Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1987 Apr 1;89(4):541–562. doi: 10.1085/jgp.89.4.541

Characterization of the basolateral membrane conductance of Necturus urinary bladder

PMCID: PMC2215918  PMID: 2438371

Abstract

Necturus urinary bladders stripped of serosal muscle and connective tissue were impaled through their basolateral membranes with microelectrodes in experiments that permitted rapid changes in the ion composition of the serosal solution. The transepithelial electrical properties exhibited a marked seasonal variation that could be attributed to variations in the conductance of the shunt pathway, apical membrane selectivity, and basolateral Na+ transport. In contrast, the passive electrical properties of the basolateral membrane remained constant throughout the year. The apparent transference numbers (Ti) of the basolateral membrane for K+ and Cl- were determined from the effect on the basolateral membrane equivalent electromotive force of a sudden increase in the serosal K+ concentration from 2.5 to 50 mM/liter or a decrease in the Cl- concentration from 101 to 10 mM/liter. TK and TCl were 0.71 +/- 0.05 and 0.04 +/- 0.01, respectively. The basolateral K+ conductance could be blocked by Ba2+ (0.5 mM), Cs+ (10 mM), or Rb+ (10 mM), but was unaffected by 3,4- diaminopyridine (100 microM), decamethonium (100 microM), or tetraethylammonium (10 mM). We conclude that a highly selective K+ conductance dominates the electrical properties of the basolateral membrane and that this conductance is different from those found in nerve and muscle membranes.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Armstrong C. M. Potassium pores of nerve and muscle membranes. Membranes. 1975;3:325–358. [PubMed] [Google Scholar]
  2. Brown A. M., Sutton R. B., Walker J. L., Jr Increased chloride conductance as the proximate cause of hydrogen ion concentration effects in Aplysia neurons. J Gen Physiol. 1970 Nov;56(5):559–582. doi: 10.1085/jgp.56.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Coronado R., Miller C. Decamethonium and hexamethonium block K+ channels of sarcoplasmic reticulum. Nature. 1980 Dec 4;288(5790):495–497. doi: 10.1038/288495a0. [DOI] [PubMed] [Google Scholar]
  4. Davis C. W., Finn A. L. Cell volume regulation in frog urinary bladder. Fed Proc. 1985 Jun;44(9):2520–2525. [PubMed] [Google Scholar]
  5. Davis C. W., Finn A. L. Sodium transport inhibition by amiloride reduces basolateral membrane potassium conductance in tight epithelia. Science. 1982 Apr 30;216(4545):525–527. doi: 10.1126/science.7071599. [DOI] [PubMed] [Google Scholar]
  6. Demarest J. R., Finn A. L. Interaction between the basolateral K+ and apical Na+ conductances in Necturus urinary bladder. J Gen Physiol. 1987 Apr;89(4):563–580. doi: 10.1085/jgp.89.4.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Demarest J. R. Ion and water transport by the flounder urinary bladder: salinity dependence. Am J Physiol. 1984 Apr;246(4 Pt 2):F395–F401. doi: 10.1152/ajprenal.1984.246.4.F395. [DOI] [PubMed] [Google Scholar]
  8. Findlay I. A patch-clamp study of potassium channels and whole-cell currents in acinar cells of the mouse lacrimal gland. J Physiol. 1984 May;350:179–195. doi: 10.1113/jphysiol.1984.sp015195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finkelstein A., Mauro A. Equivalent Circuits as Related to Ionic Systems. Biophys J. 1963 May;3(3):215–237. doi: 10.1016/s0006-3495(63)86817-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finn A. L., Bright J. The paracellular pathway in toad urinary bladder: permselectivity and kinetics of opening. J Membr Biol. 1978 Dec 8;44(1):67–83. doi: 10.1007/BF01940574. [DOI] [PubMed] [Google Scholar]
  11. Frömter E., Gebler B. Electrical properties of amphibian urinary bladder epithelia. III. The cell membrane resistances and the effect of amiloride. Pflugers Arch. 1977 Oct 19;371(1-2):99–108. doi: 10.1007/BF00580777. [DOI] [PubMed] [Google Scholar]
  12. Frömter E., Higgins J. T., Gebler B. Electrical properties of amphibian urinary bladder epithelia. IV. The current-voltage relationship of the sodium channels in the apical cell membrane. Soc Gen Physiol Ser. 1981;36:31–45. [PubMed] [Google Scholar]
  13. GATZY J. T., CLARKSON T. W. THE EFFECT OF MUCOSAL AND SEROSAL SOLUTION CATIONS ON BIOELECTRIC PROPERTIES OF THE ISOLATED TOAD BLADDER. J Gen Physiol. 1965 Mar;48:647–671. doi: 10.1085/jgp.48.4.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gallacher D. V., Maruyama Y., Petersen O. H. Patch-clamp study of rubidium and potassium conductances in single cation channels from mammalian exocrine acini. Pflugers Arch. 1984 Aug;401(4):361–367. doi: 10.1007/BF00584336. [DOI] [PubMed] [Google Scholar]
  15. Grinstein S., Clarke C. A., Dupre A., Rothstein A. Volume-induced increase of anion permeability in human lymphocytes. J Gen Physiol. 1982 Dec;80(6):801–823. doi: 10.1085/jgp.80.6.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Higgins J. T., Jr, Cesaro L., Gebler B., Frömter E. Electrical properties of amphibian urinary bladder epithelia. I. Inverse relationship between potential difference and resistance in tightly mounted preparations. Pflugers Arch. 1975 Jul 9;358(1):41–56. doi: 10.1007/BF00584568. [DOI] [PubMed] [Google Scholar]
  17. Higgins J. T., Jr, Gebler B., Frömter E. Electrical properties of amphibian urinary bladder epithelia. II. The cell potential profile in necturus maculosus. Pflugers Arch. 1977 Oct 19;371(1-2):87–97. doi: 10.1007/BF00580776. [DOI] [PubMed] [Google Scholar]
  18. KOEFOED-JOHNSEN V., USSING H. H. The nature of the frog skin potential. Acta Physiol Scand. 1958 Jun 2;42(3-4):298–308. doi: 10.1111/j.1748-1716.1958.tb01563.x. [DOI] [PubMed] [Google Scholar]
  19. Karnaky K. J., Jr, Lau K. R., Garretson L. T., Schultz S. G. Seasonal variations in the fine structure of the Necturus maculosus urinary bladder epithelium: low transporters and high transporters. Am J Anat. 1984 Oct;171(2):227–242. doi: 10.1002/aja.1001710208. [DOI] [PubMed] [Google Scholar]
  20. Kirk K. L., Dawson D. C. Basolateral potassium channel in turtle colon. Evidence for single-file ion flow. J Gen Physiol. 1983 Sep;82(3):297–313. doi: 10.1085/jgp.82.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LEB D. E., HOSHIKO T., LINDLEY B. D., DUGAN J. A. EFFECT OF ALKALI METAL CATIONS ON THE POTENTIAL ACROSS TOAD AND BULLFROG URINARY BLADDER. J Gen Physiol. 1965 Jan;48:527–540. doi: 10.1085/jgp.48.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. LINDLEY B. D., HOSHIKO T. THE EFFECTS OF ALKALI METAL CATIONS AND COMMON ANIONS ON THE FROG SKIN POTENTIAL. J Gen Physiol. 1964 Mar;47:749–771. doi: 10.1085/jgp.47.4.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Latorre R., Miller C. Conduction and selectivity in potassium channels. J Membr Biol. 1983;71(1-2):11–30. doi: 10.1007/BF01870671. [DOI] [PubMed] [Google Scholar]
  24. Lefevre M. E., Norris J., Hammer R. Sex differences in Necturus urinary bladders. Anat Rec. 1977 Jan;187(1):47–62. doi: 10.1002/ar.1091870105. [DOI] [PubMed] [Google Scholar]
  25. Lewis S. A., Wills N. K., Eaton D. C. Basolateral membrane potential of a tight epithelium: ionic diffusion and electrogenic pumps. J Membr Biol. 1978 Jun 28;41(2):117–148. doi: 10.1007/BF01972629. [DOI] [PubMed] [Google Scholar]
  26. Lewis S. A., Wills N. K. Electrical properties of the rabbit urinary bladder assessed using gramicidin D. J Membr Biol. 1982;67(1):45–53. doi: 10.1007/BF01868646. [DOI] [PubMed] [Google Scholar]
  27. Nagel W., Garcia-Diaz J. F., Armstrong W. M. Intracellular ionic activities in frog skin. J Membr Biol. 1981;61(2):127–134. doi: 10.1007/BF02007639. [DOI] [PubMed] [Google Scholar]
  28. Nagel W., Garcia-Diaz J. F., Essig A. Contribution of junctional conductance to the cellular voltage-divider ratio in frog skins. Pflugers Arch. 1983 Dec;399(4):336–341. doi: 10.1007/BF00652761. [DOI] [PubMed] [Google Scholar]
  29. Nagel W., Hirschmann W. K+-permeability of the outer border of the frog skin (R. temporaria). J Membr Biol. 1980;52(2):107–113. doi: 10.1007/BF01869115. [DOI] [PubMed] [Google Scholar]
  30. Nagel W. Inhibition of potassium conductance by barium in frog skin epithelium. Biochim Biophys Acta. 1979 Apr 4;552(2):346–357. doi: 10.1016/0005-2736(79)90289-x. [DOI] [PubMed] [Google Scholar]
  31. Nielsen R. Active transepithelial potassium transport in frog skin via specific potassium channels in the apical membrane. Acta Physiol Scand. 1984 Feb;120(2):287–296. doi: 10.1111/j.1748-1716.1984.tb00136.x. [DOI] [PubMed] [Google Scholar]
  32. Oberleithner H., Greger R., Neuman S., Lang F., Giebisch G., Deetjen P. Omission of luminal potassium reduces cellular chloride in early distal tubule of amphibian kidney. Pflugers Arch. 1983 Jun;398(1):18–22. doi: 10.1007/BF00584707. [DOI] [PubMed] [Google Scholar]
  33. Ramsay A. G., Gallagher D. L., Shoemaker R. L., Sachs G. Barium inhibition of sodium ion transport in toad bladder. Biochim Biophys Acta. 1976 Jul 1;436(3):617–627. doi: 10.1016/0005-2736(76)90445-4. [DOI] [PubMed] [Google Scholar]
  34. Reuss L. Electrical properties of the cellular transepithelial pathway in Necturus gallbladder: III. Ionic permeability of the basolateral cell membrane. J Membr Biol. 1979 May 25;47(3):239–259. doi: 10.1007/BF01869080. [DOI] [PubMed] [Google Scholar]
  35. Reuss L., Finn A. L. Passive electrical properties of toad urinary bladder epithelium. Intercellular electrical coupling and transepithelial cellular and shunt conductances. J Gen Physiol. 1974 Jul;64(1):1–25. doi: 10.1085/jgp.64.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Reuss L., Weinman S. A. Intracellular ionic activities and transmembrane electrochemical potential differences in gallbladder epithelium. J Membr Biol. 1979 Sep 14;49(4):345–362. doi: 10.1007/BF01868991. [DOI] [PubMed] [Google Scholar]
  37. Schultz S. G. Electrical potential differences and electromotive forces in epithelial tissues. J Gen Physiol. 1972 Jun;59(6):794–798. doi: 10.1085/jgp.59.6.794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schultz S. G., Thompson S. M., Hudson R., Thomas S. R., Suzuki Y. Electrophysiology of Necturus urinary bladder: II. Time-dependent current-voltage relations of the basolateral membranes. J Membr Biol. 1984;79(3):257–269. doi: 10.1007/BF01871064. [DOI] [PubMed] [Google Scholar]
  39. Spector D., Hayslett J. P., Kashgarian M. Na-K-ATPase-mediated seasonal variation of sodium transport in Necturus kidney. Am J Physiol. 1974 Oct;227(4):873–877. doi: 10.1152/ajplegacy.1974.227.4.873. [DOI] [PubMed] [Google Scholar]
  40. Spenney J. G., Shoemaker R. L., Sachs G. Microelectrode studies of fundic gastric mucosa: cellular coupling and shunt conductance. J Membr Biol. 1974;19(1):105–128. doi: 10.1007/BF01869973. [DOI] [PubMed] [Google Scholar]
  41. Strickholm A., Wallin B. G. Relative ion permeabilities in the crayfish giant axon determined from rapid external ion changes. J Gen Physiol. 1967 Aug;50(7):1929–1953. doi: 10.1085/jgp.50.7.1929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thomas S. R., Suzuki Y., Thompson S. M., Schultz S. G. Electrophysiology of Necturus urinary bladder: I. "Instantaneous" current-voltage relations in the presence of varying mucosal sodium concentrations. J Membr Biol. 1983;73(2):157–175. doi: 10.1007/BF01870439. [DOI] [PubMed] [Google Scholar]
  43. Thompson S. M. Relations between chord and slope conductances and equivalent electromotive forces. Am J Physiol. 1986 Feb;250(2 Pt 1):C333–C339. doi: 10.1152/ajpcell.1986.250.2.C333. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Ussing H. H. Volume regulation of frog skin epithelium. Acta Physiol Scand. 1982 Mar;114(3):363–369. doi: 10.1111/j.1748-1716.1982.tb06996.x. [DOI] [PubMed] [Google Scholar]
  46. Van Driessche W., Zeiske W. Ionic channels in epithelial cell membranes. Physiol Rev. 1985 Oct;65(4):833–903. doi: 10.1152/physrev.1985.65.4.833. [DOI] [PubMed] [Google Scholar]
  47. Voûte C. L., Ussing H. H. Some morphological aspects of active sodium transport. The epithelium of the frog skin. J Cell Biol. 1968 Mar;36(3):625–638. doi: 10.1083/jcb.36.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. White J. F. Activity of chloride in absorptive cells of Amphiuma small intestine. Am J Physiol. 1977 Jun;232(6):E553–E559. doi: 10.1152/ajpendo.1977.232.6.E553. [DOI] [PubMed] [Google Scholar]
  49. Wills N. K., Zeiske W., Van Driessche W. Noise analysis reveals K+ channel conductance fluctuations in the apical membrane of rabbit colon. J Membr Biol. 1982;69(3):187–197. doi: 10.1007/BF01870398. [DOI] [PubMed] [Google Scholar]
  50. Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Dynamics of aminopyridine block of potassium channels in squid axon membrane. J Gen Physiol. 1976 Nov;68(5):519–535. doi: 10.1085/jgp.68.5.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Zeiske W., Van Driessche W. Saturable K+ pathway across the outer border of frog skin (rana temporaria): kinetics and inhibition by Cs+ and other cations. J Membr Biol. 1979 May 7;47(1):77–96. doi: 10.1007/BF01869048. [DOI] [PubMed] [Google Scholar]

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

RESOURCES