Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1974 Nov 1;64(5):582–607. doi: 10.1085/jgp.64.5.582

Volume Reabsorption, Transepithelial Potential Differences, and Ionic Permeability Properties in Mammalian Superficial Proximal Straight Tubules

James A Schafer 1, Susan L Troutman 1, Thomas E Andreoli 1
PMCID: PMC2226162  PMID: 4443793

Abstract

This paper describes experiments designed to evaluate Na+ and Cl- transport in isolated proximal straight tubules from rabbit kidneys. When the perfusing solution was Krebs-Ringer buffer with 25 mM HCO3 - (KRB) and the bath contained KRB plus 6% albumin, net volume reabsorption (Jv, nl min-1 mm-1 was -0.46 ± 0.03 (SEM); Ve, the spontaneous transepithelial potential difference, was -1.13 ± 0.05 mV, lumen negative. Both Jv, and Ve, were reduced to zero at 21°C or with 10-4 M ouabain, but Jv, was not HCO3 - dependent. Net Na+ reabsorption, measured as the difference between 22Na+ fluxes, lumen to bath and bath to lumen, accounted quantitatively for volume reabsorption, assuming the latter to be an isotonic process, and was in agreement with the difference between lumen to bath 22Na+ fluxes during volume reabsorption and at zero volume flow. The observed flux ratio for Na+ was 1.46, and that predicted for a passive process was 0.99; thus, Na+ reabsorption was rationalized in terms of an active transport process. The Cl- concentration of tubular fluid rose from 113.6 to 132.3 mM during volume reabsorption. Since Ve, rose to +0.82 mV when tubules were perfused with 138.6 mM Cl- solutions, Ve may become positive when tubular fluid Cl- concentrations rise during volume reabsorption. The permeability coefficients P Na and P Cl computed from tracer fluxes were, respectively, 0.23 x 10-4 and 0.73 x 10-4 cm s-1. A P Na/P Cl ratio of 0.3 described NaCl dilution potentials at zero volume flow. The magnitudes of the potentials were the same for a given NaCl gradient in either direction and P Na/P Cl was constant in the range 32–139 mM NaCl. We infer that the route of passive ion permeation was through symmetrical extracellular interfaces, presumably tight junctions, characterized by neutral polar sites in which electroneutrality is maintained by mobile counterions.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BAKER P. F., HODGKIN A. L., MEVES H. THE EFFECT OF DILUTING THE INTERNAL SOLUTION ON THE ELECTRICAL PROPERTIES OF A PERFUSED GIANT AXON. J Physiol. 1964 Apr;170:541–560. doi: 10.1113/jphysiol.1964.sp007348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennett C. M., Brenner B. M., Berliner R. W. Micropuncture study of nephron function in the rhesus monkey. J Clin Invest. 1968 Jan;47(1):203–216. doi: 10.1172/JCI105710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boulpaep E. L., Seely J. F. Electrophysiology of proximal and distal tubules in the autoperfused dog kidney. Am J Physiol. 1971 Oct;221(4):1084–1096. doi: 10.1152/ajplegacy.1971.221.4.1084. [DOI] [PubMed] [Google Scholar]
  4. Burg M. B., Issaacson L., Grantham J., Orloff J. Electrical properties of isolated perfused rabbit renal tubules. Am J Physiol. 1968 Oct;215(4):788–794. doi: 10.1152/ajplegacy.1968.215.4.788. [DOI] [PubMed] [Google Scholar]
  5. Burg M. B., Orloff J. Electrical potential difference across proximal convoluted tubules. Am J Physiol. 1970 Dec;219(6):1714–1716. doi: 10.1152/ajplegacy.1970.219.6.1714. [DOI] [PubMed] [Google Scholar]
  6. Burg M., Grantham J., Abramow M., Orloff J. Preparation and study of fragments of single rabbit nephrons. Am J Physiol. 1966 Jun;210(6):1293–1298. doi: 10.1152/ajplegacy.1966.210.6.1293. [DOI] [PubMed] [Google Scholar]
  7. CLAPP J. R., WATSON J. F., BERLINER R. W. OSMOLALITY, BICARBONATE CONCENTRATION, AND WATER REABSORPTION IN PROXIMAL TUBULE OF THE DOG NEPHRON. Am J Physiol. 1963 Aug;205:273–280. doi: 10.1152/ajplegacy.1963.205.2.273. [DOI] [PubMed] [Google Scholar]
  8. DIAMOND J. M. TRANSPORT OF SALT AND WATER IN RABBIT AND GUINEA PIG GALL BLADDER. J Gen Physiol. 1964 Sep;48:1–14. doi: 10.1085/jgp.48.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DIAMOND J. M. The mechanism of solute transport by the gall-bladder. J Physiol. 1962 May;161:474–502. doi: 10.1113/jphysiol.1962.sp006899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frizzell R. A., Schultz S. G. Ionic conductances of extracellular shunt pathway in rabbit ileum. Influence of shunt on transmural sodium transport and electrical potential differences. J Gen Physiol. 1972 Mar;59(3):318–346. doi: 10.1085/jgp.59.3.318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. GIEBISCH G., KLOSE R. M., MALNIC G., SULLIVAN W. J., WINDHAGER E. E. SODIUM MOVEMENT ACROSS SINGLE PERFUSED PROXIMAL TUBULES OF RAT KIDNEYS. J Gen Physiol. 1964 Jul;47:1175–1194. doi: 10.1085/jgp.47.6.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GIEBISCH G. Measurements of electrical potential differences on single nephrons of the perfused Necturus kidney. J Gen Physiol. 1961 Mar;44:659–678. doi: 10.1085/jgp.44.4.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GOTTSCHALK C. W., LASSITER W. E., MYLLE M. Localization of urine acidification in the mammalian kidney. Am J Physiol. 1960 Mar;198:581–585. doi: 10.1152/ajplegacy.1960.198.3.581. [DOI] [PubMed] [Google Scholar]
  15. Grantham J. J., Qualizza P. B., Welling L. W. Influence of serum proteins on net fluid reabsorption of isolated proximal tubules. Kidney Int. 1972 Aug;2(2):66–75. doi: 10.1038/ki.1972.73. [DOI] [PubMed] [Google Scholar]
  16. HODGKIN A. L., HUXLEY A. F. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol. 1952 Apr;116(4):449–472. doi: 10.1113/jphysiol.1952.sp004717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hegel U., Frömter E., Wick T. Der elektrische Wandwiderstand des proximalen Konvolutes der Rattenniere. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;294(4):274–290. [PubMed] [Google Scholar]
  18. Hoshi T., Sakai F. A comparison of the electrical resistances of the surface cell membrane and cellular wall in the proximal tubule of the newt kidney. Jpn J Physiol. 1967 Dec 15;17(6):627–637. doi: 10.2170/jjphysiol.17.627. [DOI] [PubMed] [Google Scholar]
  19. Keynes R. D. From frog skin to sheep rumen: a survey of transport of salts and water across multicellular structures. Q Rev Biophys. 1969 Aug;2(3):177–281. doi: 10.1017/s0033583500001086. [DOI] [PubMed] [Google Scholar]
  20. Kokko J. P., Burg M. B., Orloff J. Characteristics of NaCl and water transport in the renal proximal tubule. J Clin Invest. 1971 Jan;50(1):69–76. doi: 10.1172/JCI106485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kokko J. P. Proximal tubule potential difference. Dependence on glucose on glucose, HCO 3 , and amino acids. J Clin Invest. 1973 Jun;52(6):1362–1367. doi: 10.1172/JCI107308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kokko J. P., Rector F. C. Flow dependence of transtubular potential difference in isolated perfused segments of rabbit proximal convoluted tubule. J Clin Invest. 1971 Dec;50(12):2745–2750. doi: 10.1172/JCI106776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lutz M. D., Cardinal J., Burg M. B. Electrical resistance of renal proximal tubule perfused in vitro. Am J Physiol. 1973 Sep;225(3):729–734. doi: 10.1152/ajplegacy.1973.225.3.729. [DOI] [PubMed] [Google Scholar]
  24. OKEN D. E., WHITTEMBURY G., WINDHAGER E. E., SOLOMON A. K. Single proximal tubules of Necturus kidney. V. Unidirectional sodium movement. Am J Physiol. 1963 Mar;204:372–376. doi: 10.1152/ajplegacy.1963.204.3.372. [DOI] [PubMed] [Google Scholar]
  25. RECTOR F. C., Jr, CARTER N. W., SELDIN D. W. THE MECHANISM OF BICARBONATE REABSORPTION IN THE PROXIMAL AND DISTAL TUBULES OF THE KIDNEY. J Clin Invest. 1965 Feb;44:278–290. doi: 10.1172/JCI105142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. SCHATZMANN H. J., WINDHAGER E. E., SOLOMON A. K. Single proximal tubules of the Necturus kidney. II. Effect of 2, 4-dinitro-phenol and ouabain on water reabsorption. Am J Physiol. 1958 Dec;195(3):570–574. doi: 10.1152/ajplegacy.1958.195.3.570. [DOI] [PubMed] [Google Scholar]
  27. Sandblom J. P., Eisenman G. Membrane potentials at zero current. The significance of a constant ionic permeability ratio. Biophys J. 1967 May;7(3):217–242. doi: 10.1016/S0006-3495(67)86585-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schafer J. A., Andreoli T. E. Cellular constraints to diffusion. The effect of antidiuretic hormone on water flows in isolated mammalian collecting tubules. J Clin Invest. 1972 May;51(5):1264–1278. doi: 10.1172/JCI106921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schafer J. A., Andreoli T. E. The effect of antidiuretic hormone on solute flows in mammalian collecting tubules. J Clin Invest. 1972 May;51(5):1279–1286. doi: 10.1172/JCI106922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schafer J. A., Troutman S. L., Andreoli T. E. Osmosis in cortical collecting tubules. ADH-independent osmotic flow rectification. J Gen Physiol. 1974 Aug;64(2):228–240. [PMC free article] [PubMed] [Google Scholar]
  31. Spring K. R., Paganelli C. V. Sodium flux in Necturus proximal tubule under voltage clamp. J Gen Physiol. 1972 Aug;60(2):181–201. doi: 10.1085/jgp.60.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tune B. M., Burg M. B. Glucose transport by proximal renal tubules. Am J Physiol. 1971 Aug;221(2):580–585. doi: 10.1152/ajplegacy.1971.221.2.580. [DOI] [PubMed] [Google Scholar]
  33. USSING H. H., WINDHAGER E. E. NATURE OF SHUNT PATH AND ACTIVE SODIUM TRANSPORT PATH THROUGH FROG SKIN EPITHELIUM. Acta Physiol Scand. 1964 Aug;61:484–504. [PubMed] [Google Scholar]
  34. WINDHAGER E. E., GIEBISCH G. Comparison of short-circuit current and net water movement in single perfused proximal tubules of rat kidneys. Nature. 1961 Sep 16;191:1205–1207. doi: 10.1038/1911205a0. [DOI] [PubMed] [Google Scholar]
  35. WINDHAGER E. E., WHITTEMBURY G., OKEN D. E., SCHATZMANN H. J., SOLOMON A. K. Single proximal tubules of the Necturus kidney. III. Dependence of H2O movement on NaCl concentration. Am J Physiol. 1959 Aug;197:313–318. doi: 10.1152/ajplegacy.1959.197.2.313. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES