Skip to main content
Log in

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

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

The present studies were designed to assess the ways in which antidiuretic hormone (ADH) alters water and solute permeation across isolated, rabbit cortical collecting tubules. In earlier work, it was observed: that ADH produced a tenfold increment inP f (cm per sec), the osmotic water permeability coefficient, and a fourfold increment inP D w (cm per sec), the diffusional water permeability coefficient; that small hydrophilic solutes such as urea, thiourea and acetamide (each having oil/water partition coefficients≦0.0008) had vanishingly low permeation coefficients and unity reflection coefficients, even in the presence of ADH; that lumen to bath osmosis involved a transcellular route; and, that the disparity betweenP f andP D w, either with or without ADH, could be rationalized in terms of cellular diffusion constraints, i.e., that water transport across luminal membranes was diffusional.

The present experiments evaluated the effects of ADH on diffusion of moderately lipophilic solutes (e.g., butyramide, isobutyramide, and antipyrine, each solute having an oil/water partition≧0.0008) across luminal membranes of rabbit cortical collecting tubules, and the effects of ADH on the apparent activation energies (E A, kcal per moel) for water and solute permeation across these tubules. Three major results were obtained: (1) ADH produced a 60–100% increase in the permeation rates for these solutes. (2) The ADH-dependent apparentE A for water permeation was 9.35±0.92 kcal per mole, and the ADH-dependent apparentE A for permeation of moderately lipophilic solutes was in the range 15.8–19.6 kcal per mole. (3) The ADH-independentE A values for these transport processes were statistically indistinguishable from the ADH-dependentE A values.

When viewed in the context of transport mechanisms for water and solute permeation across synthetic lipid bilayer membrane systems, these results are consistent with the possibility that diffusion of water and moderately lipophilic solutes across mammalian collecting tubules may involve parallel sites in luminal plasma membranes: routes for water diffusion which are either aqueous and/or disorganized, particularly with respect to synthetic lipid bilayer lamellae; and, discrete hydrophobic regions for diffusion of moderately lipophilic solutes. ADH may act by increasing the number of both types of sites within luminal plasma membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Al-Zahid, G., Schafer, J.A., Andreoli, T.E. 1975. The effect of ADH on branched and straight chain lipophilic solute permeation in cortical collecting tubules.Physiologist 18:120

    Google Scholar 

  2. Andreoli, T.E., Dennis, V.W., Weigl, A.M. 1969. The effect of amphotericin B on the water and nonelectrolyte permeability of thin lipid membranes.J. Gen. Physiol. 53:133

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  4. Andreoli, T.E., Troutman, S.L. 1971. An analysis of unstirred layers in series with “tight” and “porous” lipid bilayer membranes.J. Gen. Physiol. 57:464

    Article  PubMed  CAS  Google Scholar 

  5. Burg, M., Grantham, J., Abramow, M., Orloff, J. 1966. Preparation and study of fragments of single rabbit nephrons.Am. J. Physiol. 210:1293

    PubMed  CAS  Google Scholar 

  6. Burg, M., Helman, S.L., Grantham, J., Orloff, J. 1970. Effect of vasopressin on the permeability of isolated rabbit cortical collecting tubules to urea, acetamide, and thiourea.In: Urea and the Kidney. B. Schmidt-Nielsen and D.W.S. Kerr, editors. pp. 193–199. Excerpta Medica, Amsterdam

    Google Scholar 

  7. Cass, A., Finkelstein, A. 1967. Water permeability of thin lipid membranes.J. Gen. Physiol. 50:1765

    Article  PubMed  CAS  Google Scholar 

  8. Cohen, B.E. 1975. The permeability of liposomes to nonelectrolytes. I. Activation energies for permeation.J. Membrane Biol. 20:205

    Article  CAS  Google Scholar 

  9. Collander, R. 1949. Die Verteilung organischer Verbindungen zwischen Äther und Wasser.Acta Chemica Scand. 3:717

    Article  CAS  Google Scholar 

  10. Collander, R., Bärlund, H. 1933. Permeabilitätsstudien an Chara Ceratophylla. II. Die Permeabilität für Nichtelectrolyte.Acta Bot. Fenn. 11:5

    Google Scholar 

  11. Finkelstein, A. 1974. Aqueous pores created in thin lipid membranes by the antibiotics nystatin, amphotericin B and gramicidin A: Implications for pores in biological membranes.In: Drugs and Transport Processes. B.A. Callinghan, editor. pp. 241–250. University Park Press, Baltimore

    Google Scholar 

  12. Gallucci, E., Micelli, S., Lippe, C. 1971. Non-electrolyte permeability across thin lipid membranes.Arch. Int. Physiol. Biochem. 79:881

    Article  CAS  Google Scholar 

  13. Ganote, C.E., Grantham, J.J., Moses, H.L., Burg, M.B., Orloff, J. 1968. Ultrastructural studies of vasopressin effect on isolated perfused renal collecting tubules of the rabbit.J. Cell. Biol. 36:355

    Article  PubMed  CAS  Google Scholar 

  14. Gier, J. de, Mandersloot, J.G., Hupkes, J.V., McElhaney, R.N., Beer, W.P. van. 1971. On the mechanism of non-electrolyte permeation through lipid bilayers and through biomembranes.Biochim. Biophys. Acta 233:610

    Article  PubMed  Google Scholar 

  15. Grantham, J.J., Burg, M.B. 1966. Effect of vasopressin and cyclic AMP on permeability of isolated collecting tubules.Am. J. Physiol. 211:255

    PubMed  CAS  Google Scholar 

  16. Grantham, J.J., Ganote, C.E., Burg, M.B., Orloff, J. 1969. Paths of transtubular water flow in isolated renal collecting tubules.J. Cell. Biol. 41:562

    Article  PubMed  CAS  Google Scholar 

  17. Graziani, Y., Livne, A. 1972. Water permeability of bilayer lipid membranes: Sterollipid interaction.J. Membrane Biol. 7:275

    Article  CAS  Google Scholar 

  18. Grigera, J.R., Cereijido, M. 1971. The state of water in the outer barrier of the isolated frog skin.J. Membrane Biol. 4:148

    Article  Google Scholar 

  19. Hanai, T., Haydon, D.A. 1966. The permeability to water of bimolecular lipid membranes.J. Theoret. Biol. 11:370

    Article  CAS  Google Scholar 

  20. Haydon, D.A., Hladky, S.B. 1972. Ion transport across thin lipid membranes: A critical discussion of mechanism in selected systems.Q. Rev. Biophys. 5:187

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. Hays, R.M., Franki, N., Soberman, R. 1971. Activation energy for water diffusion across the toad bladder: Evidence against the pore enalrgement hypothesis.J. Clin. Invest. 50:1016

    Article  PubMed  CAS  Google Scholar 

  23. 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

    Article  PubMed  CAS  Google Scholar 

  24. Helman, S.I. 1973. Microelectrode studies of isolated cortical collecting tubules.6th Annu. Meeting Amer. Soc. Neph. p. 49 (Abstr.)

  25. Helman, S.I., Grantham, J.J., Burg, M.B. 1971. Effect of vasopressin on electrical resistance of renal cortical collecting tubules.Am. J. Physiol. 220:1825

    PubMed  CAS  Google Scholar 

  26. Kruyff, B. de, Greef, W.J. de, Eyk, R.V.W. van, Demel, R.A., Deenen, L.L.M. van. 1973. The effect of different fatty acid and sterol composition on the erythritol flux through the cell membrane of Acholeplasma laidlawii.Biochim. Biophys. Acta 298:479

    Article  PubMed  Google Scholar 

  27. Levine, S.D., Franki, N., Einhorn, R., Hays, R.M. 1976. Vasopressin-stimulated movement of drugs and uric acid across the toad urinary bladder.Kidney Int. 9:30

    Article  PubMed  CAS  Google Scholar 

  28. Levine, Y.K., Wilkins, M.H.F. 1971. Structure of oriented lipid bilayers.Nature New Biol. 230:69

    PubMed  CAS  Google Scholar 

  29. Lippe, C. 1969. Urea and thiourea permeabilities of phospholipid and cholesterol bilayer membranes.J. Mol. Biol. 39:669

    Article  PubMed  CAS  Google Scholar 

  30. MacRobbie, E.A.C., Ussing, H.H. 1961. Osmotic behaviour of epithelial cells of frog skin.Acta Physiol. Scand. 53:348

    Article  PubMed  CAS  Google Scholar 

  31. Maffly, R.H., Hays, R.M., Lamdin, E., Leaf, A. 1960. The effect of neurohypophyseal hormones on the permeability of the toad bladder to urea.J. Clin. Invest. 39:630

    Article  PubMed  CAS  Google Scholar 

  32. Marsh, D., Smith, I.C.P. 1973. An interacting spin label study of the fluidizing and condensing effects of cholesterol on lecithin bilayers.Biochim. Biophys. Acta 298:133

    Article  PubMed  CAS  Google Scholar 

  33. McElhaney, R.N., Gier, J. de, Neut-kok, E.C.M. van der. 1973. The effect of alterations in fatty acid composition and cholesterol content on the nonelectrolyte permeability of Acholeplasma laidlawii B cells and derived liposomes.Biochim. Biophys. Acta 298:500

    Article  PubMed  CAS  Google Scholar 

  34. Pietras, R.J., Wright, E.M. 1974. Nonelectrolyte probes of membrane structure in ADH-treated toad urinary bladder.Nature (London).247:222

    Article  CAS  Google Scholar 

  35. Pietras, R.J., Wright, E.M. 1975. The membrane action of antidiuretic hormone (ADH) on toad urinary bladder.J. Membrane Biol. 22:107

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Poznansky, M., Tong, S., White, P.C., Milgram, J.M., Solomon, A.K. 1976. Nonelectrolyte diffusion across lipid bilayer systems.J. Gen. Physiol. 67:45

    Article  PubMed  CAS  Google Scholar 

  38. Price, H.D., Thompson, T.E. 1969. Properties of lipid bilayer membranes separating two aqueous phases: Temperature dependence of water permeability.J. Mol. Biol. 41:443

    Article  PubMed  CAS  Google Scholar 

  39. Redwood, W.R., Haydon, D.A. 1969. Influence of temperature and membrane composition on the water permeability of lipid bilayers.J. Theoret. Biol. 22:1

    Article  CAS  Google Scholar 

  40. Reeves, J.P., Dowben, R.M. 1970. Water permeability of phospholipid vesicles.J. Membrane Biol. 3:123

    Article  CAS  Google Scholar 

  41. Schafer, J.A., Andreoli, T.E. 1972. Cellular constraints to diffusion. The effect of antidiuretic hormone on water flows in isolated mammalian collecting tubules.J. Clin. Invest. 51:1264

    Article  PubMed  CAS  Google Scholar 

  42. Schafer, J.A., Andreoli, T.E. 1972. The effect of antidiuretic hormone on solute flows in isolated mammalian collecting tubules.J. Clin. Invest. 51:1279

    Article  PubMed  CAS  Google Scholar 

  43. Schafer, J.A., Patlak, C.S., Andreoli, T.E. 1974. Osmosis in cortical collecting tubules. A theoretical and experimental analysis of the osmotic transient phenomenon.J. Gen. Physiol. 64:201

    PubMed  CAS  Google Scholar 

  44. Schafer, J.A., Troutman, S.L., Andreoli, T.E. 1974. Osmosis in cortical collecting tubules. ADH-independent osmotic flow rectification.J. Gen. Physiol. 64:228

    Article  PubMed  CAS  Google Scholar 

  45. Schafer, J.A., Troutman, S.L., Andreoli, T.E. 1974. Volume reabsorption, transepithelial potential differences, and ionic permeability properties in mammalian superficial proximal straight tubules.J Gen. Physiol. 64:582

    Article  PubMed  CAS  Google Scholar 

  46. Schatzberg, P. 1963. Solubilities of water in several normal alkanes from C7 to C16.J. Phys. Chem. 67:776

    Article  CAS  Google Scholar 

  47. Schatzberg, P. 1965. Diffusion of water through hydrocarbon liquids.J. Polymer Sci. C. 10:87

    Article  Google Scholar 

  48. Stein, W.D. 1967. The Movement of Molecules Across Cell Membranes. pp. 65–125. Academic Press, New York

    Google Scholar 

  49. Träuble, H. 1971. The movement of molecules across lipid membranes: A molecular theory.J. Membrane Biol. 4:193

    Article  Google Scholar 

  50. Urry, D.W., Goodall, M.C., Glickson, J.D., Mayers, D.F., 1971. The gramicidin A transmembrane channel: Characteristics of head to head dimerizedII L,D helices.Proc. Nat. Acad. Sci. USA 68:1907

    Article  PubMed  CAS  Google Scholar 

  51. Van Os, C.H., Slegers, J.F.G. 1973. Path of osmotic water flow through rabbit gall bladder epithelium.Biochim. Biophys. Acta 291:197

    Article  PubMed  Google Scholar 

  52. Vieira, F.L., Scha'afi, R.I., Solomon, A.K. 1970. The state of water in human and dog red cell membranes.J. Gen. Physiol. 55:451

    Article  PubMed  CAS  Google Scholar 

  53. Vreeman, H.J. 1966. Permeability of thin phospholipid films.K. Ned. Akad. Wet. Proc. Ser. B. Phys. Sci. 69:542

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Al-Zahid, G., Schafer, J.A., Troutman, S.L. et al. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules. J. Membrain Biol. 31, 103–129 (1977). https://doi.org/10.1007/BF01869401

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869401

Keywords

Navigation