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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Oct;85(19):7413–7417. doi: 10.1073/pnas.85.19.7413

Aldosterone increases the apical Na+ permeability of toad bladder by two different mechanisms.

C Asher 1, H Garty 1
PMCID: PMC282197  PMID: 3140240

Abstract

The aldosterone-induced augmentation of Na+ transport in toad bladder was analyzed by comparing the hormonal actions on the transepithelial short-circuit current and on the amiloride-sensitive 22Na+ uptake in isolated membrane vesicles. Incubating bladders with 0.5 microM aldosterone for 3 hr evoked more than a 2-fold increase of the short-circuit current (because of the activation or insertion of apical amiloride-blockable channels) but had no effect on the amiloride-sensitive Na+ transport in apical vesicles derived from the treated tissue. A longer incubation (e.g., 6 hr) produced an additional augmentation of the short-circuit current, which was accompanied by about a 3-fold increase of the channel activity in isolated membranes. The stimulatory effect of aldosterone sustained in vesicles was inhibited by the antagonist spironolactone (present at 1000-fold excess) and the protein synthesis inhibitor cycloheximide (1 microM). In addition, triiodothyronine and butyrate, previously reported to partly inhibit the aldosterone-induced increase in short-circuit current, blocked the hormonal effect in vesicles. It is suggested that aldosterone elevates the apical Na+ permeability of target epithelia by two different mechanisms: a relatively fast effect (less than or equal to 3 hr), which is insensitive to triiodothyronine or butyrate and is not sustained by the isolated membrane, and a slower or later (greater than 3 hr) response blocked by these reagents, which is preserved by the isolated membrane. The data also indicate that these processes are mediated by different nuclear receptors.

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Selected References

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  1. Barbry P., Chassande O., Vigne P., Frelin C., Ellory C., Cragoe E. J., Jr, Lazdunski M. Purification and subunit structure of the [3H]phenamil receptor associated with the renal apical Na+ channel. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4836–4840. doi: 10.1073/pnas.84.14.4836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Fanestil D. D., Park C. S. Steroid hormones and the kidney. Annu Rev Physiol. 1981;43:637–649. doi: 10.1146/annurev.ph.43.030181.003225. [DOI] [PubMed] [Google Scholar]
  3. Farman N., Kusch M., Edelman I. S. Aldosterone receptor occupancy and sodium transport in the urinary bladder of Bufo marinus. Am J Physiol. 1978 Sep;235(3):C90–C96. doi: 10.1152/ajpcell.1978.235.3.C90. [DOI] [PubMed] [Google Scholar]
  4. Garty H., Asher C. Ca2+-dependent, temperature-sensitive regulation of Na+ channels in tight epithelia. A study using membrane vesicles. J Biol Chem. 1985 Jul 15;260(14):8330–8335. [PubMed] [Google Scholar]
  5. Garty H., Asher C. Ca2+-induced down-regulation of Na+ channels in toad bladder epithelium. J Biol Chem. 1986 Jun 5;261(16):7400–7406. [PubMed] [Google Scholar]
  6. Garty H., Asher C., Yeger O. Direct inhibition of epithelial Na+ channels by a pH-dependent interaction with calcium, and by other divalent ions. J Membr Biol. 1987;95(2):151–162. doi: 10.1007/BF01869160. [DOI] [PubMed] [Google Scholar]
  7. Garty H., Edelman I. S. Amiloride-sensitive trypsinization of apical sodium channels. Analysis of hormonal regulation of sodium transport in toad bladder. J Gen Physiol. 1983 Jun;81(6):785–803. doi: 10.1085/jgp.81.6.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garty H. Mechanisms of aldosterone action in tight epithelia. J Membr Biol. 1986;90(3):193–205. doi: 10.1007/BF01870126. [DOI] [PubMed] [Google Scholar]
  9. Geering K., Claire M., Gaeggeler H. P., Rossier B. C. Receptor occupancy vs. induction of Na+-K+-ATPase and Na+ transport by aldosterone. Am J Physiol. 1985 Jan;248(1 Pt 1):C102–C108. doi: 10.1152/ajpcell.1985.248.1.C102. [DOI] [PubMed] [Google Scholar]
  10. Geering K., Gaeggeler H. P., Rossier B. C. Effects of thyromimetic drugs on aldosterone-dependent sodium transport in the toad bladder. J Membr Biol. 1984;77(1):15–23. doi: 10.1007/BF01871096. [DOI] [PubMed] [Google Scholar]
  11. Geering K., Girardet M., Bron C., Kraehenbühl J. P., Rossier B. C. Hormonal regulation of (Na+,K+)-ATPase biosynthesis in the toad bladder. Effect of aldosterone and 3,5,3'-triiodo-L-thyronine. J Biol Chem. 1982 Sep 10;257(17):10338–10343. [PubMed] [Google Scholar]
  12. Kipnowski J., Park C. S., Fanestil D. D. Modification of carboxyl of Na+ channel inhibits aldosterone action on Na+ transport. Am J Physiol. 1983 Dec;245(6):F726–F734. doi: 10.1152/ajprenal.1983.245.6.F726. [DOI] [PubMed] [Google Scholar]
  13. Kleyman T. R., Yulo T., Ashbaugh C., Landry D., Cragoe E., Jr, Karlin A., Al-Awqati Q. Photoaffinity labeling of the epithelial sodium channel. J Biol Chem. 1986 Feb 25;261(6):2839–2843. [PubMed] [Google Scholar]
  14. Kusch M., Farman N., Edelman I. S. Binding of aldosterone to cytoplasmic and nuclear receptors of the urinary bladder epithelium of Bufo marinus. Am J Physiol. 1978 Sep;235(3):C82–C89. doi: 10.1152/ajpcell.1978.235.3.C82. [DOI] [PubMed] [Google Scholar]
  15. Macknight A. D., DiBona D. R., Leaf A. Sodium transport across toad urinary bladder: a model "tight" epithelium. Physiol Rev. 1980 Jul;60(3):615–715. doi: 10.1152/physrev.1980.60.3.615. [DOI] [PubMed] [Google Scholar]
  16. Palmer L. G., Edelman I. S. Control of apical sodium permeability in the toad urinary bladder by aldosterone. Ann N Y Acad Sci. 1981;372:1–14. doi: 10.1111/j.1749-6632.1981.tb15453.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Palmer L. G., Speez N. Stimulation of apical Na permeability and basolateral Na pump of toad urinary bladder by aldosterone. Am J Physiol. 1986 Feb;250(2 Pt 2):F273–F281. doi: 10.1152/ajprenal.1986.250.2.F273. [DOI] [PubMed] [Google Scholar]
  19. Pratt R. D., Johnson J. P. Thyroid hormone. Aldosterone antagonism in cultured epithelial cells. Biochim Biophys Acta. 1984 Dec 11;805(4):405–411. doi: 10.1016/0167-4889(84)90024-7. [DOI] [PubMed] [Google Scholar]
  20. Rossier B. C., Claire M., Rafestin-Oblin M. E., Gaeggeler H. P., Geering K. Effects of thyroid hormones and aldosterone on mineralocorticoid binding sites in the toad bladder. J Membr Biol. 1984;77(1):25–32. doi: 10.1007/BF01871097. [DOI] [PubMed] [Google Scholar]
  21. Sariban-Sohraby S., Burg M., Wiesmann W. P., Chiang P. K., Johnson J. P. Methylation increases sodium transport into A6 apical membrane vesicles: possible mode of aldosterone action. Science. 1984 Aug 17;225(4663):745–746. doi: 10.1126/science.6463652. [DOI] [PubMed] [Google Scholar]
  22. Truscello A., Geering K., Gäggeler H. P., Rossier B. C. Effects of butyrate on histone deacetylation and aldosterone-dependent Na+ transport in the toad bladder. J Biol Chem. 1983 Mar 10;258(5):3388–3395. [PubMed] [Google Scholar]
  23. Truscello A., Gäggeler H. P., Rossier B. C. Thyroid hormone antagonizes an aldosterone-induced protein: a candidate mediator for the late mineralocorticoid response. J Membr Biol. 1986;89(2):173–183. doi: 10.1007/BF01869713. [DOI] [PubMed] [Google Scholar]
  24. Watlington C. O., Perkins F. M., Munson P. J., Handler J. S. Aldosterone and corticosterone binding and effects on Na+ transport in cultured kidney cells. Am J Physiol. 1982 Jun;242(6):F610–F619. doi: 10.1152/ajprenal.1982.242.6.F610. [DOI] [PubMed] [Google Scholar]

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