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Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule

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Summary

Antidiuretic hormone increases the water permeability of the cortical collecting tubule and causes the appearance of intramembrane particle aggregates in the apical plasma membrane of principal cells. Particle aggregates are located in apical membrane coated pits during stimulation of collecting ducts with ADHin situ. Removal of ADH causes a rapid decline in water permeability. We evaluated apical membrane retrieval associated with removal of ADH by studying the endocytosis of horseradish peroxidase (HRP) from an isotonic solution in the lumen. HRP uptake was quantified enzymatically and its intracellular distribution examined by electron microscopy. When tubules were perfused with HRP for 20 min in the absence of ADH, HRP uptake was 0.5±0.3 pg/min/μm tubule length (n=6). The uptake of HRP in tubules exposed continuously to ADH during the 20-min HRP perfusion period was 1.3±0.8 pg/min/μm (n=8). HPR uptake increased markedly to 3.2±1.1 pg/min/μm (n=14), when the 20-min period of perfusion with HRP began immediately after removal of ADH from the peritubular bath. Endocytosis of HRP occurred in both principal and intercalated cells via apical membrane coated pits. We suggest that the rapid decline in cortical collecting duct water permeability which occurs following removal of ADH is mediated by retrieval of water permeable membrane via coated pits.

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References

  1. Brown, D., Orci, L. 1983. Vasopressin stimulates formation of coated pits in rat kidney collecting ducts.Nature (London) 302:253–255

    Google Scholar 

  2. Brown, D., Shields, G.I., Valtin, H., Morris, J.F., Orci, L. 1985. Lack of intramembranous particle clusters in collecting duct of mice with nephrogenic diabetes insipidus.Am. J. Physiol. 249:F582-F589

    Google Scholar 

  3. Bourguet, J., Chevalier, J., Hugon, J.S. 1976. Alterations in membrane-associated particle distribution during antidiuretic challenge in frog urinary bladder epithelium.Biophys. J. 16:627–639

    Google Scholar 

  4. Burg, M. 1972. Perfusion of isolated renal tubules.Yale J. Biol. Med. 45:321–326

    Google Scholar 

  5. Coleman, R.A., Harris, H.W., Jr., Wade, J.B. 1987. Visualization of endocytosed markers in freeze-fracture studies of toad urinary bladder.J. Histochem. Cytochem. 35:1405–1414

    Google Scholar 

  6. Edwards, B.R., Harmanci, M.C. 1983. Intramembranous particle clusters in collecting duct cells of rats.Renal. Physiol. 6:275–280

    Google Scholar 

  7. Franki, N., Ding, G., Quintana, N., Hays, R.M. 1986. Evidence that heads of ADH-sensitive aggrephores are clathrin-coated vesicles: Implications for aggrephore structure and function.Tissue Cell 18:803–807

    Google Scholar 

  8. Gluck, S., Al-Awqati, Q. 1980. Vasopressin increases water permeability by inducing pores.Nature (London) 284:631–632

    Google Scholar 

  9. Grantham, J.J., Burg, M.B. 1966. Effect of vasopressin and cylic AMP on permeability of isolated collecting tubules.Am. J. Physiol. 211:255–259

    Google Scholar 

  10. Gronowicz, G., Masur, S.K., Holtzman, E. 1980. Quantitative analysis of exocytosis and endocytosis in the hydroosmotic response of toad bladder.J. Membrane Biol. 52:221–235

    Google Scholar 

  11. Handler, J.S., Orloff, J. 1973. The mechanism of action of antidiuretic hormone.In: Handbook of Physiology (Renal Physiolgyy, Section 8). pp. 791–814. American Physiological Society, Washington, D.C.

    Google Scholar 

  12. Harmanci, M.C., Kachadorian, W.A., Valtin, H., DiScala, V.A. 1978. Antidiuretic hormone-induced intramembranous alterations in mammalian collecting ducts.Am. J. Physiol. 235:F440-F443

    Google Scholar 

  13. Harmanci, M.C., Stern, P., Kachadorian, W.A., Valtin, H., DiScala, V.A. 1980. Vasopressin and collecting duct intra-membranous particle clusters: A dose-response relationship.Am. J. Physiol. 239:F560-F564

    Google Scholar 

  14. Harris, H.W., Jr., Wade, J.B., Handler, J.S. 1986. Fluorescent markers to study membrane retrieval in ADH treated toad urinary bladder.Am. J. Physiol. 251:C274-C284

    Google Scholar 

  15. Harris, H.W., Jr., Wade, J.B., Handler, J.S. 1986. Transepithelial water flow regulates apical membrane retrieval in ADH-stimulated toad urinary bladder.J. Clin. Invest. 78:703–712

    Google Scholar 

  16. Hebert, S.C., Andreoli, T.E. 1982. Water movement across the mammalian cortical collecting duct.Kidney Int. 22:526–535

    Google Scholar 

  17. Hebert, S.C., Andreoli, T.E. 1982. Water permeability of biological membranes. Lessons from antidiuretic hormone-responsive epithelia.Biochim. Biophys. Acta 650:267–280

    Google Scholar 

  18. Hebert, S.C., Schafer, J.A., Andreoli, T.E. 1981. The effect of antidiuretic hormone (ADH) on solute and water transport inthe mammalian nephron.J. Membrane Biol. 58:1–19

    Google Scholar 

  19. Humbert, F.R., Montesano, A., Grosso, A., DeSousa, R.C., Orci, L. 1977. Particle aggregates in plasma and intracellular membranes of toad bladder (granular cell).Experientia 33:1364–1367

    Google Scholar 

  20. Kachadorian, W.A., Sariban-Sohraby, S., Spring, K. 1985. Regulation of water permeability in toad urinary bladder at two barriers.Am. J. Physiol. 248:F260-F265

    Google Scholar 

  21. Kachadorian, W.A., Wade, J.B., DiScala, V.A. 1975. Vasopressin induced structural change in toad urinary bladder luminal membrane.

  22. Kaissling, B., Kriz, W. 1979. Structural analysis of the rabbit kidney.In: Advances in Anatomy and Cell Biology. A. Brodal et al., editors. Vol. 56, pp. 1–123. Springer, New York

    Google Scholar 

  23. Kirk, K.L., Buku, A., Eggena, P. 1987. Cell specificity of vasopressin binding in renal collecting duct: Computer enhanced imaging of a fluorescent hormone analog.Proc. Natl. Acad. Sci. USA 84:6000–6004

    Google Scholar 

  24. Levine, S.D., Jacoby, M., Finkelstein, A. 1984. The water permeability of toad urinary bladder. I. Permeability of barriers in series with the luminal membrane.J. Gen. Physiol. 83:529–541

    Google Scholar 

  25. Levine, S.D., Jacoby, M., Finkelstein, A. 1984. The water permeability of toad urinary bladder. II. The value of Pf/Pd for antidiuretic hormone-induced water permeation pathway.J. Gen. Physiol. 83:543–561

    Google Scholar 

  26. Lorenzen, M., Kubat, B., Reale, E. 1986. Quantification of vasopressin-induced intramembranous particle aggregates in isolated cortical collecting tubules (ICCT'S) of rabbit kidney.Kidney Int. 29:419A

    Google Scholar 

  27. Masur, S.K., Cooper, S., Rubin, M.S. 1984. Effect of an osmotic gradient on antidiuretic hormone induced endocytosis and hydroosmosis in the toad urinary bladder.Am. J. Physiol. 247:F370-F379

    Google Scholar 

  28. Muller, J., Kachadorian, W.A. 1984. Aggregate-carrying membranes during ADH stimulation and washout in toad bladder.Am. J. Physiol. 247:C90-C98

    Google Scholar 

  29. Muller, J., Kachadorian, W.A. 1985. Regulation of luminal membrane water permeability by water flow in toad urinary bladder.Biol. Cell 55:219–224

    Google Scholar 

  30. Muller, J., Kachadorian, W.A., DiScala, V.A. 1980. Evidence that ADH-stimulated intramembrane particle aggregates are transferred from cytoplasmic to luminal membranes in toad bladder epithelial cells.J. Cell Biol. 85:83–95

    Google Scholar 

  31. O'Neil, R.G., Boulpaep, E.L. 1982. Iomic conductive properties and electrophysiology of the rabbit cortical collecting tubule.Am. J. Physiol. 243:F81-F95

    Google Scholar 

  32. O'Neil, R.G., Hellman, S.I. 1977. Transport characteristics of renal collecting tubules: Influences of DOCA and diet.Am. J. Physiol. 233:F544-F558

    Google Scholar 

  33. Pastan, I., Willingham, M.C. 1983. Receptor-mediated endocytosis: Coated pits, receptosomes and the golgi.Trends Biochem. Sci. 8:245–250

    Google Scholar 

  34. Ryser, H.J., Drummond, I., Shen, W.C. 1982. The cellular uptake of horseradish peroxidase and its poly (lysine) conjugates by cultured fibroblasts is qualitatively similar despite a 900-fold difference in rate.J. Cell. Physiol. 113:167–178

    Google Scholar 

  35. Sly, W.S., Stahl, P. 1978. Receptor-mediated uptake of lysosomal enzymes.In: Transport of Macromolecules in Cellular Systems. S.A. Silverstein, editor. pp. 229–244. Dahlem-Konferenze, Berlin

    Google Scholar 

  36. Steinman, R.M., Cohn, Z.A. 1972. The interaction of soluble horseardish peroxidase with mouse peritoneal macrophages in vitro.J. Cell Biol. 55:186–204

    Google Scholar 

  37. Strange, K., Spring, K.R. 1986. Methods of imaging renal tubule cells.Kidney Int. 30:192–200

    Google Scholar 

  38. Strange, K., Spring, K.R. 1987. Cell membrane water permeability of rabbit cortical collecting duct.J. Membrane Biol. 96:27–43

    Google Scholar 

  39. Strauss, W. 1981. Cytochemical detection of mannose-specific receptors for glycoproteins with horseradish peroxidase as a ligand.Histochemistry 73:39–44

    Google Scholar 

  40. Wade, J.B. 1985. Membrane structural studies of the action of vasopressin.Fed. Proc. 44:2687–2692

    Google Scholar 

  41. Wade, J.B., Stetson, D.L., Lewis, S.A. 1981. ADH action: Evidence for a membrane shuttle hypothesis.Ann. N.Y. Acad. Sci. 372:106–117

    Google Scholar 

  42. Willingham, M.C., Pastan, I. 1984. Endocytosis and exocytosis: Current concepts of vesicle traffic in animal cells.Int. Rev. Cytol. 92:51–92

    Google Scholar 

  43. Willingham, M.C., Pastan, I. 1985. The pathway of endocytosis.In: Endocytosis. pp. 1–44. Plenum, New York

    Google Scholar 

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Author notes

  1. K. Strange

    Present address: Department of Physiology and Biophysics, Wright State University School of Medicine, 45435, Dayton, Ohio

Authors and Affiliations

  1. Laboratory of Kidney and Electrolyte Metabolism, National Heart, Lung and Blood Institute, National Institutes of Health, 20892, Bethesda, Maryland

    K. Strange & J. S. Handler

  2. Laboratory of Molecular Biology, National Cancer Institute, National Institutes of Health, 20892, Bethesda, Maryland

    M. C. Willingham

  3. Division of Nephrology, The Children's Hospital, 02115, Boston, Massachusetts

    H. W. Harris Jr.

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  1. K. Strange
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  2. M. C. Willingham
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  3. J. S. Handler
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  4. H. W. Harris Jr.
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Strange, K., Willingham, M.C., Handler, J.S. et al. Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule. J. Membrain Biol. 103, 17–28 (1988). https://doi.org/10.1007/BF01871929

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  • DOI: https://doi.org/10.1007/BF01871929

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