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The effect of cAMP on the cell membrane potential and intracellular ion activities in proximal tubule ofRana esculenta

  • Transport Processes, Metabolism and Endocrinology; Kidney, Gastrointestinal Tract, and Exocrine Glands
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Abstract

Experiments were performed in proximal tubule of the isolated perfused frog kidney to evaluate peritubular cell membrane potentials (PDpt), and the intracellular ion activities of sodium (Nai ü), chloride (Cli ) and potassium (Ki ü) under control conditions and following peritubular application of dibutyryl-cyclic AMP (cAMP, 2·10−4mol·l−1). Conventional and ion-sensitive microelectrodes were applied to record continuously cAMP-induced changes of these parameters in individual proximal tubule cells.

Within a few minutes a significant hyperpolarisation of PDpt (Δ=2.0±0.2 mV) occurs simultaneously with a decrease of Nai ü (Δ=2.5±0.5 mmol·l−1). Ki ü increases (Δ=3.6±0.9 mmol·l−1) and Cli decreases (0.4±0.07 mmol·l−1) slightly, but significantly. With both ions the alterations of the chemical gradient is significantly smaller than the potential shift. PDte is not significantly altered by cAMP. The cAMP-induced hyperpolarisation of PDpt can be observed in presenceand absence of luminal glucose. However, omission of Naü from the luminal perfusate abolishes the hyperpolarising effect of cAMP on PDpt.

The results suggest that cAMP reduces sodium entry from the lumen into the cell, thus hyperpolarising the cell membrane and decreasing Nai ü. Persistance of sensitivity of PDpt to cAMP after omission of glucose indicates that other Naü coupled transport processes and/or passive Naü conductance are affected by cAMP. the changes of Ki ü and Cli are secondary, following the change of PDpt.

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References

  1. Agus ZS, Gardner LB, Beck LH, Goldberg M (1973) Effects of parathyroid hormone on renal tubular reabsorption of calcium, sodium, and phosphate. Am J Physiol 224:1143–1148

    Google Scholar 

  2. Armstrong W McD, Bixenman WR, Frey KF, Garcia-Diaz JF, O'Regan MG, Owens JL (1979) Energetic of coupled Naü and Cl entry into epithelial cells of bullfrog small intestine. Biochim Biophys Acta 551:207–219

    Google Scholar 

  3. Baumgarten CM (1981) An improved liquid ion exchanger for chloride ion-selective microelectrodes. Am J Physiol 241:C258-C263

    Google Scholar 

  4. Bers DM, Ellis D (1982) Intracellular calcium and sodium activity in sheep heart Parkinje fibres effect of changes of external sodium and intracellular pH. Pflüger Arch 393:171–178

    Google Scholar 

  5. Boulpaep EL (1978) The necturus kidney preparation. In: Andreucci VE (ed) Manual of renal micropuncture. Idelson, Naples pp 461–465

    Google Scholar 

  6. Cemericic D, Giebisch G (1980) Intracellular sodium activity in Necturus kidney proximal tubule. Fed Proc 39:1080

    Google Scholar 

  7. Clausen T, Flatman JA (1977) The effect of catecholamines on Na−K transport and membrane potential in rat soleus muscle. J Physiol 270:383–414

    Google Scholar 

  8. Deeds DG, Sullivan LP, Fenton RA, Tucker JM, Cuppage FE (1977) Function and structure of perfused bullfrog kidney. Am J Physiol 233:F481-F490

    Google Scholar 

  9. Diez de los Rios A, DeRose NE, Armstrong WMcD (1981) Cyclic AMP and intracellular ionic activities in Necturus gallbladder. J Membr Biol 63:25–30

    Google Scholar 

  10. Duffey ME, Thompson SM, Frizzell RA, Schultz SG (1979) Intracellular chloride activities and active chloride absorption in the intestinal epithelium of the winter flounder. J Membr Biol 50: 331–341

    Google Scholar 

  11. Edelman A, Bouthier M, Anagnostopoulos T (1981) Chloride distribution in the proximal convoluted tubule of Necturus kidney. J Membr Biol 62:7–17

    Google Scholar 

  12. Field M (1971) Ion transport in rabbit ileal mucosa. II. Effects of cyclic 3′,5′-AMP. Am J Physiol 221:992–997

    Google Scholar 

  13. Frizzell RA, Dugas MC, Schultz SG (1975) Sodium chloride transport by rabbit gallbladder. Direct evidence for a coupled NaCl influx process. J Gen Physiol 65:769–795

    Google Scholar 

  14. Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. I. Basic phenomena. Pflügers Arch 393:179–189

    Google Scholar 

  15. Fujimoto M, Kubota T (1976) Physicochemical properties of a liquid ion exchanger microelectrode and its application to biological fluids. Jpn J Physiol 26:631–650

    Google Scholar 

  16. Garzia-Diaz JF, Armstrong WMcD (1980) The steady-state relation-ship between sodium and chloride transmembrane electrochemical potential differences in Necturus gallbladder. J Membr Biol 55:213–222

    Google Scholar 

  17. Graf J, Giebisch G (1979) Intracellular sodium activity and sodium transport in Necturus gallbladder epithelium. J Membr Biol 47:327–355

    Google Scholar 

  18. Gill JR, Casper AGT, Tate J (1971) Renal effects of adenosine 3′,5′-cyclic monophosphate and dibutyryl adenosine 3′,5′-cyclic monophosphate. J Clin Invest 50:1231–1239

    Google Scholar 

  19. Jacobson HR (1979) Altered permeability in the proximal tubule response to cyclic AMP. Am J Physiol 236:F71-F79

    Google Scholar 

  20. Kinne R, Berner W, Hoffmann N, Murer H (1981) Phosphate transport by isolated renal and intestinal plasma membranes. In: Massry SG, Ritz E (eds) Adv Exp Med Biol. Plenum Press, New York, pp 265–277

    Google Scholar 

  21. Kubota T, Honda M, Kotera K, Fujimoto M (1980) The effect of diffusible ions on the peritubular membrane potential of proximal tubular cells in perfused bullfrog kidneys. Jpn J Physiol 30:775–790

    Google Scholar 

  22. Kuntziger H, Amiel C, Roinel N, Morel F (1974) Effects of parathyroidectomy and cyclic AMP on renal transport of phosphate, calcium, and magnesium. Am J Physiol 227:905–911

    Google Scholar 

  23. Lee CO, Taylor A, Windhager EE (1980) Cytosolic calcium ion activity in epithelial cells of Necturus kidney. Nature [Lond] 287:859–861

    Google Scholar 

  24. Lewis SA, Wills NK (1980) Resistive artifacts in liquid-ion exchanger microelectrode estimates of Naü activity in epithelial cells. Biophys J 31:127–138

    Google Scholar 

  25. Lorentz WB (1974) The effect of cyclic AMP and dibutyryl cyclic AMP on the permeability characteristics of the renal tubule. J Clin Invest 53:1250–1257

    Google Scholar 

  26. Nellans HN, Frizzell RA, Schultz SG (1974) Brush-border processes and transepithelial Na and Cl transport by rabbit ileum. Am J Physiol 226:1131–1141

    Google Scholar 

  27. Oberleithner H, Guggino W, Giebisch G (1982) Mechanism of distal tubular chloride transport in Amphiuma kidney. Am J Physiol 242:F331-F339

    Google Scholar 

  28. Oberleithner H, Lang F, Wang W, Giebisch G (1982) Effects of inhibition of chloride transport on intracellular sodium activity in distal Amphibian nephron. Pflügers Arch 394:55–60

    Google Scholar 

  29. Robinson RA, Stokes RH (1970) Electrolytic solutions, 2nd edn. Butterworth, London

    Google Scholar 

  30. Samarizija I, Hinton BT, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. II. Dependence on various transport parameters and inhibitors. Pflügers Arch 393:190–197

    Google Scholar 

  31. Schultz SG (1981) Homocellular regulatory mechanisms in sodiumtransporting epithelia: avoidance of extinction by “flushthrough”. Am J Physiol 241:F579-F590

    Google Scholar 

  32. Spring KR, Kimura G (1978) Chloride reabsorption by renal proximal tubules of Necturus. J Membr Biol 38:233–254

    Google Scholar 

  33. Steiner RA, Oehme M, Ammann D, Simon W (1979) Neutral carrier sodium ion-selective microelectrode for intracellular studies. Anal Chem 51:351–353

    Google Scholar 

  34. Taylor A, Windhager EE (1979) Possible role of cytosolic calcium and Na−Ca exchange in regulation of transepithelial sodium transport. Am J Physiol 236:F505-F512

    Google Scholar 

  35. Thomas RC (1972) Intracellular sodium activity and the sodium pump in snail neurones. J Physiol [Lond] 220:55–71

    Google Scholar 

  36. White JF (1977) Activity of chloride in absorptive cells of Amphiuma small intestine. Am J Physiol 232:E553-E559

    Google Scholar 

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Wang, W., Oberleithner, H. & Lang, F. The effect of cAMP on the cell membrane potential and intracellular ion activities in proximal tubule ofRana esculenta . Pflugers Arch. 396, 192–198 (1983). https://doi.org/10.1007/BF00587855

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  • DOI: https://doi.org/10.1007/BF00587855

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