, by adenine derivatives. FEBS Lett. 208:397–400

  28. 28.

    Suzuki, N.C., Takahashi, K., Ikeda, M., Hayakawa, H., Ogawa, A., Kawaguchi, Y., Sukai, O. 1994. Cloning of a pH-sensitive K+ channel possessing two transmembrane segments. Nature 367:642–645

  29. 29.

    Swandulla, D., Partridge, L.D. 1990. Non specific Cation Channels in Potassium Channels, Structure, Classification, Function and Therapeutic Potential. N.S. Cook Editor. John Wiley & Sons, New York

  30. 30.

    Teulon, J., Paulais, M., Bouthier, M. 1987. A Ca2+-activated cation-selective channel in the basolateral membrane of the cortical thick ascending limb of Henle's loop of the mouse. Biochim. Biophys. Acta 905:125–132

  31. 31.

    Thorn, P., Petersen, O.H. 1992. Activation of nonselective cation channels by physiological cholecystokinin concentrations in mouse pancreatic acinar cells. J. Gen. Physiol. 100:11–25

  32. 32.

    Van Den Abbeele, T., Tran Ba Huy, P., Teulon, J. 1994. A calcium-activated nonselective cationic channel in the basolateral membrane of outer hair cells of the guinea-pig cochlea. Pfluegers Arch. 417:56–63

  33. 33.

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

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Additional information

We thank M. Blonde for expert technical assistance, and M. Poitou for secretarial help. A. Chraïbi was supported by the French Society of Nephrology, R. Guinamard is the recipient of a MRE research studentship and J. Teulon is a CNRS researcher. The manuscript was edited by Owen Parkes.

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Chraïbi, A., Guinamard, R. & Teulon, J. Effects of internal ph on the nonselective cation channel from the mouse collecting tubule. J. Membarin Biol. 148, 83–90 (1995). https://doi.org/10.1007/BF00234159

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Key words

  • Cation channel
  • pH
  • Nucleotides