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Na+ transport by rabbit urinary bladder, a tight epithelium

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By in vitro experiments on rabbit bladder, we reassessed the traditional view that mammalian urinary bladder lacks ion transport mechanisms. Since the ratio of actual-to-nominal membrane area in folded epithelia is variable and hard to estimate, we normalized membrane properties to apical membrane capacitance rather than to nominal area (probably 1 μF ∼ 1 cm2 actual area). A new mounting technique that virtually eliminates edge damage yielded resistances up to 78,000 ΩμF for rabbit bladder, and resistances for amphibian skin and bladder much higher than those usually reported. This technique made it possible to observe a transport-related conductance pathway, and a close correlation between transepithelial conductance (G) and short-circuit current (I sc) in these tight epithelia.G andI sc were increased by mucosal (Na+) [I sc∼0 when (Na+)∼0], aldosterone, serosal (HCO 3 ) and high mucosal (H+); were decreased by amiloride, mucosal (Ca++), ouabain, metabolic inhibitors and serosal (H+); and were unaffected by (Cl) and little affected by antidiuretic hormone (ADH). Physiological variation in the rabbits' dietary Na+ intake caused variations in bladderG andI sc similar to those caused by the expectedin vivo changes in aldosterone levels. The relation betweenG andI sc was the same whether defined by diet changes, natural variation among individual rabbits, or most of the above agents. A method was developed for separately resolving conductances of junctions, basolateral cell membrane, and apical cell membrane from thisG−I sc relation. Net Na+ flux equalledI sc. Net Cl flux was zero on short circuit and equalled only 25% of net Na+ flux in open circuit. Bladder membrane fragments contained a Na+−K+-activated, ouabain-inhibited ATPase. The physiological significance of Na+ absorption against steep gradients in rabbit bladder may be to maintain kidney-generated ion gradients during bladder storage of urine, especially when the animal is Na+-depleted.

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References

  • Adelman, W.J., Moore, J.W. 1962. Action of external divalent ion reduction on sodium movement in the squid axon.J. Gen. Physiol. 45:93

    Google Scholar 

  • Baer, J.E., Jones, C.B., Spitzer, S.A., Russo, H.F. 1967. The potassium sparing and natriuretic activity of amiloride.J. Pharmacol. Exp. Ther. 157:472

    Google Scholar 

  • Bartter, F.G. 1956. The role of aldosterone in normal homeostasis and in certain disease states.Metabolism 5:369

    Google Scholar 

  • Bentley, P.J. 1968. Amiloride: A potent inhibitor of sodium transport across the toad bladder.J. Physiol. 195:317

    Google Scholar 

  • Bindslev, N., Tormey, J.McD., Pietras, R.J., Wright, E.M., 1974. Electrically and osmotically induced changes in permeability and structure of toad urinary bladder.Biochim. Biophys. Acta 332:286

    Google Scholar 

  • Bonting, S.L. 1970. Sodium-potassium activated adenosinetriphosphatase and cation transport.In: Membranes and Ion Transport. E.E. Bittar, editor. Vol. 1, p. 257. Wiley Interscience, London

    Google Scholar 

  • Borzelleca, J.F. 1965. Drug movement from the isolated urinary bladder of the rabbit.Arch. Int. Pharmacodyn. Ther. 154:40

    Google Scholar 

  • Burg, M.B., Orloff, J. 1973. Perfusion of isolated renal tubules. Chapter 7.In: Handbook of Physiology. Section 8: Renal Physiology. J. Orloff and W. Berliner, editors. p. 145. American Physiological Society, Washington, D.C.

    Google Scholar 

  • Civan, M.M., Hoffman, R.E. 1971. Effect of aldosterone on electrical resistance of toad bladder.Am. J. Physiol. 220:324

    Google Scholar 

  • Crabbé, J. 1972. Aldosterone: Mechanism of action on isolated sodium transporting epithelia.J. Steroid Biochem. 3:557

    Google Scholar 

  • Crabbé, J., Erlij, E.N. 1968. Amiloride and the mode of action of aldosterone on sodium transport across toad bladder and skin.Pfluegers Arch. 304:284

    Google Scholar 

  • Curran, P.F., Gill, J.R. 1962. The effect of calcium on sodium transport by frog skin.J. Gen. Physiol. 45:625

    Google Scholar 

  • Cuthbert, A.W., Painter, E. 1969a. The action of antidiuretic hormone on cell membranes. Voltage transient studies.Br. J. Pharmacol. 35:24

    Google Scholar 

  • Cuthbert, A.W., Painter, E. 1969b. Capacitance changes in frog skin caused by theophylline and antidiuretic hormone.Br. J. Pharmacol. 37:314

    Google Scholar 

  • Cuthbert, A.W., Wong, P.Y.D. 1971. The effect of metal ions and antidiuretic hormone on oxygen consumption in toad bladder.J. Physiol. 219:39

    Google Scholar 

  • Cuthbert, A.W., Wong, P.Y.D. 1972. The role of calcium ions in the interaction of amiloride with membrane receptors.Mol. Pharmacol. 8:222

    Google Scholar 

  • Diamond, J.M. 1964. Transport of salt and water in rabbit and guinea pig gallbladder.J. Gen. Physiol. 48:1

    Google Scholar 

  • Diamond, J.M., Wright, E.M. 1969. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Ann. Rev. Physiol. 31:581

    Google Scholar 

  • Dobsob, J.G., Jr., Kidder, G.W. III. 1968. Edge damage effect inin vitro frog skin preparations.Am. J. Physiol. 214:719

    Google Scholar 

  • Edelman, I.S., Fimognari, G.M. 1968. On the biochemical mechanism of action of aldosterone.Recent Prog. Horm. Res. 24:1

    Google Scholar 

  • Ehrlij, E.N., Crabbé, J. 1968. The mechanism of action of amipramizide.Pfluegers Arch. 302:79

    Google Scholar 

  • Englund, S.E. 1956. Observations on the migration of some labelled substances between the urinary bladder and the blood in rabbit. Review of the literature.Acta radiol. Suppl. 135:1

    Google Scholar 

  • Fellows, G.J., Marshall, D.H. 1972. The permeability of human bladder epithelium to water and sodium.Invest. Urol. 9:339

    Google Scholar 

  • Fellows, G.J., Turnbull, G.J. 1971. The permeability of mammalian urinary bladder epithelium.Rev. Eur. Etud. Clin. Biol. 16:303

    Google Scholar 

  • Fettiplace, R., Andrews, D.M., Haydon, D.A. 1971. The thickness, composition and structure of some lipid bilayers and natural membranes.J. Membrane Biol. 5:277

    Google Scholar 

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

    Google Scholar 

  • Fujita, M., Matsui, H., Nagano, K., Nakao, M. 1971. Asymmetric distribution of ouabain-sensitive ATPase activity in rat intestinal mucosa.Biochim. Biophys. Acta 233:404

    Google Scholar 

  • Giebisch, G., Windhager, E. 1973. Electrolyte transport across renal tubular membranes.

  • Chapter 11.In: Handbook of Physiology. Section 8: Renal Physiology. J. Orloff and W. Berliner, editors. p. 315. American Physiological Society, Washington, D.C.

  • Hakim, A.A., Lifson, N., Creevy, C.D. 1965. Fluxes of Na+ and Cl in the dog urinary bladder.Invest. Urol. 2:348

    Google Scholar 

  • Helman, S.I., Miller, D.A. 1971.In vitro techniques for avoiding edge damage in studies of frog skin.Science 173:146

    Google Scholar 

  • Higgins, J.T., Jr., Cesaro, L., Gebler, B., Frömter, E. 1975. Electrical properties of amphibian urinary bladder epithelia. 1. Inverse relationship between potential difference and resistance in tightly mounted preparations.Pfluegers Arch. 358:41

    Google Scholar 

  • Hlad, J.C., Nelson, R., Holmes, J.H. 1956. Transfer of electrolytes across the urinary bladder in the dog.Am. J. Physiol. 184:406

    Google Scholar 

  • Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. 108:37

    Google Scholar 

  • Knauf, H., Frömter, E. 1970. Studies on the origin of the transepithelial electrical potential difference in salivary duct epithelium. Electrophysiology of Epithelial Cells, Symposia. Medica Hocchst. G. Giebisch, editor. p. 187. Schattauer Verlag, Stuttgart

    Google Scholar 

  • Leaf, A. 1955. Ion transport by the isolated bladder of the toad.Proc. 3rd Int. Congr. Biochem., Brussels

  • Lewis, S.A., Clausen, C.J., Diamond, J.M. 1975. Conductance related transport phenomena of some tight epithelia.Physiologist 18:291

    Google Scholar 

  • Lewis, S.A., Diamond, J.M. 1974. Active ion transport across rabbit urinary bladder.Fed. Proc. (Abstr.) Vol. 33, no. 680

    Google Scholar 

  • Lewis, S.A., Diamond, J.M. 1975. Active sodium transport by mammalian urinary bladder.Nature 253:747

    Google Scholar 

  • Lewis, S.A., Eaton, D.C., Diamond, J.M. 1975. Location of transport-related conductance pathway in rabbit urinary bladder, a tight epithelium.Biophys. J. 15:232a

    Google Scholar 

  • Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41

    Google Scholar 

  • Martin, D.W., Murphy, B. 1974. Carbamyl phosphate and glutamine stimulation of the gallbladder salt pump.J. Membrane Biol. 18:231

    Google Scholar 

  • Moreno, J.H. 1974. Blockage of cation permeability across the tight junctions of gallbladder and other leaky epithelia.Nature 251:150

    Google Scholar 

  • Rapoport, A., Nicholson, T.F., Yendt, E.R. 1960. Movement of electrolytes across the wall of the urinary bladder in dogs.Am. J. Physiol. 198:191

    Google Scholar 

  • Richter, W.R., Moize, S.M. 1963. Electron microscopic observations on the collapsed and distended mammalian urinary bladder.J. Ultrastruct. Res. 9:1

    Google Scholar 

  • Rosenfeld, J.B., Aboulafia, E.D., Schwartz, W.B. 1963. Influence of non-ionic diffusion on absorption of NH +4 and HCO 3 from bladder.Am. J. Physiol. 204:568

    Google Scholar 

  • Saito, T., Essig, A. 1973. Effect of aldosterone on active and passive conductance andE Na in the toad bladder.J. Membrane Biol. 13:1

    Google Scholar 

  • Salako, L.A., Smith, A.J. 1970. Effects of amiloride on active sodium transport by the isolated frog skin: Evidence concerning site of action.Br. J. Pharmacol. 38:702

    Google Scholar 

  • Schoffeniels, E. 1955. Influence du pH sur le transport actif de sodium à travers de la peau de grenoeuille.Arch. Int. Physiol. Biochim. 58:513

    Google Scholar 

  • Sharp, G.W.G., Leaf, A. 1973. Effects of aldosterone and its mechanism of action on sodium transport.In: Handbook of Physiology, Section 8. Renal Physiology. R.W. Berliner and J. Orloff, editors, p. 815. American Physiological Society, Washington, D.C.

    Google Scholar 

  • Sherry, H.S. 1969. The ion exchange properties of zeolites.In: Ion Exchange. J.A. Marinsky, editor, Vol. 2, p. 89. Marcel Dekker, New York

    Google Scholar 

  • Smith, P.G. 1975. Aldosterone-induced moulting in amphibian skin and its effect on electrical capacitance.J. Membrane Biol. 22:165

    Google Scholar 

  • Teorell, T. 1946. Application of “square wave analysis” to bioelectric studies.Acta Physiol. Scand. 12:235

    Google Scholar 

  • Turnbull, G.J., Fellows, G.J. 1972. Permeability of the urinary bladder of the rabbit.Rev. Eur. Etud. Clin. Biol. 17:745

    Google Scholar 

  • Ussing, H.H., Erlij, D., Lassen, U. 1974. Transport pathways in biological membranes.Annu. Rev. Physiol. 36:17

    Google Scholar 

  • Ussing, H.H., Zerahn, K. 1951. Active transport of sodium as the source of electric current in the short circuited isolated frog skin.Acta Physiol. Scand. 23:110

    Google Scholar 

  • Walker, J.L., Eisenman, G., Sandblom, J.P. 1968. Electrical phenomena associated with the transport of ions and ion pairs in liquid ion exchange membranes.J. Phys. Chem. 72:978

    Google Scholar 

  • Walser, M. 1970. Role of edge damage in sodium permeability of toad bladder and means of avoiding it.Am. J. Physiol. 219:252

    Google Scholar 

  • Wheeler, H.O., Ross, E.D., King, K.K. 1969. Effect of carbonic anhydrase inhibitors on isolated rabbit gallbladders.Am. J. Physiol. 216:175

    Google Scholar 

  • Wickham, J.E.A. 1964. Active transport of sodium ion by the mammalian bladder epithelium.Invest. Urol. 2:145

    Google Scholar 

  • Wilczewski, T., Brodsky, W.A. 1975. Effects of ouabain and amiloride on Na pathways in turtle bladder.Am. J. Physiol. 228:781

    Google Scholar 

  • Wright, E.M., Diamond, J.M. 1968. Effects of pH and polyvalent cations on the selective permeability of gallbladder epithelium to monovalent ions.Biochim. Biophys. Acta 163:57

    Google Scholar 

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Lewis, S.A., Diamond, J.M. Na+ transport by rabbit urinary bladder, a tight epithelium. J. Membrain Biol. 28, 1–40 (1976). https://doi.org/10.1007/BF01869689

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