Cell and Tissue Research

, Volume 188, Issue 2, pp 299–315 | Cite as

Ultrastructural, cyto- and biochemical observations during turnover of plasma membrane in duck salt gland

  • Fred E. Hossler
  • Michael P. SarrasJr.
  • E. Raworth Allen
Article
Accepted:

Summary

The mechanism of plasma membrane turnover was investigated using the duckling salt gland as a model system. Feeding fresh water to saltstressed ducklings results in a decrease in the Na, K-ATPase in salt gland to nonstressed levels in about 7 days, as measured by ATP hydrolysis and 3H-ouabain binding. Electron micrographs reveal that this is accompanied by a decrease in plasma membrane infoldings on the basal and lateral borders of gland secretory cells. Simultaneously there is an increase in filamentous material and a rise in acid phosphatase and peptidase activities in these cells. Cytochemistry shows that the acid phosphatase activity is mostly associated with the basal or basolateral regions of secretory cells. These observations could indicate that the removal of plasma membrane components is accomplished by internalization and digestion within the secretory cells.

Key words

Plasma membrane Salt gland (duckling) Na, K-ATPase Ouabain binding Electron microscopy, cytochemistry 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anner, B.M., Lane, L.K., Schwartz, A., Pitts, B.J.R.: A reconstituted Na+ + K+ pump in liposomes containing purified (Na+ + K+)-ATPase from kidney medulla. Biochim. biophys. Acta(Amst.) 467, 340–345 (1977)Google Scholar
  2. Arias, I.M., Doyle, D., Schimke, R.T.: Studies on the synthesis and degradation of proteins of the endoplasmic reticulum of rat liver. J. biol. Chem. 244 3303–3315 (1969)Google Scholar
  3. Berger, L., Broida, D.: Leucine aminopeptidase. Sigma Technical Bulletin, No. 251. St. Louis, Mo.: Sigma Chemical Co., 1974Google Scholar
  4. Cook, J.S., Will, P.C., Proctor, W.R., Brake, E.T.: Turnover of ouabain-binding sites and plasma membrane proteins in HeLa cells. In: Biogenesis and turnover of membrane macromolecules (Cook, J.S., ed.), pp. 15–36. New York: Raven Press 1976Google Scholar
  5. Ellis, R.A.: DNA labelling and x-irradiation studies of the phosphatase-positive peripheral cells in the nasal (salt) glands of ducklings. Amer. Zool. 5, 648 (1965)Google Scholar
  6. Ellis, R.A., Goertemiller, C.C., Jr., DeLellis, R.A., Kablotsky, Y.H.: The effect of a salt water regimen on the development of the salt glands of domestic ducklings. Develop. Biol. 8, 286–308 (1963)Google Scholar
  7. Ernst, S.A.: Transport adenosine triphosphatase cytochemistry. I. Biochemical characterization of a cytochemical medium for the ultrastructural localization of ouabain-sensitive, potassiumdependent phosphatase activity in the avian salt gland. J. Histochem. Cytochem. 20, 13–22 (1972a)Google Scholar
  8. Ernst, S.A.: Transport adenosine triphosphatase cytochemistry. II. Cytochemical localization of ouabain-sensitive, potassium-dependent phosphatase activity in the secretory epithelium of the avian salt gland. J. Histochem. Cytochem. 20, 23–28 (1972b)Google Scholar
  9. Ernst, S.A., Ellis, R.A.: The development of surface specialization in the secretory epithelium of the avian salt gland in response to osmotic stress. J. Cell Biol. 40, 305–321 (1969)Google Scholar
  10. Ernst, S.A., Goertemiller, C.C., Jr., Ellis, R.A.: The effect of salt regimens on the development of (Na+-K+)-dependent ATPase activity during the growth of salt glands of ducklings. Biochim. biophys. Acta (Amst.) 135, 682–692 (1967)Google Scholar
  11. Ernst, S.A., Mills, J.W.: Basolateral plasma membrane localization of ouabain-sensitive sodium transport sites in the secretory epithelium of the avian salt gland. J. Cell Biol. 75, 74–94 (1977)Google Scholar
  12. Ernster, L., Orrenius, S.: Substrate-induced synthesis of the hydroxylating enzyme system of liver microsomes. Fed. Proc. 24, 1190–1199 (1965)Google Scholar
  13. Fletcher, G.L., Stanier, I.M., Holmes, W.N.: Sequential changes in adenosine triphosphatase activity and the electrolyte excretory capacity of the nasal-glands of the duck during the period of adaptation to salt-water. J. exp. Biol. 47, 375–391 (1967)Google Scholar
  14. Goldberg, A.L., St. John, A.C.: Intracellular protein degradation in mammalian and bacterial cells: part 2. Ann. Rev. Biochem. 45, 747–803 (1976)Google Scholar
  15. Hilden, S., Hokin, L.E.: Active potassium transport coupled to active sodium transport in vesicles reconstituted from purified sodium and potassium ion-activated adenosine triphosphatase from the rectal gland of Squalus acanthias J. biol. Chem. 250, 6296–6303 (1975)Google Scholar
  16. Holmes, W.N., Stewart, D J.: Changes in nucleic acid and protein composition of the nasal glands from the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. J. exp. Biol. 48, 509–519 (1968)Google Scholar
  17. Holtzman, E.: Lysosomes: a survey. New York: Springer 1976Google Scholar
  18. Hossler, F.E., Sarras, M.P., Jr., Barrnett, R.J.: Ouabain binding during plasma membrane biogenesis in the duck salt gland. J. Cell Sci., in press (1977)Google Scholar
  19. Karlsson, K.A., Samuelsson, B.E., Steen, G.O.: Lipid pattern and Na+-K+-dependent adenosine triphosphatase activity in the salt gland of duck before and after adaptation to hypertonic saline. J. Membr. Biol. 5, 169–184 (1971)Google Scholar
  20. Levine, A.M., Higgins, J.A., Barrnett, RJ.: Biogenesis of plasma membranes in salt glands of saltstressed domestic ducklings: localization of acyltransferase activity. J. Cell Sci. 11, 855–873 (1972)Google Scholar
  21. Mollenhauer, H.H.: Plastic embedding mixtures for use in electron microscopy. Stain Technol. 39, 111–114 (1964)Google Scholar
  22. Orrenius, S., Ericsson, J.L.E.: Phenobarbital-induced synthesis of the microsomal drug-metabolizing enzyme system and its relationship to the proliferation of endoplasmic membranes. J. Cell Biol. 25, 627–639 (1965)Google Scholar
  23. Peaker, M., Linzell, J.L.: Salt glands in reptiles and birds. London: Cambridge University Press 1975Google Scholar
  24. Rendi, R.: Sodium-potassium requiring adenosinetriphosphatase activity. III. Purification and properties of the adenosinediphosphate-adenosinetriphosphate exchange enzyme. Biochim. biophys. Acta (Amst.) 118, 621–630 (1966)Google Scholar
  25. Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)Google Scholar
  26. Schimke, R.T., Dehlinger, P.J.: Turnover of membrane proteins of animal cells. In: Membrane research (C.F. Fox, ed.). First ICN-UCLA Symposium on Mol. Biol., pp. 115–133. New York: Academic Press (1972)Google Scholar
  27. Siekevitz, P.: Biological membranes: the dynamics of their organization. Ann. Rev. Physiol. 34, 117–140 (1972)Google Scholar
  28. Siekevitz, P.: Dynamics of intracellular membranes. In: Cell membranes — biochemistry, cell biology, and pathology (G. Weissmann and R. Claiborne, eds.), pp. 115–122. New York: H.P. Publishing Co., Inc., 1975Google Scholar
  29. Soll, A.H.: Hormone regulation of hormone receptor concentration: A possible mechanism for altered sensitivity to hormones. In: Biogenesis and turnover of membrane macromolecules (Cook, J.S., ed.), pp. 179–205. New York: Raven Press, 1976Google Scholar
  30. Stewart, D.J., Semple, E.W., Swart, G.T., Sen, A.K.: Induction of the catalytic protein of (Na+ + K+)-ATPase in the salt gland of the duck. Biochim. biophys. Acta (Amst.) 419, 150–163 (1976)Google Scholar
  31. Sweadner, K.J., Goldin, S.M.: Reconstitution of active ion transport by the sodium and potassium ionstimulated adenosine triphosphatase from canine brain. J. biol. Chem. 250, 4022–4024 (1975)Google Scholar
  32. Vaughan, G.L., Cook, J.S.: Regeneration of cation-transport capacity in HeLa cell membranes after specific blockade by ouabain. Proc. nat. Acad. Sci. (Wash.) 69, 2627–2631 (1972)Google Scholar
  33. Wilson, D.R., Knox, W.H., Sax, J., Sen, A.K.: Effect of methylprednisolone on renal Na, K-ATPase deficiency in the postobstructive kidney. In: Biogenesis and turnover of membrane macromolecules (Cook, J.S., ed.), pp. 161–177. New York: Raven Press, 1976Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Fred E. Hossler
    • 1
  • Michael P. SarrasJr.
    • 1
  • E. Raworth Allen
    • 1
  1. 1.Department of AnatomyLouisiana State University Medical CenterNew OrleansUSA

Personalised recommendations