Abstract
The electrical events associated with the absorption ofd-glucose orl-amino acids in renal proximal tubules were studied in microperfusion experiments on rat kidneys in vivo. Intratubular application of these substrates led concomittantly to: 1) a shift of the transepithelial potential into lumen negative direction, 2) a partial depolarization of the tubular cell membranes and 3) a reduction of the electrical resistance of the brushborder membrane. By means of rapid perfusion experiments it was possible to discern two phases in the potential response to substrate perfusion, a fast initial response which reflects a substrate-induced Na+ ion current from lumen to cell, and a slower secondary response which reflects the relaxation of the intracellular ion and substrate concentrations towards new steady states. A quantitative analysis of the data yielded estimates of 1) the apical (R a) and basal (R b) cell membrane resistances and of the shunt resistance,R s, of rat proximal tubule of approximatelyR a=255 Ω cm2,R b=92 Ω cm2 andR s=5 Ω cm2 (all referred to the quasi macroscopic surface area of the tubular lumen), 2) the conductance of the Na+ and glucose cotransport pathway and 3) the driving forces acting on the cotransport mechanism in the brushborder membrane. The latter were found to be a) the electrical cell membrane potential of −74mV, b) the Na+ ion concentration gradient between the tubular lumen (c lumNa =145 mmol/l) and the cytoplasm (c cellNa ≈22mmol/l) which corresponds to an additional equivalent potential of 51 mV and c) the substrate concentration gradient, which varies according to the experimental conditions. Moreover the analysis provided a quantitative estimate of the relationship between the substrate-induced changes in transepithelial potential or short circuit current and the actual cotransport current in the brushborder membrane. Based on this analysis it is concluded that the stoichiometry of Na+ and glucose flux coupling in the brushborder membrane of rat proximal tubule is close to 1.0.
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References
Barry RJC, Dikstein S, Matthews J, Smyth DH (1960) Electrical potentials in the isolated intestine. J Physiol 155: 17P-18P
Burg M, Patlak C, Green N, Villey D (1976) Organic solutes in fluid absorption by renal proximal convoluted tubules. Am J Physiol 231: 627–637
Crane RK, (1962) Hypothesis for mechanism of intestinal active transport of sugars. Fed Proc 21: 891–895
Frömter E (1972) The route of passive ion movement through the epithelium of Necturus gallbladden. J Membr Biol 8: 259–301
Frömter E (1977) Magnitude and significance of the paracellular shunt path in rat kidney proximal tubule. In: Kramer M, Lauterbach F (eds) Intestinal permeation. Excerpta Medica. Amsterdam, pp 166–178
Frömter E (1979) Solute transport across epithelia: What can we learn from micropuncture studies on kidney tubules. J Physiol 288: 1–31
Frömter E, Diamond JM (1972) Route of passive ion permeation in epithelia. Nature New Biol 235: 9–13
Frömter E, Gebler B (1977) Electrical properties of amphibian urinary epithelia. III. The cell membrane resistances and the effect of amiloride. Pflügers Arch 371: 99–108
Frömter E, Geßner K (1974) Active transport potentials, membrane diffusion potentials and streaming potentials across rat kidney proximal tubular epithelium. Pflügers Arch 351: 85–98
Frömter E, Lüer K (1973) Electrical studies on sugar transport kinetics of rat proximal tubule. Pflügers Arch (Suppl) 343: R47
Frömter E, Müller CW, Wick T (1971) Permeability properties of the proximal tubular epithelium of the rat kidney studied with electrophysiological methods. In: Giebisch G (ed) Electrophysiology of epithelial cells. F. K. Schattauer. Stuttgart New York, pp 119–146
Hansen UP, Slayman CL (1978) Current-voltage relationships for a clearly electrogenic cotransport system. In: Hoffman JF (ed) Membrane transport processes, Vol 1. Raven Press, New York, pp 141–154
Hoshi T (1976) Electrophysiological studies on amino acid transport across the luminal membrane of the proximal tubular cells of Triturus kidney. In: Silbernagl S, Lang F, Greger R (eds) Amino acid transport and uric acid transport. Georg Thieme, Stuttgart, pp 96–104
Hoshi T, Kawahara K, Yokoyama R, Suenaga K (1981) Changes in membrane resistances of renal proximal tubule induced by cotransport of sodium and organic solutes. In: Takács L (ed) Adv Physiol Sci Vol 11, Kidney and body fluids. Pergamon Press and Akademiai Akido, Budapest, pp 403–407
Hoshi T, Kikuta Y (1977) Effects of organic solute-sodium cotransport on the transmembrane potentials and resistance parameters of the proximal tubule of Triturus kidney. In: Anagnostopoulos T (ed) Electrophysiology of the nephron. Vol 67. Edition INSERM, Paris, pp 135–160
Iwatsuki N, Petersen OH (1980) Amino acid-evoked membrane potential and resistance changes in pancreatic acinar cells. Pflügers Arch 386: 153–159
Khuri RN (1979) Electrochemistry of the nephron. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology. Vol IVA, Springer, Berlin Heidelberg New York, pp 47–95
Kinne R (1976) Properties of the glucose transport system in the renal brush border membrane. In: Bronner F, Kleinzeller A (eds) Current topics in membranes and transport. Vol 8. Academic Press, New York, pp 209–267
Kohn PG, Smyth DH, Wright EM (1968) Effects of amino acids, dipeptides and disaccharides on the electric potential across rat small intestine. J Physiol 196: 723–746
Kokko JP (1973) Proximal tubule potential difference. Dependence on glucose, HCO3 and amino acids. J Clin Invest 52: 1362–1367
Loeschke K, Baumann K, Renschler R, Ullrich KJ (1969) Differenzierung zwischen aktiver und passiver Komponente desd-Glukosetransports am proximalen Konvolut der Rattenniere. Pflügers Arch 305: 118–138
Maruyama T, Hoshi T (1972) The effect ofd-glucose on the electrical potential profile across the proximal tubule of Newt kidney. Biochim Biophys Acta 282: 214–225
Maunsbach AB (1973) Ultrastructure of the proximal tubule. In: Orloff J, Berliner RW (eds) Handbook of physiology. Vol 8, Renal physiology. American Physiological Society. Washington, pp 31–79
Okada Y (1979) Solute transport process in intestinal epithelial cells. Membr Biochem 2: 339–365
Reuss L, Finn AL (1975) Electrical properties of the cellular transepithelial pathway in Necturus gallbladder. I. Circuit analysis and steady state effects of mucosal solution ionic substitutions. J Membr Biol 25: 115–139
Rose RC, Schultz SG (1971) Studies on the electrical potential profile across rabbit ileum. Effects of sugars and amino acids on transmural and transmucosal electrical potential differences. J Gen Physiol 57: 639–663
Sacktor B (1977) Transport in membrane vesicles isolated from the mammalian kidney and intestine. In: Sanadi DR (ed) Current topics in bioenergetics. Vol 6. Academic Press, New York San Francisco London, pp 39–81
Samaržija I, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. III. Neutral amino acids. Pflügers Arch 393: 199–209
Samaržija I, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. IV. Basic amino aicds. Pflügers Arch (in press)
Samaržija I, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. V. Acidic amino acids. Pflügers Arch (in press)
Samaržija 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
Samaržija I, Molnar E, Frömter E (1982) Mechanism of Na+-coupled anion absorption across the brush border membrane of rat renal proximal tubule. In: Takács L (ed) Advances in physiological sciences. Vol 1, Kidney and body fluids. Pergamon Press and Akadémiai Kiado, Budapest, pp 419–423
Schultz SG, Zalusky R (1964) Ion transport in isolated rabbit ileum. II. The interaction between active sodium and active sugar transport. J Gen Physiol 47: 1043–1059
Thurau K, Dörge A, Mason J, Beck F, Rick R (1979) Intracellular elemental concentrations in renal tubular cells. An electron microprobe analysis. Klin Wochenschr 57: 993–1000
Ullrich KJ (1976) Renal tubular mechanisms of organic solute transport. Kidney Int 9: 134–148
Ullrich KJ, Frömter E, Baumann K (1969) Micropuncture and microanalysis in kidney physiology. In: Passow H, Stämpfli R (eds) Laboratory techniques in membrane biophysics. Springer, Berlin Heidelberg New York, pp 106–129
White JF, Armstrong WMcD (1971) Effect of transported solutes on membrane potentials in bullfrog small intestine. Am J Physiol 221: 194–201
Welling LW, Welling DJ (1976) Shape of epithelial cells and intercellular channels in the rabbit proximal nephron. Kidney Int 9: 385–394
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Frömter, E. Electrophysiological analysis of rat renal sugar and amino acid transport. Pflugers Arch. 393, 179–189 (1982). https://doi.org/10.1007/BF00582942
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DOI: https://doi.org/10.1007/BF00582942