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.
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References
Anagnostopoulos, T. 1971. Evidence for independent Na and Cl transport pathways inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 3
Asterita, M. F. 1971. Electrophysiological estimate of relative thickness of peritubular interstitial space inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 5
Barry, P. H., Diamond, J. M. 1971. A theory of ion permeation through membranes with fixed neutral sites. J. Membrane Biol.4:295
Barry, P. H., Hope, A. B. 1969. Electroosmosis in membranes: Effects of unstirred layers and transport numbers. I. Theory.Biophys. J. 9:700
Bentzel, C. J. 1971. Proximal tubular structure-function relationship during volume expansion inNecturus kidney.Abst. Amer. Soc. Nephrol. p. 9
Bentzel, C. J., Anagnostopoulos, T., Pandit, H. 1970.Necturus kidney: Its response to effects of isotonic volume expansion.Amer. J. Physiol. 218:205
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
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
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)
Bentzel, C. J., Tourville, D. R., Parsa, B. 1971. Bidirectional transport of horseradish peroxidase in proximal tubule ofNecturus kidney.J. Cell Biol. 48:197
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
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
Boulpaep, E. L. 1972. Permeability changes of the proximal tubule ofNecturus during saline loading.Amer. J. Physiol. 222:517
Clarkson, T. W. 1967. The transport of salt and water across isolated rat ileum.J. Gen. Physiol. 50:695
Claude, P. 1968. An Electron Microscopic Study of the Urinary Tubules ofNecturus Maculosus. Ph. D. Thesis. University of Pennsylvania, Philadelphia, Pa.
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
Diamond, J. M., Bossert, W. H. 1967. Standing-gradient osmotic flow.J. Gen. Physiol. 50:2061
Frömter, E. F. 1972. The route of passive ion movement through the epithelium ofNecturus gall bladder.J. Membrane Biol. 8:259
Frömter, E. F., Diamond, J. M., 1972. Route of passive ion permeation in epithelia.Nature, New Biol. 235:9
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
Giebisch, G. 1969. Functional organization of proximal and distal tubular electrolyte transport.Nephron 6:260
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
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
Hoshiko, T., Lindley, B. D. 1967. Phenomenological description of active transport of salt and water.J. Gen. Physiol. 50:729
Jacquez, J. A., Carnahan, B., Abbrecht, P., 1967. A model of the renal cortex and medulla.Math. Biosci. 1:227
Katchalsky, A. 1968. Thermodynamic treatment of membrane transport.Pure Appl. Chem. 16:229
Kedem, O., Katchalsky, A. 1961. A physical interpretation of the phenomenological coefficients of membrane permeability.J. Gen. Physiol. 45:143
Kedem, O., Katchalsky, A. 1963. Permeability of composite membranes.Trans. Faraday Soc. 59:1918
Mandel, L. J., Curran, P. F. 1972. Responses of frog skin to steady-state voltag clamping.J. Gen. Physiol 59:503
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
Rose, R. C., Schultz, S. G. 1971. Studies on the electrical potential profile across rabbit ileum.J. Gen. Physiol. 57:639
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
Solomon, A. K. 1963. Single proximal tubules ofNecturus kidney. VII. Ion fluxes across individual faces of cell.Amer. J. Physiol. 204:381
Spring, K. R. 1973. Current-induced voltage transients inNecturus proximal tubule.J. Membrane Biol. 13:299
Spring, K. R., Paganelli, C. V. 1972. Sodium flux inNecturus proximal tubule under voltage clamp.J. Gen. Physiol. 60:181
Tormey, J. M., Diamond, J. M. 1967. The ultrastructural route of fluid transport in rabbit gall bladder.J. Gen. Physiol. 50:2031
Welling, L. W., Grantham, J. J. 1972. Physical properties of isolated perfused renal tubules and tubular basement membranes.J. Clin. Invest. 51:1063
Whittembury, G. 1967. Sobre los mecanismos de absorción en el tubo proximal del riñón.Acta Cient. Venezolana Suppl. I.3:71
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
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
Whittembury, G., Sugino, N., Solomon A. K. 1961. Ionic permeability and electrical potential differences inNecturus kidney cells.J. Gen. Physiol. 44:689
Windhager, E. E. 1968. Glomerulo-tubular balance of salt and water.Physiologist 2:103
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
Windhager, E. E., Giebisch, G. 1965. Electrophysiology of the nephron.Physiol. Rev. 45:214
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
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Spring, K.R. A parallel path model forNecturus proximal tubule. J. Membrain Biol. 13, 323–352 (1973). https://doi.org/10.1007/BF01868235
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DOI: https://doi.org/10.1007/BF01868235