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Properties of the basolateral membrane of the cortical thick ascending limb of Henle's loop of rabbit kidney

A model for secondary active chloride transport

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

The present study utilizes the transepithelial and transmembrane electrophysiological approach to study the properties of the basolateral membrane of the in vitro perfused cortical thick ascending limb of Henle's loop (cTAL) of rabbit kidney. Eight different series were performed in a total of 119 tubules. The key observations are: 1. A K+ concentration upward step in the bath from 3.6 to 18.6 mmol · l−1 depolarizes the basolateral membrane by 19±2 mV. 2. This depolarization can be abolished when Ba2+ (3 mmol · l−1) is added to the bath: The depolarization by Ba2+ alone is equal to that by Ba2+ plus the K+ concentration upward step (21.7 versus 22.4 mV). 3. This effect of Ba2+ is not accompanied by any change in transepithelial resistance nor in the fractional resistance of the basolateral membrane. 4. A Cl concentration downward step in the bath from 150 to 50 mmol · l−1 leads to a depolarization between 8–15 mV.

We conclude that the K+ exit at the basolateral membrans is mainly electroneutral and that Cl leaves the cell both electroneutrally (KCl) and diffusionally. The present data, together with previous findings from our laboratory, are used to draw a tentative model for the NaCl reabsorption in the cTAL segment. In this model the (Na++K+)-ATPase provides the primary driving force. Na+, 2 Cl, K+ are cotransported luminally, K+ recycles across the lumen membrane. Cl leaves the cell in part in conjunction with K+, and thus utilizing the chemical gradient for K+, and the remainder leaves the cell through the Cl conductive pathway. The discrepancy of the conductivity properties of both cell membranes, the lumen membrane K+ conductive, and the basolateral membrane Cl conductive, is the main source for the lumen positive transepithelialPD. ThePD, in turn, drives a seizable fraction of the Na+ through the paracellular shunt pathway.

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References

  1. Aull F (1981) Potassium chloride cotransport in steady-state ascites tumor cells. Does bumetanide inhibit? Biochim Biophys Acta 643:339–345

    Google Scholar 

  2. Beck F, Bauer R, Bauer U, Mason J, Dörge A, Rick R, Thurau K (1980) Electron microprobe analysis of intracellular elements in the rat kidney. Kidney Int 17:756–763

    Google Scholar 

  3. Bello-Reuss E (1982) Electrical properties of the basolateral membrane of the straight portion of the rabbit proximal renal tubule. J Physiol 326:49–63

    Google Scholar 

  4. Biagi B, Kubota T, Sohtell M, Giebisch G (1981) Intracellular potentials in rabbit proximal tubules perfused in vitro. Am J Physiol 240:F200-F210

    Google Scholar 

  5. Boulpaep EL (1979) Electrophysiology of the kidney. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology. Springer, Berlin Heidelberg New York, pp 97–144

    Google Scholar 

  6. Burckhardt BCH, Frömter E (1981) Bicarbonate and hydroxylion permeability of the peritubular cell membrane of rat renal proximal tubular cells. Pflügers Arch 389:R40

    Google Scholar 

  7. Burg MB (1982) Thick ascending limb of Henle's loop. Kidney Int 22:454–464

    Google Scholar 

  8. Burg M, Grantham J, Abramow M, Orloff J (1966) Preparation and study of fragments of single rabbit nephrons. Am J Physiol 210:1293–1298

    Google Scholar 

  9. Chipperfield AR (1980) An effect of chloride on (Na+K) co-transport in human red blood cells. Nature 286:281–282

    Google Scholar 

  10. DiBona DR, Mills JW (1979) Distribution of Na+-pump sites in transporting epithelia. Fed Proc 38:134–143

    Google Scholar 

  11. Dunham PB, Stewart GW, Ellory JC (1980) Chloride-activated passive potassium transport in human erythrocytes. Proc Natl Acad Sci USA 77:1711–1715

    Google Scholar 

  12. Dunn MJ (1970) The effect of transport inhibitors on sodium outflux and influx in red blood cells: Evidence for exchange diffusion. J Clin Invest 49:1804–1814

    Google Scholar 

  13. Eveloff J, Kinne R, Kinne-Saffran E, Murer H, Silva P, Epstein FH, Stoff J, Kinter WB (1978) Coupled sodium and chloride transport into plasma membrane vesicles prepared from dogfish rectal gland. Pflügers Arch 378:87–92

    Google Scholar 

  14. Field M, Kimberg LS, Orellana SA, Frizzell RA (1981) Potassium dependence of chloride transport in the intestine of the flounder, Pseudopleuronectes americanus. Mount Desert Island Bull 21:93–95

    Google Scholar 

  15. Garg LC, Knepper MA, Burg MB (1981) Mineralocorticoid effects on Na−K-ATPase in individual nephron segments. Am J Physiol 240:F536-F544

    Google Scholar 

  16. Geck P, Pietrzyk C, Burckhardt BC, Pfeiffer B, Heinz E (1980) Electrically silent cotransport of Na+, K+ and Cl in Ehrlich cells. Biochim Biophys Acta 600:432–447

    Google Scholar 

  17. Greger R (1981) Cation selectivity of the isolated perfused cortical thick ascending limb of Henle's loop of rabbit kidney. Pflügers Arch 390:30–37

    Google Scholar 

  18. Greger R (1981) Chloride reabsorption in the rabbit cortical thick ascending limb of the loop of Henle. A sodium dependent process. Pflügers Arch 390:38–43

    Google Scholar 

  19. Greger R (1981) Coupled transport of Na+ and Cl in the thick ascending limb of Henle's loop of rabbit nephron. Scand Audiol (Suppl) 14:1–15

    Google Scholar 

  20. Greger R, Frömter E (1981) Time course of ouabain and furosemide effects on transepithelial potential difference in cortical thick ascending limbs of rabbit nephrons. In: Takács L (ed) Kidney and body fluids, vol 11. Pergamon, Budapest, p 375

    Google Scholar 

  21. Greger R, Hampel W (1981) A modified system for in vitro perfusion of isolated renal tubules. Pflügers Arch 389:175–176

    Google Scholar 

  22. Greger R, Schlatter E (1981) Presence of luminal K+, a prerequisite for active NaCl transport in the cortical thick ascending limb of Henle's loop of rabbit kidney. Pflügers Arch 392:92–94

    Google Scholar 

  23. Greger R, Schlatter E (1983) Properties of the lumen membrane of the cortical thick ascending limb of Henle's loop of rabbit kidney. Pflügers Arch 396:315–324

    Google Scholar 

  24. Greger R, Schlatter E, Cassola AC, Oberleithner H (1982) Cellular mechanisms involved in secondary active chloride transport in the cortical thick ascending limb of Henle's loop of rabbit nephron (cTAL). IVth Eur Col Renal Physiol Praha

  25. Greger R, Schlatter E, Lang F (1983) Evidence for electroneutral sodium chloride cotransport in the cortical thick ascending limb of Henle's loop in rabbit kidney. Pflügers Arch 396:308–314

    Google Scholar 

  26. Guggino WB, Stanton BA, Giebisch G (1982) Electrical properties of isolated early distal tubule of Amphiuma kidney. Fed Proc 41: 1597

    Google Scholar 

  27. Katz AI, Doucet A, Morel F (1979) Na−K-ATPase activity along the rabbit, rat and mouse nephron. Am J Physiol 237:F114-F120

    Google Scholar 

  28. Koenig B, Kinne R (1982) Sodium transport by plasma membranes isolated from cells of the thick ascending limb of Henle's loop. Fed Proc 41:1007

    Google Scholar 

  29. Koeppen BM, Biagi BA, Giebisch G (1982) Intracellular microelectrode characterization of the rabbit cortical collecting duct. Am J Physiol (in press)

  30. Krasny EJ, Halm DR, Frizzell RA (1982) Apical membrane potassium conductance in flounder intestine: Relation to chloride absorption. Fed Proc 41:1261

    Google Scholar 

  31. Musch MW, Orellana SA, Kimberg LS, Field M, Hahn DR, Krasny Jr EJ, Frizzell RA (1982) Na+−K+−Cl co-transport in the intestine of a marine teleost. Nature 300:351–353

    Google Scholar 

  32. Nagel W (1979) Inhibition of potassium conductance by barium in frog skin epithelium. Biochim Biophys Acta 552:346–357

    Google Scholar 

  33. Oberleithner H, Giebisch G (1981) Mechanism of potassium transport across distal tubular epithelium of Amphiuma. In: Macknight ADC, Leader JP (eds) Epithelial ion and water transport. Raven, New York, p 97

    Google Scholar 

  34. Oberleithner H, Giebisch G, Lang F, Wang W (1982) Cellular mechanism of the furosemide sensitive transport system in the kidney. Klin Wochenschr 60:1173–1179

    Google Scholar 

  35. Oberleithner H, Guggino W, Giebisch G (1983) The effect of furosemide on luminal sodium, chloride and potassium transport in the early distal tubule of Amphiuma kidney. Pflügers Arch 396:27–33

    Google Scholar 

  36. Oberleithner H, Guggino W, Giebisch G (1982) Mechanism of distal tubular chloride transport in Amphiuma kidney. Am J Physiol 242:F331–339

    Google Scholar 

  37. Palfrey HC, Feit PW, Greengard P (1980) cAMP-stimulated cation cotransport in avian erythrocytes: inhibition by “loop” diuretics. Am J Physiol 238:C139-C148

    Google Scholar 

  38. Planelles G, Teulon J, Anagnostopoulos T (1981) The effects of barium on the electrical properties of the basolateral membrane in proximal tubule. Naunyn-Schmiedeberg's Arch Pharmacol 318: 135–141

    Google Scholar 

  39. Reuss L (1981) Potassium transport mechanisms by amphibian gallbladder. In: Schultz SG (ed) Ion transport by epithelia. Raven, New York, pp 109–128

    Google Scholar 

  40. Rocha AS, Kokko JP (1973) Sodium chloride and water transport in the medullary thick ascending limb of Henle. Evidence for active chloride transport. J Clin Invest 52:612–623

    Google Scholar 

  41. Sackin H, Morgunov N, Boulpaep EL (1982) Electrical potentials and luminal membrane ion transport in the amphibian renal diluting segment. Fed Proc 41:1495

    Google Scholar 

  42. Schmidt U, Dubach UC (1969) Activity of (Na+, K+)-stimulated adenosin-triphosphatase in the rat nephron. Pflügers Arch 306:219–226

    Google Scholar 

  43. Shindo T, Spring KR (1981) Chloride movement across the basolateral membrane of proximal tubule cells. J Membr Biol 58:35–42

    Google Scholar 

  44. Silva P, Stoff JS, Solomon RJ, Rosa R, Stevens A, Epstein J (1980) Oxygen cost of chloride transport in perfused rectal gland of Squalus acanthias. J Membr Biol 53:215–221

    Google Scholar 

  45. Stokes JB (1982) Consequences of potassium recycling in the renal medulla. Effects on ion transport by the medullary thick ascending limb of Henle's loop. J Clin Invest 70:219–229

    Google Scholar 

  46. Welsh MJ (1982) The effect of barium and potassium on chloride secretion by canine tracheal epithelium. Fed Proc 41:1260

    Google Scholar 

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Greger, R., Schlatter, E. Properties of the basolateral membrane of the cortical thick ascending limb of Henle's loop of rabbit kidney. Pflugers Arch. 396, 325–334 (1983). https://doi.org/10.1007/BF01063938

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