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.
Similar content being viewed by others
References
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
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
Baumgarten CM (1981) An improved liquid ion exchanger for chloride ion-selective microelectrodes. Am J Physiol 241:C258-C263
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
Boulpaep EL (1978) The necturus kidney preparation. In: Andreucci VE (ed) Manual of renal micropuncture. Idelson, Naples pp 461–465
Cemericic D, Giebisch G (1980) Intracellular sodium activity in Necturus kidney proximal tubule. Fed Proc 39:1080
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
Deeds DG, Sullivan LP, Fenton RA, Tucker JM, Cuppage FE (1977) Function and structure of perfused bullfrog kidney. Am J Physiol 233:F481-F490
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
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
Edelman A, Bouthier M, Anagnostopoulos T (1981) Chloride distribution in the proximal convoluted tubule of Necturus kidney. J Membr Biol 62:7–17
Field M (1971) Ion transport in rabbit ileal mucosa. II. Effects of cyclic 3′,5′-AMP. Am J Physiol 221:992–997
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
Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. I. Basic phenomena. Pflügers Arch 393:179–189
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
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
Graf J, Giebisch G (1979) Intracellular sodium activity and sodium transport in Necturus gallbladder epithelium. J Membr Biol 47:327–355
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
Jacobson HR (1979) Altered permeability in the proximal tubule response to cyclic AMP. Am J Physiol 236:F71-F79
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
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
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
Lee CO, Taylor A, Windhager EE (1980) Cytosolic calcium ion activity in epithelial cells of Necturus kidney. Nature [Lond] 287:859–861
Lewis SA, Wills NK (1980) Resistive artifacts in liquid-ion exchanger microelectrode estimates of Naü activity in epithelial cells. Biophys J 31:127–138
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
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
Oberleithner H, Guggino W, Giebisch G (1982) Mechanism of distal tubular chloride transport in Amphiuma kidney. Am J Physiol 242:F331-F339
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
Robinson RA, Stokes RH (1970) Electrolytic solutions, 2nd edn. Butterworth, London
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
Schultz SG (1981) Homocellular regulatory mechanisms in sodiumtransporting epithelia: avoidance of extinction by “flushthrough”. Am J Physiol 241:F579-F590
Spring KR, Kimura G (1978) Chloride reabsorption by renal proximal tubules of Necturus. J Membr Biol 38:233–254
Steiner RA, Oehme M, Ammann D, Simon W (1979) Neutral carrier sodium ion-selective microelectrode for intracellular studies. Anal Chem 51:351–353
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
Thomas RC (1972) Intracellular sodium activity and the sodium pump in snail neurones. J Physiol [Lond] 220:55–71
White JF (1977) Activity of chloride in absorptive cells of Amphiuma small intestine. Am J Physiol 232:E553-E559
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00587855