Skip to main content
Log in

A parallel path model forNecturus proximal tubule

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

Summary

A parallel path model based on the principles of nonequilibrium thermodynamics was developed for theNecturus proximal tubule. The cellular path was represented as a luminal membrane followed by an irreversible active NaCl transport system in the peritubular barrier. The shunt pathway was described as three “coarse” barriers in series: tight junction, lateral intercellular spaces, and basement membrane with connective tissue. Volume and solute flows were predicted by the model equations as a function of applied electric current. Variations of the model parameters revealed the quantitative importance of the shunt path properties and the relative insensitivity of epithelial transport to changes in most cell parameters. Circulation of electric current and solute within the epithelium were shown to significantly influence the bahavior of the tubule in the presence of an electric field. Values for all transport parameters of the shunt path and epithelium were calculated and compared with available experimental evidence. Volume flow and electric currents predicted by the model compared favorably with experimental observations.

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. Anagnostopoulos, T. 1971. Evidence for independent Na and Cl transport pathways inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 3

  2. Asterita, M. F. 1971. Electrophysiological estimate of relative thickness of peritubular interstitial space inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 5

  3. Barry, P. H., Diamond, J. M. 1971. A theory of ion permeation through membranes with fixed neutral sites. J. Membrane Biol.4:295

    Google Scholar 

  4. Barry, P. H., Hope, A. B. 1969. Electroosmosis in membranes: Effects of unstirred layers and transport numbers. I. Theory.Biophys. J. 9:700

    PubMed  Google Scholar 

  5. Bentzel, C. J. 1971. Proximal tubular structure-function relationship during volume expansion inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 9

  6. Bentzel, C. J., Anagnostopoulos, T., Pandit, H. 1970.Necturus kidney: Its response to effects of isotonic volume expansion.Amer. J. Physiol. 218:205

    PubMed  Google Scholar 

  7. Bentzel, C. J., Davies, M., Scott, W. N., Zatzman, M., Solomon, A. K. 1968. Osmotic volume flow in the proximal tubule ofNecturus kidney.J. Gen. Physiol. 51:517

    PubMed  Google Scholar 

  8. Bentzel, C. J., Parsa, B., Hare, D. K. 1969. Osmotic flow across proximal tubule ofNecturus: Correlation of physiologic and anatomic studies.Amer. J. Physiol. 217:570

    PubMed  Google Scholar 

  9. Bentzel, C. J., Spring, K. R., Hare, D., Paganelli, C. V. 1973. Analog computer simulation of active and passive NaCl fluxes inNecturus proximal tubule.Amer. J. Physiol. (In press)

  10. Bentzel, C. J., Tourville, D. R., Parsa, B. 1971. Bidirectional transport of horseradish peroxidase in proximal tubule ofNecturus kidney.J. Cell Biol. 48:197

    PubMed  Google Scholar 

  11. Boulpaep, E. L. 1967. Ion permeability of the peritubular and luminal membrane of the renal tubule cell.In: Symposium über Transport und Funktion intracellulär Elektrolyte. F. Krück, editor. p. 98. Urban and Schwanzenberg, Berlin

    Google Scholar 

  12. Boulpaep, E. L. 1971. Electrophysiological properties of the proximal tubule: Importance of cellular and intercellular pathways.In: Electrophysiology of Epithelial Cells. G. Giebisch, editor. p. 91 F. K. Schattauer Verlag, Stuttgart

    Google Scholar 

  13. Boulpaep, E. L. 1972. Permeability changes of the proximal tubule ofNecturus during saline loading.Amer. J. Physiol. 222:517

    PubMed  Google Scholar 

  14. Clarkson, T. W. 1967. The transport of salt and water across isolated rat ileum.J. Gen. Physiol. 50:695

    PubMed  Google Scholar 

  15. Claude, P. 1968. An Electron Microscopic Study of the Urinary Tubules ofNecturus Maculosus. Ph. D. Thesis. University of Pennsylvania, Philadelphia, Pa.

    Google Scholar 

  16. Diamond, J. M., Barry, P. H., Wright, E. M. 1971. The route of transepithelial ion permeation in the gall bladder.In: Electrophysiology of Epithelial Cells. G. Giebisch, editor. p. 23. F. K. Schattauer Verlag, Stuttgart

    Google Scholar 

  17. Diamond, J. M., Bossert, W. H. 1967. Standing-gradient osmotic flow.J. Gen. Physiol. 50:2061

    PubMed  Google Scholar 

  18. Frömter, E. F. 1972. The route of passive ion movement through the epithelium ofNecturus gall bladder.J. Membrane Biol. 8:259

    Google Scholar 

  19. Frömter, E. F., Diamond, J. M., 1972. Route of passive ion permeation in epithelia.Nature, New Biol. 235:9

    Google Scholar 

  20. Frömter, E. F., Müller, C. W., Wick, T. 1971. Permeability properties of proximal tubular epithelium of the rat kidney as studied with electrophysiological methods.In: Electrophysiology of Epithelial Cells. G. Giebisch, editor. p. 119. F. K. Schattauer Verlag, Stuttgart

    Google Scholar 

  21. Giebisch, G. 1969. Functional organization of proximal and distal tubular electrolyte transport.Nephron 6:260

    PubMed  Google Scholar 

  22. Grandchamp, A., Boulpaep, E. L. 1972. Effect of intraluminal pressure on proximal tubular sodium reabsorption. A shirinking drop micropuncture study.Yale J. Biol. Med. 45:275

    PubMed  Google Scholar 

  23. Grim, E., Sollner, K. 1957. The contributions of normal and anomalous osmosis to the osmotic effects arising across charged membranes with solutions of electrolytes.J. Gen. Physiol. 40:887

    PubMed  Google Scholar 

  24. Hoshiko, T., Lindley, B. D. 1967. Phenomenological description of active transport of salt and water.J. Gen. Physiol. 50:729

    PubMed  Google Scholar 

  25. Jacquez, J. A., Carnahan, B., Abbrecht, P., 1967. A model of the renal cortex and medulla.Math. Biosci. 1:227

    Google Scholar 

  26. Katchalsky, A. 1968. Thermodynamic treatment of membrane transport.Pure Appl. Chem. 16:229

    Google Scholar 

  27. Kedem, O., Katchalsky, A. 1961. A physical interpretation of the phenomenological coefficients of membrane permeability.J. Gen. Physiol. 45:143

    PubMed  Google Scholar 

  28. Kedem, O., Katchalsky, A. 1963. Permeability of composite membranes.Trans. Faraday Soc. 59:1918

    Google Scholar 

  29. Mandel, L. J., Curran, P. F. 1972. Responses of frog skin to steady-state voltag clamping.J. Gen. Physiol 59:503

    PubMed  Google Scholar 

  30. Oken, D. E., Whittembury, G., Windhager, E. E., Solomon, A. K. 1963. Single proximal tubules ofNecturus kidney. V. Unidirectional sodium movement.Amer. J. Physiol. 204:372

    PubMed  Google Scholar 

  31. Rose, R. C., Schultz, S. G. 1971. Studies on the electrical potential profile across rabbit ileum.J. Gen. Physiol. 57:639

    PubMed  Google Scholar 

  32. Smulders, A. P., Tormey, J. McD., Wright, E. M. 1972. The effect of osmotically induced water flows on the permeability and ultrastructure of the rabbit gallbladder.J. Membrane Biol. 7:164

    Google Scholar 

  33. Solomon, A. K. 1963. Single proximal tubules ofNecturus kidney. VII. Ion fluxes across individual faces of cell.Amer. J. Physiol. 204:381

    Google Scholar 

  34. Spring, K. R. 1973. Current-induced voltage transients inNecturus proximal tubule.J. Membrane Biol. 13:299

    Google Scholar 

  35. Spring, K. R., Paganelli, C. V. 1972. Sodium flux inNecturus proximal tubule under voltage clamp.J. Gen. Physiol. 60:181

    PubMed  Google Scholar 

  36. Tormey, J. M., Diamond, J. M. 1967. The ultrastructural route of fluid transport in rabbit gall bladder.J. Gen. Physiol. 50:2031

    PubMed  Google Scholar 

  37. Welling, L. W., Grantham, J. J. 1972. Physical properties of isolated perfused renal tubules and tubular basement membranes.J. Clin. Invest. 51:1063

    PubMed  Google Scholar 

  38. Whittembury, G. 1967. Sobre los mecanismos de absorción en el tubo proximal del riñón.Acta Cient. Venezolana Suppl. I.3:71

    Google Scholar 

  39. Whittembury, G., Oken, D. E., Windhager, E. E., Solomon, A. K. 1959. Single proximal tubules ofNecturus kidney. IV. Dependence of H2O movement on osmotic gradients.Amer. J. Physiol. 197:1121

    PubMed  Google Scholar 

  40. Whittembury, G., Sugino, N., Solomon, A. K. 1960. Effect of anti-diuretic hormone and calcium on the equivalent pore radius of kidney slices fromNecturus.Nature 187:699

    PubMed  Google Scholar 

  41. Whittembury, G., Sugino, N., Solomon A. K. 1961. Ionic permeability and electrical potential differences inNecturus kidney cells.J. Gen. Physiol. 44:689

    PubMed  Google Scholar 

  42. Windhager, E. E. 1968. Glomerulo-tubular balance of salt and water.Physiologist 2:103

    Google Scholar 

  43. Windhager, E. E., Boulpaep, E. L., Giebisch, G. 1967. Electrophysiological studies on single nephrons.In: Proceedings of the International Congress of Nephrology, Volume I: Physiology J. S. Handler, editor. p. 35. S. Karger, Basel

    Google Scholar 

  44. Windhager, E. E., Giebisch, G. 1965. Electrophysiology of the nephron.Physiol. Rev. 45:214

    PubMed  Google Scholar 

  45. Wright, E. M., Smulders, A. P., Tormey, J. McD. 1972. The role of the lateral intercellular spaces and solute polarization effects in the passive flow of water across the rabbit gallbladder.J. Membrane Biol. 7:198

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spring, K.R. A parallel path model forNecturus proximal tubule. J. Membrain Biol. 13, 323–352 (1973). https://doi.org/10.1007/BF01868235

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01868235

Keywords

Navigation