Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1984 Jan;73(1):46–52. doi: 10.1172/JCI111205

Energetics of sodium transport in the urinary bladder of the toad. Effect of aldosterone and sodium cyanide.

N Cortas, E Abras, M Arnaout, A Mooradian, S Muakasah
PMCID: PMC424969  PMID: 6317718

Abstract

Experiments were designed to determine whether the stimulatory effect of aldosterone on sodium transport involves an increase in tissue ATP. Urinary bladders that were removed from toads presoaked in 0.6% saline for 48-72 h, mounted as sacs, and maintained in open circuit except for brief observation of short circuit current every 30 min responded to 100 nM aldosterone added to the serosal bath with an increase in short circuit current to 170% of control hemibladders, which plateaus at 2-3 h. Tissue (ATP)/(ADP) X (Pi) measured in perchloric acid extracts increased to a maximum of 208% of controls (P less than 0.001) and ATP increased to 116% of controls (P less than 0.01) at 180 min. The short circuit current response to aldosterone paralleled the increase in ATP and (ATP)/(ADP) X (Pi) measured at 75, 120, 180, and 240 min. In bladders clamped at -150 mV, the short circuit current response to aldosterone was greater: 280% of controls (P less than 0.001) and tissue (ATP)/(ADP) X (Pi) increased to 191% of controls (P less than 0.001). In continuously short circuited bladders and bladders clamped at +75 mV, the short circuit current response to aldosterone and the change in ATP, ADP, or Pi were markedly diminished. 100 microM amiloride added to mucosal bath decreased the short circuit current to zero and inhibited the short circuit current response to aldosterone, whereas tissue ATP increased to 141% (P less than 0.05). 100, 250, and 500 microM NaCN dropped the short circuit current to 59, 35, and 24% of control values, respectively. Concurrently, tissue ATP measured at 60 min after the addition of NaCN dropped to 79, 66, and 56% of control values, respectively, and tissue ATP/ADP dropped to 68, 50, and 40%, respectively. The data revealed significant correlation between the change in the rate of sodium transport produced by aldosterone or NaCN as measured by the short circuit current and the concentration of ATP (r = 0.96, P less than 0.001), as well as ATP/ADP (r = 0.95, P less than 0.001). In conclusion, these results support the view that the stimulatory effects of aldosterone on sodium transport involve an increase in ATP or (ATP)/(ADP) X (Pi).

Full text

PDF
46

Images in this article

49Image
on p.49

Selected References

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

  1. Bobrycki V. A., Mills J. W., Macknight A. D., DiBona D. R. Structural responses to voltage-clamping in the toad urinary bladder. I. The principal role of granular cells in the active transport of sodium. J Membr Biol. 1981 May 15;60(1):21–33. doi: 10.1007/BF01870829. [DOI] [PubMed] [Google Scholar]
  2. Civan M. M., Hoffman R. E. Effect of aldosterone on electrical resistance of toad bladder. Am J Physiol. 1971 Feb;220(2):324–328. doi: 10.1152/ajplegacy.1971.220.2.324. [DOI] [PubMed] [Google Scholar]
  3. Cortas N., Walser M. (Na + -K + )-activated ATPase in isolated mucosal cells of toad bladder. Biochim Biophys Acta. 1971 Oct 12;249(1):181–187. doi: 10.1016/0005-2736(71)90095-2. [DOI] [PubMed] [Google Scholar]
  4. De Weer P. Effects of intracellular adenosine-5'-diphosphate and orthophosphate on the sensitivity of sodium efflux from squid axon to external sodium and potassium. J Gen Physiol. 1970 Nov;56(5):583–620. doi: 10.1085/jgp.56.5.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dixon T. E., Al-Awqati Q. H+/ATP stoichiometry of proton pump of turtle urinary bladder. J Biol Chem. 1980 Apr 25;255(8):3237–3239. [PubMed] [Google Scholar]
  6. Edelman I. S. Mechanism of action of aldosterone: energetic and permeability factors. J Endocrinol. 1979 May;81(2):49P–53P. [PubMed] [Google Scholar]
  7. Fanestil D. D., Edelman I. S. On the mechanism of action of aldosterone on sodium transport: effects of inhibitors of RNA and of protein synthesis. Fed Proc. 1966 May-Jun;25(3):912–916. [PubMed] [Google Scholar]
  8. Fuchs W., Larsen E. H., Lindemann B. Current-voltage curve of sodium channels and concentration dependence of sodium permeability in frog skin. J Physiol. 1977 May;267(1):137–166. doi: 10.1113/jphysiol.1977.sp011805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garland H. O., Hendersen I. W. Influence of environmental salinity on renal and adrenocortical function in the toad, Bufo marinus. Gen Comp Endocrinol. 1975 Oct;27(2):136–143. doi: 10.1016/0016-6480(75)90227-0. [DOI] [PubMed] [Google Scholar]
  10. Goodman D. B., Allen J. E., Rasmussen H. On the mechanism of action of aldosterone. Proc Natl Acad Sci U S A. 1969 Sep;64(1):330–337. doi: 10.1073/pnas.64.1.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Handler J. S., Preston A. S., Orloff J. Effect of aldosterone on the sodium content and energy metabolism of epithelial cells of the toad urinary bladder. J Steroid Biochem. 1972 Feb;3(2):137–141. doi: 10.1016/0022-4731(72)90043-x. [DOI] [PubMed] [Google Scholar]
  12. Handler J. S., Preston A. S., Orloff J. The effect of aldosterone of glycolysis in the urinary bladder of the toad. J Biol Chem. 1969 Jun 25;244(12):3194–3199. [PubMed] [Google Scholar]
  13. Hill J. H., Cortas N., Walser M. Aldosterone action and sodium- and potassium-activated adenosine triphosphatase in toad bladder. J Clin Invest. 1973 Jan;52(1):185–189. doi: 10.1172/JCI107163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kirsten E., Kirsten R., Leaf A., Sharp G. W. Increased activity of enzymes of the tricarboxylic acid cycle in response to aldosterone in the toad bladder. Pflugers Arch Gesamte Physiol Menschen Tiere. 1968;300(4):213–225. doi: 10.1007/BF00364295. [DOI] [PubMed] [Google Scholar]
  15. Kirsten E., Kirsten R., Salibian A. A stucy on the effect of aldosterone on the extramitochondrial adenine nucleotide system in rat kidney. J Steroid Biochem. 1972 Feb;3(2):173–179. doi: 10.1016/0022-4731(72)90048-9. [DOI] [PubMed] [Google Scholar]
  16. Kirsten R., Kirsten E. Redox state of pyridine nucleotides in renal response to aldosterone. Am J Physiol. 1972 Jul;223(1):229–235. doi: 10.1152/ajplegacy.1972.223.1.229. [DOI] [PubMed] [Google Scholar]
  17. Lipton P., Edelman I. S. Effects of aldosterone and vasopressin on electrolytes of toad bladder epithelial cells. Am J Physiol. 1971 Sep;221(3):733–741. doi: 10.1152/ajplegacy.1971.221.3.733. [DOI] [PubMed] [Google Scholar]
  18. Majumdar A. P., Trachewsky D. Protein synthesis by ribosomes from rat kidney cortex: effect of aldosterone and bilateral adrenalectomy. Can J Biochem. 1971 May;49(5):501–509. doi: 10.1139/o71-075. [DOI] [PubMed] [Google Scholar]
  19. PORTER G. A., EDELMAN I. S. THE ACTION OF ALDOSTERONE AND RELATED CORTICOSTEROIDS ON SODIUM TRANSPORT ACROSS THE TOAD BLADDER. J Clin Invest. 1964 Apr;43:611–620. doi: 10.1172/JCI104946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Palmer L. G., Edelman I. S., Lindemann B. Current-voltage analysis of apical sodium transport in toad urinary bladder: effects of inhibitors of transport and metabolism. J Membr Biol. 1980 Nov 15;57(1):59–71. doi: 10.1007/BF01868986. [DOI] [PubMed] [Google Scholar]
  21. Palmer L. G., Li J. H., Lindemann B., Edelman I. S. Aldosterone control of the density of sodium channels in the toad urinary bladder. J Membr Biol. 1982;64(1-2):91–102. doi: 10.1007/BF01870771. [DOI] [PubMed] [Google Scholar]
  22. SHARP G. W., LEAF A. BIOLOGICAL ACTION OF ALDOSTERONE IN VITRO. Nature. 1964 Jun 20;202:1185–1188. doi: 10.1038/2021185a0. [DOI] [PubMed] [Google Scholar]
  23. Scott W. N., Sapirstein V. S. Identification of aldosterone-induced proteins in the toad's urinary bladder. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4056–4060. doi: 10.1073/pnas.72.10.4056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sharp G. W., Leaf A. Mechanism of action of aldosterone. Physiol Rev. 1966 Oct;46(4):593–633. doi: 10.1152/physrev.1966.46.4.593. [DOI] [PubMed] [Google Scholar]
  25. Snart R. S., Wheldrake J. F. Effects of saline exposure on the response of toad bladder (Bufo marinus) to aldosterone. Biochim Biophys Acta. 1980 Aug 1;631(1):104–111. doi: 10.1016/0304-4165(80)90058-6. [DOI] [PubMed] [Google Scholar]
  26. USSING H. H., ZERAHN K. Active transport of sodium as the source of electric current in the short-circuited isolated frog skin. Acta Physiol Scand. 1951 Aug 25;23(2-3):110–127. doi: 10.1111/j.1748-1716.1951.tb00800.x. [DOI] [PubMed] [Google Scholar]
  27. Veech R. L., Lawson J. W., Cornell N. W., Krebs H. A. Cytosolic phosphorylation potential. J Biol Chem. 1979 Jul 25;254(14):6538–6547. [PubMed] [Google Scholar]
  28. Vieira F. L., Caplan S. R., Essig A. Energetics of sodium transport in frog skin. I. Oxygen consumption in the short-circuited state. J Gen Physiol. 1972 Jan;59(1):60–76. doi: 10.1085/jgp.59.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Walser M., Butler S. E., Hammond V. Reversible stimulation of sodium transport in the toad bladder by stretch. J Clin Invest. 1969 Sep;48(9):1714–1723. doi: 10.1172/JCI106137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walser M. Components of sodium and chloride flux across toad bladder. Biophys J. 1972 Apr;12(4):351–368. doi: 10.1016/S0006-3495(72)86089-2. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES