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Extracellular Ca2+ and the effect of antidiuretic hormone on the water permeability of the toad urinary bladder: An example of flow-induced alteration of flow

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Summary

The extracellular Ca2+ requirement for antidiuretic hormone (ADH) stimulation of water permeability in the toad urinary bladder has been critically examined. The polarity of the tissue was maintained with 1mm Ca2+ in the mucosal bathing medium and a serosal bath nominally free of Ca2+. Under these condition, ADH-induced osmotic water flow was inhibited by more than 60% while enhancement of the diffusional permeability to water was unaffected. Structural studies revealed that low serosal Ca2+ led to parallel alterations in epithelial architecture that amounted to a significant distorition of the osmotic water pathway. Prevention of these alterations, or restoration of normal cell-cell contact showed that the reduction of serosal Ca2+ did not restrict hormonal action,per se, but that it resulted in a weakening of cell-cell junctions such that intercellular space distension during water flow occurred to a point where the geometric conditions for maintenance of osmotic flow were compromised. We conclude that extracellular Ca2+ is not a requirement for the molecular aspects of ADH action but that, in its absence, a direct measurement of ADH-induced osmotic flow proves to be an inaccurate index of the hormone-generated changes in epithelial transport characteristics. Under certain conditions the ADH-effect on the tissue's hydraulic permeability is probably best assessed by measurement of the diffusional permability to water; although accuracy in this determination is difficult, it is not as strongly dependent on tissue geometry.

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References

  1. Andreoli, T.E., Schafer, J.A. 1976. Mass transport across cell membranes: The effects of antidiretic hormone on water and solute flows in epithelia.Annu. Rev. Physiol. 39:451–500

    Google Scholar 

  2. Arruda, J.A.L., Sabatini, S. 1980. Cholinergic modulation of water transport in the toad bladder.Am. J. Physiol. 239 (Renal Fluid Electrolyte Physiol. 8):F154-F159

    PubMed  Google Scholar 

  3. Bennett, M.V.L. 1973. Funtion of electrotonic junctions in embryonic and adult tissues.Fed. Proc. 32:65–75

    PubMed  Google Scholar 

  4. Bentley, P.J. 1958. The effects of ionic changes on water transfer across the urinary bladder of the toadBufo marinus.J. Endocrinol. 18:327–333

    Google Scholar 

  5. Bentley, P.J. 1960. The effects of vasopressin on the shortcircuit current across the wall of the isolated bladder of the toad,Bufo marinus.J. Endocrinol. 21:161–170

    Google Scholar 

  6. Borle, A.B. 1978. On the difficulty of assessing the role of extracellular calcium in cell function.In: Calcium Transport and Cell Function. A. Scarpa and E. Carafolik editors.Ann. N. Y. Acad. Sci. 307:431–432.

  7. Civan, M.M., DiBona, D.R. 1974. Pathways for movement of ions and water across toad urinary bladder: II. Site and mode of action of vasopressin.J. Membrane Biol. 19:195–220

    Google Scholar 

  8. Cuthbert, A.W., Wong, P.Y.D. 1974. Calcium release in relation to permeability changes in toad bladder epithelium following antidiuretic hormone.J. Physiol. (London) 241:407–422

    Google Scholar 

  9. Dainty, J., House, C.R. 1966a. Unstirred layers in frog skin.J. Physiol. (London) 182:66

    Google Scholar 

  10. Dainty, J., House, C.R. 1966b. An examination of the evidence for membrane pores in frog skin.J. Physiol. (London) 185:172

    Google Scholar 

  11. DiBona, D.R. 1978. Direct visualization of epithelial morphology in the living amphibian urinary bladder.J. Membrane Biol. Special Issue: 45–70.

  12. DiBona, D.R. 1979. Direct visuatization of ADH-mediated transepithelial osmotic flow.In: Hormonal Control of Epithelial Transport. J. Bourguet, editor. Vol. 85, pp. 195–206. Inserm, Paris

    Google Scholar 

  13. DiBona, D.R., Civan, M.M. 1969. Toad urinary bladder: Intercellualr spaces.Science 165:503–504

    PubMed  Google Scholar 

  14. DiBona, D.R., Civan, M.M., Leaf, A. 1969. The cellular specificity of the effect of vasopressin on toad urinary bladder.J. Membrane Biol. 1:79–91

    Google Scholar 

  15. Eggena, P. 1972a. Glutaraldehyde-fixation method for determining the permeability to water of the toad urinary bladder.Endocrinology 91:240–246

    PubMed  Google Scholar 

  16. Eggena, P. 1972b. Osmotic regulation of toad bladder responsiveness to neurohypophyseal hormones.J. Gen. Physiol. 60:665–674

    PubMed  Google Scholar 

  17. Eggena, P., Christakis, J., Deppisch, L. 1975. Effect of hypotonicity on cyclic adenosine monophosphate formation and action in vaspressin target cells.Kidney Int. 7:161–169

    PubMed  Google Scholar 

  18. Ellis, S.J., Kachadorian, W.A., DiScala, V.A. 1980. Effect of osmotic gradient of ADH-induced intramembraneous particle aggregates in toad bladder.J. Membrane Biol. 52:181–184

    Google Scholar 

  19. Handler, J.S., Orloff, J. 1973. The mechanism of antidiuretic hormone.In: Handbook of Physiology; Section 8: Renal Physiology. R. Berliner and J. Orloff, editors. pp. 791–814. American Physiological Society, Washington, D.C.

    Google Scholar 

  20. Hardy, M.A. 1977. Effects of Ca2+ on the hydroosotic action of vasopressin.Physiologist 20:41 (Abstr.)

    Google Scholar 

  21. Hardy, M.A. 1978. Intracellualar calcium as a modulator of transepithelial permeability to water in frog urinary bladder.J. Cell Biol. 76:787–791

    PubMed  Google Scholar 

  22. Hardy, M.A. 1979a. Roles of Na+ and Ca2+ in the inhibition by low pH of the hydroosmotic response to serosal hypertonicity in toad bladder.Biochim. Biophys. Acta 552:169–177

    PubMed  Google Scholar 

  23. Hardy, M.A. 1979b. Ionic requirements of the transepithelial water flow induced by hypertonicity.In: Hormonal Control of Epithelial Transport. J. Bourguet, J. Chevalier, M. Parisi, and P. Ripoche, editors. pp. 311–322. Inserm, Paris

    Google Scholar 

  24. Hardy, M.A., Balsam, P., Bourgoignie, J.J. 1979. Reversible inhibition by lanthanum of the hydrosmotic response to serosal hypertonicity in toad bladder.J. Membrane Biol. 48:13–19

    Google Scholar 

  25. Hardy, M.A., Montoreano, R., Parisi, M. 1975. Colchicine dissociates the toad (Bufo arenarum) urinary bladder responses to antidiuretic hormone and to serosal hypertonicity.Experientia 31:803–804

    PubMed  Google Scholar 

  26. Hays, R.M.,1972. The movement of water across vasopressinsensitive epithelia.In: Current Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. Vol. 3, pp. 339–366. Academic Press New York

    Google Scholar 

  27. Hays, R.M., Franki, N. 1970. The role of water diffusion in the action of vasopressin.J. Membrane Biol. 2:263–276

    Google Scholar 

  28. Hays, R.M., Leaf, A. 1962. Studies on the movement of water through the isolated toad bladder and its modification by vasopressin.J. Gen. Physiol. 45:905–919

    PubMed  Google Scholar 

  29. Hays, R.M., Singer, B., Malamed, S. 1965. The effect of calcium withdrawal on the structure and function of the toad bladder.J. Cell Biol. 25:195–208

    PubMed  Google Scholar 

  30. House, C.R. 1974. Water Transport in Cells and Tissues. Monograph of the Physiological Society, No. 24. H. Davson, A.D.M. Greenfield, R. Whittam, and G.S. Brindley, editors. Edward Arnold, London

    Google Scholar 

  31. Humes, H.D., Simmons, C.F., Brenner, B.M. 1980. Effect of verapamil on the hydroosmotic response to antidiuretic hormone in toad urinary bladder.Am. J. Physiol. 239 (Renal Fluid Electrolyte Physiol. 8):F250-F257

    PubMed  Google Scholar 

  32. Jard, S., Bockaert, J. 1975. Stimulus-response coupling in neurohypophyseal peptide target cells.Physiol. Rev. 55:489–536

    PubMed  Google Scholar 

  33. Levine, S.D., Kachadorian, W.A., Levin, D.N., Schlodorff, D. 1981. Effects of trifluoropeazine on function and structure of toad urinary bladder: The role of calmodulin in vasopressinstimulation of water permeability.J. Clin. Invest. 67:662–672

    PubMed  Google Scholar 

  34. Lipman, K.M., Dodelson, R., Hays, R.M. 1966. The surface charge of isolated toad bladder epithelial cells.J. Gen. Physiol. 49:501–511

    PubMed  Google Scholar 

  35. Parisi, M., Piccini, Z.F. 1973. The penetration of water into the epithelium of toad urinary bladder and its modification by oxytocin.J. Membrane Biol. 12:227–246

    Google Scholar 

  36. Petersen, M.J., Edelman, I.S. 1964. Calcium inhibition of the action of vasopressin on the urinary bladder of the toad.J. Clin. Invest. 43:583–594

    PubMed  Google Scholar 

  37. Pietras, R.J., Naujokaitis, P.J., Szego, C.M. 1976. Differential effects of vasopressin on the water, calcium and lysosomal enzyme contents of mitochondria-rich and lysosome-rich (granular) epithelial cells isolated from bullfrog urinary bladder.Molec. Cell. Endocrinol. 4:89–106

    PubMed  Google Scholar 

  38. Rasmusussen, H., Goodman, D.B.P. 1977. Relationship between calcium and cyclic nucleotides in cell activations.Physsiol. Rev. 57:421–509

    Google Scholar 

  39. Robinson, R.A., Stokes, R.H. 1970. Electrolyte Solutions (2nd ed.) Butteworth & Company, London

    Google Scholar 

  40. Rose, B., Rick, R. 1978. Intracellular pH, intracellualar free Ca, and junctional cell-cell coupling.J. Membrane Biol. 44:377–415

    Google Scholar 

  41. Rosenberg, P.A., Finkelstein, A. 1978a. Interaction of ions and water in gramicidin A channels. Streaming potentials across lipid bilayer membranes.J. Gen. Physiol. 72:327–340

    PubMed  Google Scholar 

  42. Rosenberg, P.A., Finkelstein, A. 1978b. Water permeability of gramicidin A-treated lipid bilayer membranes.J. Gen. Physiol. 72:341–350

    PubMed  Google Scholar 

  43. Shimomura, O., Johnson, F.H. 1976. Calcium-triggered luminescence of the photoprotein aequorin.In: Calcium in Biological Systems. C.J. Duncan, editor. pp. 41–54. Cambridge University Press, London

    Google Scholar 

  44. Spray, D.C., Harris, A.L., Bennett, M.V.L. 1981. Gap juncetional conductance is a simple and sensitive function of intracellular pH.Science 211:712–714

    PubMed  Google Scholar 

  45. Taylor, A., Eich, E., Pearl, M., Brem, A. 1979. Role of cytosolic Ca++ and Na−Ca exchange in the action of vasopressin.In: Hormonal Control of Epithelial Transport. J. Bouguet, J. Chevalier, M. Rarisi, and P. Ripiche, editors. pp. 167–174. Inserm, Paris

    Google Scholar 

  46. Taylor, A., Mamelak, M., Reaven, E., Maffly, R. 1973. Vasopressin: Possible role of microtubules and microfilaments in its action.Science 181:347–350

    PubMed  Google Scholar 

  47. Wade, J.B. 1978. Membrane structural specialization of the toad urinary bladder revealed by the freeze-fracture technique: III. Location, structure and vasopressin dependence of intramembrane particle arrays.J. Membrane Biol..Special Issue:281–296

  48. Wietzerbin, J., Lange, Y., Gary-Bobo, C.M. 1974. Lanthanum inhibtion of the action of oxytocin on the water permeability of the frog urinary bladder: Effect on the serosal and the apical membrane.J. Membrane Biol. 17: 27–40

    Google Scholar 

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Authors and Affiliations

  1. Departments of Medicine (Division of Nephrology) and Pharmacology, University of Miami School of Medicine, 33101, Miami, Florida

    Marcos A. Hardy

  2. Departments of Physiology & Biophysics and Medicine, Nephrology Research and Training Center, University of Alabama in Birmingham, 35294, Birmingham, Alabama

    Donald R. DiBona

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  1. Marcos A. Hardy
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  2. Donald R. DiBona
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Hardy, M.A., DiBona, D.R. Extracellular Ca2+ and the effect of antidiuretic hormone on the water permeability of the toad urinary bladder: An example of flow-induced alteration of flow. J. Membrain Biol. 67, 27–44 (1982). https://doi.org/10.1007/BF01868645

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  • DOI: https://doi.org/10.1007/BF01868645

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