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. 1984 Apr 1;83(4):543–561. doi: 10.1085/jgp.83.4.543

The water permeability of toad urinary bladder. II. The value of Pf/Pd(w) for the antidiuretic hormone-induced water permeation pathway

PMCID: PMC2215645  PMID: 6726174

Abstract

Using the methods described in the preceding paper (Levine et al., 1984) for measuring the magnitude of the water-permeable barriers in series with the luminal membrane, we correct measured values of Pd(w) in bladders stimulated with low doses of antidiuretic hormone (ADH) or 8-bromo cyclic AMP to obtain their true values in the luminal membrane. Simultaneously, we also determine Pf. We thus are able to calculate Pf/Pd(w) for the hormone-induced water permeation pathway in the luminal membrane. Our finding is that Pf/Pd(w) approximately equal to 17. Two channel models consistent both with this value and the impermeability of the ADH-induced water permeation pathway to small nonelectrolytes are: (a) a long (approximately equal to 50 A), small- radius (approximately equal to 2 A) pore through which 17 water molecules pass in single-file array, and (b) a shower-head-like structure in which the stem is long and of large radius (approximately equal to 20 A) and the cap has numerous short, small-radius (approximately equal to 2 A) pores. A third possibility is that whereas the selective permeability to H2O results from small-radius (approximately equal to 2 A) pores, the large value of Pf/Pd(w) arises from their location in the walls of long tubular vesicles (approximately 2 micron in length and 0.1 micron in diameter) that are functionally part of the luminal membrane after having fused with it. Aggregate-containing tubular vesicles of these dimensions have been reported to fuse with the luminal membrane in response to ADH stimulation and have been implicated in the ADH-induced hydroosmotic response.

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Selected References

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  1. ANDERSEN B., USSING H. H. Solvent drag on non-electrolytes during osmotic flow through isolated toad skin and its response to antidiuretic hormone. Acta Physiol Scand. 1957 Jun 8;39(2-3):228–239. doi: 10.1111/j.1748-1716.1957.tb01425.x. [DOI] [PubMed] [Google Scholar]
  2. Al-Zahid G., Schafer J. A., Troutman S. L., Andreoli T. E. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules: evidence for parallel ADH-sensitive pathways for water and solute diffusion in luminal plasma membranes. J Membr Biol. 1977 Feb 24;31(1-2):103–129. doi: 10.1007/BF01869401. [DOI] [PubMed] [Google Scholar]
  3. Cass A., Finkelstein A. Water permeability of thin lipid membranes. J Gen Physiol. 1967 Jul;50(6):1765–1784. doi: 10.1085/jgp.50.6.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DURBIN R. P. Osmotic flow of water across permeable cellulose membranes. J Gen Physiol. 1960 Nov;44:315–326. doi: 10.1085/jgp.44.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Finkelstein A. Nature of the water permeability increase induced by antidiuretic hormone (ADH) in toad urinary bladder and related tissues. J Gen Physiol. 1976 Aug;68(2):137–143. doi: 10.1085/jgp.68.2.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Finkelstein A. Thin lipid membranes. A model for cell membranes. Arch Intern Med. 1972 Feb;129(2):229–240. [PubMed] [Google Scholar]
  7. Finkelstein A. Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol. 1976 Aug;68(2):127–135. doi: 10.1085/jgp.68.2.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grantham J. J., Burg M. B. Effect of vasopressin and cyclic AMP on permeability of isolated collecting tubules. Am J Physiol. 1966 Jul;211(1):255–259. doi: 10.1152/ajplegacy.1966.211.1.255. [DOI] [PubMed] [Google Scholar]
  9. HAYS R. M., LEAF A. Studies on the movement of water through the isolated toad bladder and its modification by vasopressin. J Gen Physiol. 1962 May;45:905–919. doi: 10.1085/jgp.45.5.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hebert S. C., Andreoli T. E. Interactions of temperature and ADH on transport processes in cortical collecting tubules. Am J Physiol. 1980 Jun;238(6):F470–F480. doi: 10.1152/ajprenal.1980.238.6.F470. [DOI] [PubMed] [Google Scholar]
  11. Holz R., Finkelstein A. The water and nonelectrolyte permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B. J Gen Physiol. 1970 Jul;56(1):125–145. doi: 10.1085/jgp.56.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. KOEFOED-JOHNSEN V., USSING H. H. The contributions of diffusion and flow to the passage of D2O through living membranes; effect of neurohypophyseal hormone on isolated anuran skin. Acta Physiol Scand. 1953 Mar 31;28(1):60–76. doi: 10.1111/j.1748-1716.1953.tb00959.x. [DOI] [PubMed] [Google Scholar]
  13. Kachadorian W. A., Levine S. D., Wade J. B., Di Scala V. A., Hays R. M. Relationship of aggregated intramembranous particles to water permeability in vasopressin-treated toad urinary bladder. J Clin Invest. 1977 Mar;59(3):576–581. doi: 10.1172/JCI108673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kachadorian W. A., Muller J., Finkelstein A. Role of osmotic forces in exocytosis: studies of ADH-induced fusion in toad urinary bladder. J Cell Biol. 1981 Nov;91(2 Pt 1):584–588. doi: 10.1083/jcb.91.2.584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kachadorian W. A., Wade J. B., DiScala V. A. Vasopressin: induced structural change in toad bladder luminal membrane. Science. 1975 Oct 3;190(4209):67–69. doi: 10.1126/science.809840. [DOI] [PubMed] [Google Scholar]
  16. Kachadorian W. A., Wade J. B., Uiterwyk C. C., DiScala V. A. Membrane structural and functional responses to vasopressin in toad bladder. J Membr Biol. 1977 Jan 28;30(4):381–401. doi: 10.1007/BF01869678. [DOI] [PubMed] [Google Scholar]
  17. Levine S. D., Jacoby M., Finkelstein A. The water permeability of toad urinary bladder. I. Permeability of barriers in series with the luminal membrane. J Gen Physiol. 1984 Apr;83(4):529–541. doi: 10.1085/jgp.83.4.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Levine S. D., Kachadorian W. A. Barriers to water flow in vasopressin-treated toad urinary bladder. J Membr Biol. 1981;61(2):135–139. doi: 10.1007/BF02007640. [DOI] [PubMed] [Google Scholar]
  19. Levine S. D., Kachadorian W. A., Levin D. N., Schlondorff D. Effects of trifluoperazine on function and structure of toad urinary bladder. Role of calmodulin vasopressin-stimulation of water permeability. J Clin Invest. 1981 Mar;67(3):662–672. doi: 10.1172/JCI110081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levine S., Franki N., Hays R. M. Effect of phloretin on water and solute movement in the toad bladder. J Clin Invest. 1973 Jun;52(6):1435–1442. doi: 10.1172/JCI107317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Levitt D. G. A new theory of transport for cell membrane pores. I. General theory and application to red cell. Biochim Biophys Acta. 1974 Nov 27;373(1):115–131. doi: 10.1016/0005-2736(74)90111-4. [DOI] [PubMed] [Google Scholar]
  22. Muller J., Kachadorian W. A., DiScala V. A. Evidence that ADH-stimulated intramembrane particle aggregates are transferred from cytoplasmic to luminal membranes in toad bladder epithelial cells. J Cell Biol. 1980 Apr;85(1):83–95. doi: 10.1083/jcb.85.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. PAGANELLI C. V., SOLOMON A. K. The rate of exchange of tritiated water across the human red cell membrane. J Gen Physiol. 1957 Nov 20;41(2):259–277. doi: 10.1085/jgp.41.2.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. PAPPENHEIMER J. R. Passage of molecules through capillary wals. Physiol Rev. 1953 Jul;33(3):387–423. doi: 10.1152/physrev.1953.33.3.387. [DOI] [PubMed] [Google Scholar]
  25. PRESCOTT D. M., ZEUTHEN E. Comparison of water diffusion and water filtration across cell surfaces. Acta Physiol Scand. 1953 Mar 31;28(1):77–94. doi: 10.1111/j.1748-1716.1953.tb00960.x. [DOI] [PubMed] [Google Scholar]
  26. Parisi M., Bourguet J. The single file hypothesis and the water channels induced by antidiuretic hormone. J Membr Biol. 1983;71(3):189–193. doi: 10.1007/BF01875460. [DOI] [PubMed] [Google Scholar]
  27. Parsegian A. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature. 1969 Mar 1;221(5183):844–846. doi: 10.1038/221844a0. [DOI] [PubMed] [Google Scholar]
  28. Pietras R. J., Wright E. M. The membrane action of antidiuretic hormone (ADH) on toad urinary bladder. J Membr Biol. 1975;22(2):107–123. doi: 10.1007/BF01868166. [DOI] [PubMed] [Google Scholar]
  29. ROBBINS E., MAURO A. Experimental study of the independence of diffusion and hydrodynamic permeability coefficients in collodion membranes. J Gen Physiol. 1960 Jan;43:523–532. doi: 10.1085/jgp.43.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rosenberg P. A., Finkelstein A. Water permeability of gramicidin A-treated lipid bilayer membranes. J Gen Physiol. 1978 Sep;72(3):341–350. doi: 10.1085/jgp.72.3.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]

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