Skip to main content
NCBI home page
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
. 1974 Jul;71(7):2595–2599. doi: 10.1073/pnas.71.7.2595

Target Cell Polarity and Membrane Phosphorylation in Relation to the Mechanism of Action of Antidiuretic Hormone

Irving L Schwartz *, Linda J Shlatz *, Evamarie Kinne-Saffran †, Rolf Kinne †
PMCID: PMC388512  PMID: 4369261

Abstract

The plasma membrane of the bovine renal collecting duct epithelial cell has been resolved into its apical (luminal) and basal-lateral (contraluminal) components by free flow electrophoresis. The contraluminal, but not the luminal, membrane was found to contain antidiuretic hormone-sensitive adenylate cyclase. The luminal membrane was found to contain a cyclic 3′:5′-adenosine monophosphate-sensitive self-phosphorylating system consisting of a membrane-bound protein kinase and its membrane-bound substrate(s); this intrinsic protein kinase was not present in the contraluminal membrane.

These findings provide direct evidence that the initiating steps in the action of antidiuretic hormone on the kidney take place at the contraluminal pole of the hormonesensitive target cell and that the late or terminal steps occur at the luminal pole, where they involve an alteration in the level of membrane phosphorylation.

Keywords: adenylate cyclase, protein kinase, renal collecting duct, luminal and contraluminal membranes

Full text

PDF
2595

Selected References

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

  1. BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
  2. Bentley P. J. The physiology of the urinary bladder of amphibia. Biol Rev Camb Philos Soc. 1966 May;41(2):275–316. doi: 10.1111/j.1469-185x.1966.tb01494.x. [DOI] [PubMed] [Google Scholar]
  3. Blum A. L., Shah G., St Pierre T., Helander H. F., Sung C. P., Wiebelhaus V. D., Sachs G. Properties of soluble ATPase of gastric mucosa. I. Effect of HCO 3 -. Biochim Biophys Acta. 1971 Oct 12;249(1):101–113. doi: 10.1016/0005-2736(71)90087-3. [DOI] [PubMed] [Google Scholar]
  4. Bär H. P., Hechter O. Adenyl cyclase assay in fat cell ghosts. Anal Biochem. 1969 Jun;29(3):476–489. doi: 10.1016/0003-2697(69)90332-7. [DOI] [PubMed] [Google Scholar]
  5. Campbell B. J., Woodward G., Borberg V. Calcium-mediated interactions between the antidiuretic hormone and renal plasma membranes. J Biol Chem. 1972 Oct 10;247(19):6167–6175. [PubMed] [Google Scholar]
  6. DeLorenzo R. J., Walton K. G., Curran P. F., Greengard P. Regulation of phosphorylation of a specific protein in toad-bladder membrane by antidiuretic hormone and cyclic AMP, and its possible relationship to membrane permeability changes. Proc Natl Acad Sci U S A. 1973 Mar;70(3):880–884. doi: 10.1073/pnas.70.3.880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Delorenzo R. J., Greengard P. Activation by adenosine 3':5'-monophosphate of a membrane-bound phosphoprotein phosphatase from toad bladder. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1831–1835. doi: 10.1073/pnas.70.6.1831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dousa T. P., Sands H., Hechter O. Cyclic AMP-dependent reversible phosphorylation of renal medullary plasma membrane protein. Endocrinology. 1972 Sep;91(3):757–763. doi: 10.1210/endo-91-3-757. [DOI] [PubMed] [Google Scholar]
  9. Dousa T., Hechter O., Walter R., Schwartz I. L. [8-Arginine]-vasopressinoic acid: an inhibitor of rabbit kidney adenyl cyclase. Science. 1970 Feb 20;167(3921):1134–1135. doi: 10.1126/science.167.3921.1134. [DOI] [PubMed] [Google Scholar]
  10. Forte L. R., Chao W. T., Walkenbach R. J., Byington K. H. Kidney membrane cyclic AMP receptor and cyclic AMP-dependent protein kinase activities: comparison of plasma membrane and cytoplasmic fractions. Biochem Biophys Res Commun. 1972 Dec 18;49(6):1510–1517. doi: 10.1016/0006-291x(72)90511-6. [DOI] [PubMed] [Google Scholar]
  11. Forte L. R. Characterization of the adenyl cyclase of rat kidney plasma membranes. Biochim Biophys Acta. 1972 May 9;266(2):524–542. doi: 10.1016/0005-2736(72)90108-3. [DOI] [PubMed] [Google Scholar]
  12. GIBBS G. E., REIMER K. QUANTITATIVE MICRODETERMINATION OF ENZYMES IN SWEAT GLAND. 3. SUCCINIC DEHYDROGENASE IN CYSTIC FIBROSIS. Proc Soc Exp Biol Med. 1965 Jun;119:470–473. doi: 10.3181/00379727-119-30213. [DOI] [PubMed] [Google Scholar]
  13. Ganote C. E., Grantham J. J., Moses H. L., Burg M. B., Orloff J. Ultrastructural studies of vasopressin effect on isolated perfused renal collecting tubules of the rabbit. J Cell Biol. 1968 Feb;36(2):355–367. doi: 10.1083/jcb.36.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Handler J. S., Orloff J. Factors involved in the action of cyclic AMP on the permeability of mammalian kidney and toad urinary bladder. Ann N Y Acad Sci. 1971 Dec 30;185:345–350. doi: 10.1111/j.1749-6632.1971.tb45260.x. [DOI] [PubMed] [Google Scholar]
  16. Heidrich H. G., Kinne R., Kinne-Saffran E., Hannig K. The polarity of the proximal tubule cell in rat kidney. Different surface charges for the brush-border microvilli and plasma membranes from the basal infoldings. J Cell Biol. 1972 Aug;54(2):232–245. doi: 10.1083/jcb.54.2.232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jard S., Bastide F. A cyclic AMP-dependent protein kinase from frog bladder epithelial cells. Biochem Biophys Res Commun. 1970 May 22;39(4):559–566. doi: 10.1016/0006-291x(70)90240-8. [DOI] [PubMed] [Google Scholar]
  18. Kirchberger M. A., Schwartz I. L., Walter R. Cyclic 3',5'-AMP-dependent protein kinase activity in toad bladder epithelium. Proc Soc Exp Biol Med. 1972 Jun;140(2):657–660. doi: 10.3181/00379727-140-36524. [DOI] [PubMed] [Google Scholar]
  19. Kuo J. F., Krueger B. K., Sanes J. R., Greengard P. Cyclic nucleotide-dependent protein kinases. V. Preparation and properties of adenosine 3',5'-monophosphate-dependent protein kinase from various bovine tissues. Biochim Biophys Acta. 1970 Jul 15;212(1):79–91. doi: 10.1016/0005-2744(70)90180-4. [DOI] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Leaf A. Membrane effects of antidiuretic hormone. Am J Med. 1967 May;42(5):745–756. doi: 10.1016/0002-9343(67)90092-7. [DOI] [PubMed] [Google Scholar]
  22. Marx S. J., Fedak S. A., Aurbach G. D. Preparation and characterization of a hormone-responsive renal plasma membrane fraction. J Biol Chem. 1972 Nov 10;247(21):6913–6918. [PubMed] [Google Scholar]
  23. Neer E. J. The vasopressin-sensitive adenylate cyclase of the rat renal medulla. J Biol Chem. 1973 Jul 10;248(13):4775–4781. [PubMed] [Google Scholar]
  24. Orloff J., Handler J. The role of adenosine 3',5'-phosphate in the action of antidiuretic hormone. Am J Med. 1967 May;42(5):757–768. doi: 10.1016/0002-9343(67)90093-9. [DOI] [PubMed] [Google Scholar]
  25. PEACHEY L. D., RASMUSSEN H. Structure of the toad's urinary bladder as related to its physiology. J Biophys Biochem Cytol. 1961 Aug;10:529–553. doi: 10.1083/jcb.10.4.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sutherland E. W. Studies on the mechanism of hormone action. Science. 1972 Aug 4;177(4047):401–408. doi: 10.1126/science.177.4047.401. [DOI] [PubMed] [Google Scholar]
  27. ULLRICH K. J., EIGLER F. W. Sekretion von Wasserstoffionen in den Sammelrohren des Säugetierniere. Pflugers Arch. 1958;267(5):491–496. doi: 10.1007/BF00361735. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES