Pflügers Archiv

, Volume 394, Issue 4, pp 287–293 | Cite as

Poorly selective cation channels in the skin of the larval frog (Stage≤XIX)

  • Stanley D. Hillyard
  • Wolfgang Zeiske
  • Willy Van Driessche
Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands

Abstract

The abdominal skin of bullfrog larvae (Rana catesbeiana) was placed in an Ussing-type chamber, and its transepithelial electrical parameters were recorded with mucosal solutions of different ionic composition. With “K+-like” cations (K+, NH 4 + , Rb+, Cs) the power spectra of the fluctuations in short-circuit current displayed a Lorentzian component (f c =30–40 Hz). The relaxation noise could be suppressed by addition of the K+-channel blockers Ba2+ and TEA to the mucosal solution. Also, in presence of the ionophore antibiotic nystatin the Lorentzian noise was abolished. The Na+-channel probes amiloride and benzimidazolyl-2-guanidine (BIG) both enhanced the relaxation noise obtained with the K+-like cations but, with Na+, and Li+, also caused the rise of a relaxation component above the background noise. In presence of amiloride or BIG, the addition of Ba2+, TEA and nystatin still abolished the Lorentzian noise. It can be concluded that the relaxation-noise source is located in the apical cell membranes of the tadpole skin. These spontaneously fluctuating cation channels do not seem to strictly discriminate between K+-like ions (K+, NH 4 + , Rb+, Cs+) and Na+-like ions (Na+, Li+). On the other hand, well-known specific probes for K+ channels (Ba2+, TEA) and for Na+ channels (amiloride, BIG) interact with this apical cation channel. It is possible that the poorly selective channel plays a role in the ontogenesis of the specific Na+ transport in the maturing frog skin.

Key words

Noise analysis Tadpole skin Apical membrane Cation channel Barium TEA (Tetraethyl ammonium) Amiloride 

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References

  1. Alvarado RH, Moody A (1970) Sodium and chloride transport in tadpoles of the bullfrog Rana catesbeiana. Am J Physiol 218: 1510–1516Google Scholar
  2. Armstrong CM, Hille B (1972) The inner quaternary ammonium ion receptor in potassium channels of the node of Ranvier. J Gen Physiol 59:388–400Google Scholar
  3. Coronado R, Rosenberg RL, Miller CJ (1980) Ionic selectivity, saturation, and block in a K+-selective channel from sarcoplasmic reticulum. J Gen Physiol 76:425–446Google Scholar
  4. Cox TC, Alvarado RH (1979) Electrical and transport characteristics of skin of laryal Rana catesbeiana. Am J Physiol 237:R74-R79Google Scholar
  5. Crabbé J (1980) Decreased sensitivity to amiloride of amphibian epithelia treated with aldosterone. Further evidence for an apical hormonal effect. Pflügers Arch 383:151–158Google Scholar
  6. Ehrlich EN, Crabbé J (1968) The mechanism of action of amipramizide. Pflügers Arch 302:79–96Google Scholar
  7. Fishman HM, Moore LE, Poussart DJM (1975) Potassium ion conduction noise in squid axon membranes. J Membr Biol 24:305–328Google Scholar
  8. Fishman HM, Moore LE, Poussart DJM (1977) Ion movements and kinetics in squid axon: II. Spontaneous electrical fluctuations. In: Takashima S, Fishman HM (eds) Electrical properties of biological polymers. Ann NY Acad Sci 303:399–423Google Scholar
  9. Gögelein H, Van Driessche W (1981) Noise analysis of the K+ current through the apical membrane of Necturus gallbladder. J Membr Biol 63:243–254Google Scholar
  10. Hille B (1973) Potassium channels in myelinated nerve. Selective permeability to small monovalent cations. J Gen Physiol 61:669–686Google Scholar
  11. Katz U (1978) Changes in ionic conductances and in sensitivity to amiloride during the natural moulting cycle of toad skin (Bufo viridis, L). J Membr Biol 38:1–9Google Scholar
  12. Koefoed-Johnsen V, Ussing HH (1958) The nature of the frog skin potential. Acta Physiol Scand 42:298–308Google Scholar
  13. Lewis SA, Eaton DC, Clausen C, Diamond JM (1977) Nystatin as a probe for investigating the electrical properties of a tight epithelium. J Gen Physiol 70:427–440Google Scholar
  14. Li JH, de Sousa RC (1979) Inhibitory and stimulatory effects of amiloride analogues on sodium transport in frog skin. J Membr Biol 46:155–169Google Scholar
  15. Lindemann B, Van Driessche W (1977) Sodium-specific membrane channels reveal high turnover. Science 195:292–294Google Scholar
  16. Nagel W, Garcia-Diaz JF, Armstrong WMcD (1981) Intracellular ionic activities in frog skin. J Membr Biol 61:127–134Google Scholar
  17. Reuter H, Stevens CF (1980) Ion conductance and ion selectivity of potassium channels in snail neurones. J Membr Biol 57:103–118Google Scholar
  18. Smith MW, Cremaschi D, Ferguson DR, Hénin S, James PS, Meyer G (1979) Onset of amiloride sensitivity in the developing pig colon. In: Cuthbert AW, Fanelli Jr GM, Scribine A (eds) Amiloride and epithelial sodium transport. Urban and Schwarzenberg, Baltimore München, pp 131–144Google Scholar
  19. Sperelakis N, Schnieder MF, Harris EJ (1967) Decreased K+ conductance produced by Ba++ in frog sartorius fibers. J Gen Physiol 50:1565–1583Google Scholar
  20. Stanfield PR, Ashcroft FM, Plant TD (1981) Gating of a muscle K+-channel and its dependence on the permeating ion species. Nature 289:509–511Google Scholar
  21. Swenson Jr RP, Armstrong CM (1981) K+ channels close more slowly in the presence of external K+ and Rb+. Nature 291:427–429Google Scholar
  22. Taylor RE, Barker SB (1965) Transepidermal potential difference: development in anuran larvae. Science 148:1612–1613Google Scholar
  23. Van Driessche W, Gögelein H (1978) Potassium channels in the apical membrane of the toad gallbladder. Nature 275:665–667Google Scholar
  24. Van Driessche W, Zeiske W (1980a) Spontaneous fluctuations of potassium channels in the apical membrane of frog skin. J. Physiol (Lond) 299:101–116Google Scholar
  25. Van Driessche W, Zeiske W (1980b) Ba2+-induced conductance fluctuations of spontaneously fluctuating K+ channels in the apical membrane of frog skin (Rana temporaria). J Membr Biol 56:31–42Google Scholar
  26. Zeiske W (1978) The stimulation of Na+ uptake in frog skin by uranyl ions. Biochim Biophys Acta 509:218–229Google Scholar
  27. Zeiske W, Lindemann B (1974) Chemical stimulation of Na+ current through the outer surface of frog skin epithelium. Biochim Biophys Acta 352:323–326Google Scholar
  28. Zeiske W, Van Driessche W (1981) Apical K+ channels in frog skin (Rana temporaria): Cation adsorption and voltage influence gating kinetics. Pflügers Arch 390:22–29Google Scholar
  29. Zeiske W, Wills NK, Van Driessche W (1981) Fluctuating K+ channels in the apical membranes of rabbit descending colon epithelium. Pflügers Arch (Suppl) 389:R48Google Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • Stanley D. Hillyard
    • 1
  • Wolfgang Zeiske
    • 1
  • Willy Van Driessche
    • 1
  1. 1.Laboratorium voor FysiologieK.U.L.LeuvenBelgium

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