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Electrophysiological analysis of rat renal sugar and amino acid transport

III. Neutral amino acids

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

We have used electrophysiological techniques in rat kidney proximal tubule to study the transport of the followingl-α-amino acids: alanine, phenylalanine, glutamine, methionine, cysteine, cystine, proline, and hydroxyproline as well as the transport of glycine and β-alanine. When applied in millimolar concentrations in the tubular lumen in the presence of Na+, all amino acids tested were found to depolarize the tubular cell membranes partially. This depolarization arises from current flow that is associated with the cotransport of Na+ and amino acids across the brushborder membrane (Frömter 1982 [9]). Peritubular application did not alter the membrane potentials in a conclusive way. The magnitude of the depolarization in response to luminal perfusion increased with increasing amino acid concentration and obeyed simple Michaelis-Menten kinetics, except for proline, hydroxyproline, and glycine, which exhibited double-site saturation kinetics. By analyzing the time course of the potential changes and distinguishing between initial and steady state depolarizations, it was possible to separate kinetic properties of the brushborder transport mechanisms from the lumped kinetic properties of the overall epithelium. Knowing the concentration dependence of the depolarizations, the competition of different amino acids for the same transport site was investigated: Two amino acids were applied in saturating concentrations in the tubular lumen, either singly or jointly, to determine whether the depolarizations were additive and whether the additivity exceeded the predictions from the kinetic experiments. From such studies the presence of three separate rheogenic transport systems is postulated for neutral amino acids: System I transports all neutrall-α-amino acids with the exception of cystine, system II transports proline, hydroxyproline and glycine, and system III transports β-alanine or under physiological conditions taurine. Studies with the oxidant diamide suggest that cystine may be mostly reduced to cysteine and transported as cysteine, however it is likely that an extra transport system exists which transports cystine possibly in electroneutral fashion together with dibasic amino acids.

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References

  1. Barfuss DW, Mays JM, Schafer JA (1980) Peritubular uptake and transepithelial transport of glycine in isolated proximal tubules. Am J Physiol 238:F324-F333

    Google Scholar 

  2. Bowyer F (1957) The kinetics of penetration of nonelectrolytes into the mammalian erythrocyte. Int Rev Cytol 6:469–511

    Google Scholar 

  3. Čemerikić, D, Giebisch G (1981) Intracellular Na activity measurements in Necturus kidney proximal tubule. 8th International Congress of Nephrology, Abstracts Athen, p 71

  4. Evers J, Murer H, Kinne R (1976) Phenylalanine uptake in isolated renal brushborder vesicles. Biochim Biophys Acta 426:598–615

    Google Scholar 

  5. Fass SJ, Hammermann MR, Sacktor B (1977) Transport of amino acids in renal brushborder membrane vesicles. J Biol Chem 252:583–590

    Google Scholar 

  6. Frömter E (1972) The route of passive ion movement through the epithelium if Necturus gallbladder. J Memb Biol 8:259–301

    Google Scholar 

  7. Frömter E (1977) Stofftransport durch biologische Membranen. In: Hoppe W, Lohmann W, Markl H (eds) Biophysik-Ein Lehrbuch. Springer, Berlin Heidelberg New York, pp 328–361

    Google Scholar 

  8. Frömter E (1979) Solute transport across epithelia: what can we learn from micropuncture studies on kidney tubules. J Physiol 288:1–31

    Google Scholar 

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

    Google Scholar 

  10. Geck P, Heinz E (1976) Coupling in secondary transport. Effect of electrical potentials on the kinetics of ion linked cotransport. Biochim Biophys Acta 443:49–53

    Google Scholar 

  11. Heinz E, Geck P, Wilbrandt W (1971) Coupling in secondary active transport. Activation of transport by co-transport and/or counter-transport with the fluxes of other solutes. Biochim Biophys Acta 255:442–461

    Google Scholar 

  12. Hillmann RE, Rosenberg LE (1969) Amino acid transport by isolated mammalian renal tubules. II. Transport systems forl-proline. J Biol. Chem 214:4494–4498

    Google Scholar 

  13. Hopfer U, Groseclose R (1979) The mechanism of Na+-dependentd-glucose transport. J Biol Chem 255:4435–4462

    Google Scholar 

  14. 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

    Google Scholar 

  15. Hoshi T, Sudo K, Suzuki Y (1976) Characteristics of changes in the intracellular potential associated with transport of neutral, dibasic and acidic amino acids in Triturus proximal tubule. Biochim Biophys Acta 448:492–504

    Google Scholar 

  16. Lagarde AE (1976) A nonequilibrium thermodynamics analysis of active transport within the framework of the chemiosmotic theory. Biochim Biophys Acta 426:198–217

    Google Scholar 

  17. Lingard JM, Rumrich G, Young JA (1973) Kinetics ofl-histidine transport in the proximal convolution of the rat nephron studied using the stationary microperfusion technique. Pflügers Arch 342:13–28

    Google Scholar 

  18. Lingard JM, Györy AZ, Young JA (1975) Microperfusion study of the kinetics of reabsorption of cycloleucine in early and late segments of the proximal convolution of the rat nephron. Pflügers Arch 357:51–61

    Google Scholar 

  19. Loeschke K, Baumann K (1969) Kinetische Studien derd-Glukoseresorption im proximalen Konvolut der Rattenniere. Pflügers Arch 305:139–154

    Google Scholar 

  20. McNamara P, Pepe LM, Segal S (1979) Sodium gradient dependence of proline and glycine uptake in rat renal brushborder membrane vesicles. Biochim Biophys Acta 556:151–160

    Google Scholar 

  21. Mircheff AK, van Os CH, Wright EM (1980) Pathways for alanine transport in intestinal basal lateral membrane vesicles. J Memb Biol 52:83–92

    Google Scholar 

  22. Mohyuddin F, Scriver CR (1970) Amino acid transport in mammalian kidney: multiple systems for imino acids and glycine in rat kidney. Am J Physiol 219:1–8

    Google Scholar 

  23. Murer H (1981) Personal communication

  24. Philo RD, Eddy AA (1978) The membrane potential of mouse ascites-tumour cells studied with the fluorescent probe 3,3′-dipropyloxadicarbocyanine. Amplitude of the depolarization caused by amino acids. Biochem J 174:801–810

    Google Scholar 

  25. Sacktor B (1977) Transport in membrane vesicles isolated from the mammalian kidney and intestine. Curr Top Bioenerg 6:39–78

    Google Scholar 

  26. Samaržija I, Frömter E (1975) Electrical studies on amino acid transport across brushborder membrane of rat proximal tubule in vivo. Pflügers Arch 359 (Suppl): R119

    Google Scholar 

  27. Samaržija I, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino transport. IV. Basic amino acids. Pflügers Arch 393:210–214

    Google Scholar 

  28. Samaržija I, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino transport. V. Acidic amino acids Pflügers Arch 393:215–221

    Google Scholar 

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

    Google Scholar 

  30. Schafer JA, Watkins ML (1981) Transport ofl-cystine in the pars recta. 8th International Congress of Nephrology, Athen, p 36

  31. Schneider EG, Hammermann MR, Sacktor B (1980) Sodium gradient-dependentl-glutamate transport in renal brush border membrane vesicles. J Biol Chem 255:7650–7656

    Google Scholar 

  32. Schultz SG, Curran PF (1970) Coupled transport of sodium and organic solutes. Physiol Rev 50:637–718

    Google Scholar 

  33. Schwartzman L, Blair A, Segal S (1967) Exchange diffusion of dibasic amino acids in rat kidney cortex slices. Biochim Biophys Acta 135:120–126

    Google Scholar 

  34. Scriver CR, Bergeron M (1974) Amino acid transport in kidney. The use of mutation to dissect membrane and transepithelial transport. In: Nyhan WL (ed) Heritable disorders of amino acid metabolism. J Wiley & Sons, New York, pp 515–592

    Google Scholar 

  35. Scriver CR, Chesney RW, McInnes RR (1976) Genetic aspects of renal tubular transport: Diversity and topology of carriers. Kidney Int 9:149–171

    Google Scholar 

  36. Segal S, Thier SO (1973) Renal handling of amino acids. In: Berliner RW, Orloff J (eds) Handbook of Physiology Section 8, Renal Physiology. Am Physiol Soc, Washington, pp 653–676

    Google Scholar 

  37. Segal S, McNamara PD, Pepe LM (1977) Transport interaction of cystine and dibasic amino acids in renal brush border vesicles. Science 197:169–171

    Google Scholar 

  38. Shalhoub R, Webber W, Glabman S, Canessa-Fischer M, Klein J, De Haas J, Pitts R (1963) Glutaminextraction exceeds filtration and reabsorption in acidotic dog. Am J Physiol 204:181–186

    Google Scholar 

  39. Silbernagl S (1979) Renal transport of amino acids. Klin Wochenschr 57:1009–1019

    Google Scholar 

  40. Silbernagl S, Foulkes EC, Deetjen P (1975) Renal transport of amino acids. Rev Physiol, Biochem Pharmacol 74:105–167

    Google Scholar 

  41. Stein WD (1967) The movement of molecules across cell membranes. Academic Press, New York

    Google Scholar 

  42. Toggenburger G, Kessler M, Rothstein A, Semenza G, Tannenbaum C (1978) Similarity in effects of Na gradients and membrane potential ond-glucose transport by, and phlorizin binding to, vesicles derived from brushborders of rabbit intestinal mucosal cells. J Membr Biol 40:269–290

    Google Scholar 

  43. Völkl H, Silbernagl S (1981) Molecular specificity of tubular resorption of cysteine and cystine in rat kidney. 8th International Congress of Nephrology, Athen, p 34

  44. Völkl H, Silbernagl S, Deetjen P (1979) Kinetics ofl-proline reabsorption in rat kidney studied by continuous microperfusion. Pflügers Arch 382:115–121

    Google Scholar 

  45. Wilbrandt W, Rosenberg T (1961) The concept of carrier transport and its corollaries in pharmacology. Pharmacol Rev 13:109–183

    Google Scholar 

  46. Young JA, Freedman BS (1971) Renal tubular transport of amino acids. Clin Chem 17:245–266

    Google Scholar 

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Authors and Affiliations

  1. Max-Planck-Institut für Biophysik, Kennedyallee 70, D-6000, Frankfurt 70, Federal Republic of Germany

    E. Frömter

  2. Centar za Hemodijalizu i Nefrologiju, P. Miskina 64, YU-41000, Zagreb, Yugoslavia

    I. Samaržija

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  1. I. Samaržija
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  2. E. Frömter
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Samaržija, I., Frömter, E. Electrophysiological analysis of rat renal sugar and amino acid transport. Pflugers Arch. 393, 199–209 (1982). https://doi.org/10.1007/BF00584070

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  • DOI: https://doi.org/10.1007/BF00584070

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