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Mechanisms of 1,25(OH)2D3-induced rapid changes of membrane potential in proximal tubule: Role of Ca2+-dependent K+ channels

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Summary

Eleven different secosteroids or steroids (10−10 to 10−8 m) were acutely and reversibly introduced in solutions delivered to the lumen of single proximal tubules of the amphibianNecturus kidney while recording basolateral cell membrane potentialV m. Seven of these molecules (1,25(OH)2D3, 25(OH)D3, 24,25(OH)2D3, 5,6-trans-25(OH)D3, 19-diol-cholesterol, estradiol and testosterone) resulted in changes ofV m (ΔV m) occurring in a few seconds, the largest ΔV m being observed with 1,25(OH)2D3, +6.5±0.75 mV (n=19); these seven (seco)steroids but not the four inactive sterols (vitamin D3, cholesterol, 1αD3 and aldosterone) possess a hydroxyl group on at least one carbon of the C17 to C25 lateral chain of the sterol ring. The ΔV m effect was present in Na+-free or Cl−-free media, but it was abolished in HCO3-free media. Depolarization of cell membrane potential by addition of glucose, 11mm, in luminal perfusion fluid abolished the 1,25(OH)2D3-evoked ΔV m effect, suggesting dependence of the latter on the absolute value of membrane potential. Barium, a blocking agent of K+ conductances, suppressed the 1,25(OH)2D3-evoked ΔV m effect, even when the proper effects of barium of cell membrane potential were canceled by current clamp. Pretreatment with quinine, a putative blocker of Ca2+-dependent K+ channels also abolished the 1,25(OH)2D3-evoked depolarization. Such observations are consistent with the presence of Ca2+-dependent K+ channels at the apical cell membrane of the proximal tubule, these channels being inactivated by 1,25(OH)2D3 and probably by other (seco)steroids.

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References

  1. Anagnostopoulos, T. 1973. Biionic potentials in the proximal tubule ofNecturus kidney.J. Physiol. (London) 233:375–394

    Google Scholar 

  2. Anagnostopoulos, T. 1975. Anion permeation in the proximal tubule ofNecturus kidney: The shunt pathway.J. Membrane Biol. 24:365

    Article  Google Scholar 

  3. Anagnostopoulos, T. 1981. Electrophysiology of the nephron.In: Proc. 8th Int. Congr. Nephrol.. W. Zurukzoglu, M. Papadimitriou, M. Pyrpasopoulos, M. Sion & C. Zamboulis, editors. pp. 39–45. S. Karger, Basel

    Google Scholar 

  4. Anagnostopoulos, T., Edelman, A. 1977. Electrophysiological study of bicarbonate effects on antiluminal membrane at the proximal tubule ofNecturus kidney.J. Physiol. (London) 266:40P-41P

    Google Scholar 

  5. Bello-Reuss, E. 1982. Electrical properties of the basolateral membrane of the straight portion of the rabbit proximal renal tubule.J. Physiol. (London) 326:49–63

    Google Scholar 

  6. Burckhardt, B.C., Sato, K., Frömter, E. 1984. Electrophysiological analysis of bicarbonate permeation across the peritubular cell membrane of rat kidney proximal tubule. I. Basic observations.Pfluegers Arch. 401:34–42

    Google Scholar 

  7. Burges, G.M., Claret, M., Jenkinson, D.H. 1981. Effects of quinine and apamin on the calcium dependent potassium permeability of mammalian hepatocytes and red cells.J. Physiol. (London) 317:67–90

    Google Scholar 

  8. Cook, N.S., Haylett, D.G. 1985. Effects of apamin, quinine and neuromuscular blockers on calcium-activated potassium channels in guinea-pig hepatocytes.J. Physiol. (London) 358:373–394

    Google Scholar 

  9. Dufy, B., Vincent, J.D., Fleury, H., Du Pasquier, P., Gourdji, D., Tixier-Vidal, A. 1979. Membrane effects of thyrotropin-releasing hormone and estrogen shown by intracellular recording by pituitary cells.Science 204:509–511

    PubMed  Google Scholar 

  10. Duval, D., Durant, S., Homo-Delarche, F. 1983. Non-genomic effects of steroids. Interactions of steroid molecules with membrane structures and functions.Biochim. Biophys. Acta 737:409–442

    PubMed  Google Scholar 

  11. Edelman, A., Anagnostopoulos, T. 1978. Further studies of ion permeation in proximal tubule ofNecturus kidney.Am. J. Physiol. 235:F89

    PubMed  Google Scholar 

  12. Edelman, A., Bouthier, M., Anagnostopoulos, T. 1981. Chloride distribution in the proximal convoluted tubule ofNecturus kidney.J. Membrane Biol. 62:7–17

    Google Scholar 

  13. Edelman, A., Teulon, J., Anagnostopoulos, T. 1983. Peculiarities of the Na+/d-glucose cotransport system inNecturus renal tubules.Biochim. Biophys. Acta 731:211–216

    PubMed  Google Scholar 

  14. Edelman, A., Thil, C.L., Garabedian, M., Anagnostopoulos, T., Balsan, S. 1983. Genome-independent effects of 1,25-dihydroxyvitamin D3 on membrane potential.Biochim. Biophys. Acta 732:300–303

    PubMed  Google Scholar 

  15. Edelman, A., Thil, C.L., Garabedian, M., Plachot, J.J., Guillozo, H., Fritsch, J., Thomas, S.R., Balsan, S. 1985. Vitamin D metabolite effects on membrane potential and potassium intracellular activity in rabbit cartilage.Mineral Electrolyte Metab. 11:97–105

    Google Scholar 

  16. Greger, R., Schlatter, E. 1983. Properties of the lumen membrane of the cortical thick ascending limb of Henle's loop of rabbit kidney.Pfluegers Arch. 396:315

    Google Scholar 

  17. Hille, B., Woodhull, A.M., Shapiro, B.I. 1975. Negative surface charge near sodium channels of nerve: Divalent ions, monovalent ions, and pH.Philos. Trans. R. Soc. London B 270:301–318

    Google Scholar 

  18. Kubota, T., Biagi, B.A., Giebisch, G. 1983. Effects of acidbase disturbance on the basolateral membrane potential and intracellular potassium activity in the proximal tubule ofNecturus.J. Membrane Biol. 73:61–68

    Google Scholar 

  19. O'Neil, R., Sansom, S. 1984. Characterization of apical cell membrane Na+ and K+ conductances of cortical collecting duct using microelectrode techniques.Am. J. Physiol. 247:F14-F24

    PubMed  Google Scholar 

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

    Google Scholar 

  21. Planelles, G., Kurkdjian, A., Anagnostopoulos, T. 1984. Cell and luminal pH in the proximal tubule ofNecturus kidney.Am. J. Physiol. 247:F932-F938

    PubMed  Google Scholar 

  22. Planelles, G., Teulon, J., Anagnostopoulos, T. 1981. The effects of barium on the electrical properties of the basolateral membrane in proximal tubule.Naunyn Schmiedeberg's Arch. Pharmacol. 318:135–141

    Google Scholar 

  23. Preece, M.A., O'Riordan, J.L.H., Lawson, D.E.M., Kodicek, E. 1974. A competitive protein binding assay for 25(OH)D3 and 25-hydroxyergocalciferol in serum.Clin. Chim. Acta 54:235

    PubMed  Google Scholar 

  24. Shepard, R.M., Horst, R.L., Hamstra, A.J., Deluca, H.F. 1979. Determination of vitamin D metabolites in plasma from normal and anephric man.Biochem. J. 182:55

    PubMed  Google Scholar 

  25. Van Driessche, W., Zeiske, W. 1982. Cation selective channels in the apical membrane of frog skin unmasked by decreasing external [Ca2+] and intracellular [H+].Arch. Int. Physiol. Biochim. 90:P94-P95

    Google Scholar 

  26. Wasserman, R.H., Fullmer, C.S. 1983. Calcium transport protein, calcium absorption, and vitamin D.Annu. Rev. Physiol. 45:375–390

    PubMed  Google Scholar 

  27. Willmer, E.N. 1961. Steroids and cell surfaces.Biol. Rev. 36:368–398

    PubMed  Google Scholar 

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Authors and Affiliations

  1. INSERM U. 192, Hôpital Necker-Enfants-Malades, 75743, Paris, Cedex 15, France

    A. Edelman & T. Anagnostopoulos

  2. CNRS UA 583 and INSERM U. 30, Hôpital Necker-Enfants-Malades, 75743, Paris, Cedex 15, France

    M. Garabedian

Authors
  1. A. Edelman
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  2. M. Garabedian
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  3. T. Anagnostopoulos
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Edelman, A., Garabedian, M. & Anagnostopoulos, T. Mechanisms of 1,25(OH)2D3-induced rapid changes of membrane potential in proximal tubule: Role of Ca2+-dependent K+ channels. J. Membrain Biol. 90, 137–143 (1986). https://doi.org/10.1007/BF01869931

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  • DOI: https://doi.org/10.1007/BF01869931

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