Skip to main content
SpringerLink
Log in

Pre-steady-state analysis of the turn-on and turn-off of water permeability in the kidney collecting tubule

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

Summary

Water transport across the mammalian collecting tubule is regulated by vasopressin-dependent water channel insertion into and retrieval from the cell apical membrane. The time course of osmotic water permeability (P f ) following addition and removal of vasopressin (VP) and 8-Br-cAMP was measured continuously by quantitative fluorescence microscopy using an impermeant fluorophore perfused in the lumen. Cortical collecting tubules were subjected to a 120 mOsm bath-to-lumen osmotic gradient at 37°C with 10–15 nl/min lumen perfusion and 10–20 ml/min bath exchange rate. With addition of VP (250 μU/ml), there was a 23±3 sec (sem,n=16) lag in whichP f did not change, followed by a rise inP f (initial rate 1.4±0.2×10−4 cm/sec2) to a maximum of 265±10×10−4 cm/sec. With addition of 8-Br-cAMP (0.01–1mm) there was an 11±2 sec lag. For [8-Br-cAMP]=0.01, 0.1 and 1mm, the initial rate ofP f increase following the lag was (units 10−4 cm/sec2): 1.1±0.1, 1.2±0.1 and 1.7±0.3. MaximumP f was (units 10−4 cm/sec): 64±4, 199±9 and 285±11. With removal of VP,P f decreased to baseline (12×10−4 cm/sec) with aT 1/2 of 18 min; removal of 0.1 and 1mm 8-Br-cAMP gaveT 1/2 of 4 and 8.5 min. These results demonstrate (i) a brief lag in theP f response, longer for stimulation by VP than by 8-Br-cAMP, representing the transient build-up of biochemical intermediates proximal to the water channel insertion step, (ii) similar initialdP f /dt (water channel insertion) over a wide range of [8-Br-cAMP] and steady-stateP f values, and (iii) more rapidP f decrease with removal of 8-Br-cAMP than with VP. These pre-steady-state results define the detailed kinetics of the turn-on and turn-off of tubuleP f and provide kinetic evidence that the rate-limiting step for turn-on ofP f is not the step at which VP regulates steady-stateP f . If water channel insertion is assumed to be the rate-limiting step in the turn-on ofP f , these results raise the possibility that water channels must be activated following insertion into the apical membrane.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Al-Zahid, G., Schafer, J. A., Troutman, S. L., Andreoli, T. E. 1977. Effect of antidiuretic hormone on water and solute permeation, and the activation energies for these processes, in mammalian cortical collecting tubules.J. Membrane Biol. 31:103–129

    Google Scholar 

  2. Ando, Y., Jacobson, H. R., Breyer, M. D. 1988. Phorbol myristate acetate, dioctanoylglycerol and phosophatidic acid inhibit the hydroosmotic effect of vasopressin on rabbit cortical collecting tubule.J. Clin. Invest. 80:590–593

    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. Brown, D., Grosso, A., DeSousa, R. C. 1983. Correlation between water flow and intramembrane particle aggregates in toad epidermis.Am. J. Physiol. 245:C334-C342

    Google Scholar 

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

    Google Scholar 

  6. Burg, M., Grantham, J., Abramow, M., Orloff, J. 1966. Preparation and study of fragments of single rabbit nephrons.Am. J. Physiol. 210:1293–1298

    Google Scholar 

  7. Cassel, D., Eckstein, F., Lowe, M., Selinger, Z. 1979. Determination of the turn-off reaction for the hormone-activated adenylate cyclase.J. Biol. Chem. 254:9835–9838

    Google Scholar 

  8. Fine, L. G., Schlondorff, D., Trizna, W., Gilbert, R. M., Bricker, N. S. 1978. Functional profile of the isolated uremic nephron. Impaired water permeability and adenylate cyclase responsiveness of the cortical collecting tubule to vasopressin.J. Clin. Invest. 61:1519–1527

    Google Scholar 

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

    Google Scholar 

  10. Hall, D. A., Grantham, J. J. 1980. Temperature effect on ADH response of isolated perfused rabbit collecting tubules.Am. J. Physiol. 239:F595-F601

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  14. Hays, R. M. 1983. Alteration of luminal membrane structure by antidiuretic hormone.Am. J. Physiol. 245:C289-C296

    Google Scholar 

  15. Hebert, S. C., Andreoli, T. E. 1980. Interactions of temperature and ADH on transport processes in cortical collecting tubules.Am. J. Physiol. 238:F470-F480

    Google Scholar 

  16. Jones, S. M., Frindt, G., Windhager, E. E. 1988. Effect of peritubular [Ca] or ionomycin on hydrosmotic response of CCTs to ADH or cAMP.Am. J. Physiol. 254:F240-F253

    Google Scholar 

  17. Kim, Y., Illsley, N. P., Verkman, A. S. 1988. Rapid fluorescence assay of glucose and neutral solute transport using an entrapped volume indicator.Anal. Biochem. 172:403–409

    Google Scholar 

  18. Kuwahara, M., Berry, C. A., Verkman, A. S. 1988. Rapid development of vasopressin-induced hydroosmosis in kidney collecting tubules measured by a new fluorescence technique.Biophys. J. 54:595–602

    Google Scholar 

  19. Kuwahara, M., Verkman, A. S. 1988. Direct fluorescence measurement of diffusion water permeability in the vasopressin-sensitive kidney collecting tubule.Biophys. J. 54:587–593

    Google Scholar 

  20. Kuwahara, M., Verkman, A. S. 1989. Transcellular water flow modulates water channel exocytosis and endocytosis in kidney collecting tubule.Kidney Int. 35:188 (Abstr.)

    Google Scholar 

  21. Levine, S. D., Levin, D. N., Schlondorff, D. 1983. Calcium flow-independent actions of calcium channel blockers in toad urinary bladder.Am. J. Physiol. 244:C243-C249

    Google Scholar 

  22. Levine, S. D., Kachadorian, W. A. 1981. Barriers to water flow in vasopressin-treated toad urinary bladder.J. Membrane Biol. 61:135–139

    Google Scholar 

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

    Google Scholar 

  24. 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. 85:83–93

    Google Scholar 

  25. Parisi, M., Ripoche, P., Prevost, G., Bourguet, J. 1981. Regulation by ADH and cellular osmolarity of water permeability in frog urinary bladder: A time course study.Ann. NY Acad. Sci. 372:144–163

    Google Scholar 

  26. Reif, M. C., Troutman, S. L., Schafer, J. A. 1984. Sustained response to vasopressin in isolated rat cortical collecting tubule.Kidney Int. 26:725–732

    Google Scholar 

  27. Roy, C., Ausiello, D. A. 1981. Characterization of (8-lysine) vasopressin binding sites on a pig kidney cell line (LLC-PK1): Evidence for hormone-induced receptor transition.J. Biol. Chem. 256:3415–3422

    Google Scholar 

  28. 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. 51:1264–1278

    Google Scholar 

  29. Schlondorff, D., Levine, S. D. 1985. Inhibition of vasopressin-stimulated water flow in toad bladder by phorbol myristate acetate and dioctanoylglycerol, and RHC-80267. Evidence for modulation of action of vasopressin by protein kinase C.J. Clin. Invest. 76:1071–1078

    Google Scholar 

  30. Schlondorff, D., Petty, E., Oates, J. A., Jacoby, M., Levine, S. D. 1987. Epoxygenase metabolites or arachidonic acid inhibit vasopressin response in toad bladder.Am. J. Physiol. 253:F464-F470

    Google Scholar 

  31. Strange, K., Willingham, M. C., Handler, J. S., Harris, H. W., Jr. 1988. Apical membrane endocytosis via coated pits is stimulated by removal of antidiuretic hormone from isolated, perfused rabbit cortical collecting tubule.J. Membrane Biol. 103:17–28

    Google Scholar 

  32. Verkman, A. S., Lencer, W., Brown, D., Ausiello, D. A. 1988. Endosomes from kidney collecting tubule cells contain the vasopressin-sensitive water channel.Nature (London) 333:268–269

    Google Scholar 

  33. Wade, J. B., Stetson, D. L., Lewis, S. A. 1981. AHD action: Evidence for a membrane shuttle hypothesis.Ann. NY Acad. Sci. 372:106–117

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine and Division of Nephrology, Cardiovascular Research Institute, University of California, 94143, San Francisco, California

    Michio Kuwahara & A. S. Verkman

Authors
  1. Michio Kuwahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. S. Verkman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuwahara, M., Verkman, A.S. Pre-steady-state analysis of the turn-on and turn-off of water permeability in the kidney collecting tubule. J. Membrain Biol. 110, 57–65 (1989). https://doi.org/10.1007/BF01870993

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01870993

Key Words

Search

Navigation