Summary
Ouabain abolishes the short-circuit current (I sc ) and decreases the transepithelial conductance (G t ) of rabbit colon. In contrast, amphotericin B elicits a maximumI sc and markedly increasesG t . However, inboth instances the amiloride-sensitive Na entry step is completely blocked, presumably due to an increase in cell Na. Conversely, when Na-depleted tissues are suddenly exposed to 140mm Na, the amiloride-sensitiveI sc and the amiloride-sensitive component ofG t ( a G Na ) increase abruptly to their maximum values and the decline to steady-state plateaus with a half time of ∼ 6 min; throughout the decline (I sc/a G Na)=E Na is constant at a value of 95 mV. In the presence of amphotericin B, theI sc abruptly rises to the same maximum but does not decline. These findings indicate that in the presence of 140mm Na the conductance of the amiloride-sensitive Na entry step can vary from a maximum value of approximately 1.6 mmhos/cm2 when cell Na is depleted, to zero when cell Na is abnormally elevated (e.g., in the presence of ouabain or amphotericin B). Our findings are consistent with a system in which the pathway responsible for transcellular Na transport parallels another cellular compartment with which it communicates. The Na capacity of the active transport pathway appears to be very small so that this compartment fills rapidly after exposure of Na-depleted cells to 140mm Na, and active transepithelial Na transport is initiated and reaches steady-state levels quickly. The Na capacity of the second compartment is much larger; the Na content of this compartment appears to be responsible for the negative feedback effect on the permeability of the amiloride-sensitive entry step.
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References
Bentley, P.J. 1968. Amiloride: A potent inhibitor of sodium transport across the toad bladder.J. Physiol. (London) 195:317
Biber, T.U.L. 1971. Effect of changes in transepithelial transport on the uptake of sodium across the outer surface of the frog skin.J. Gen. Physiol. 58:131
Cereijido, M., Rabito, C.A., Boulan Rodriquez, E., Rotunno, C.A. 1974. The sodiumtransporting compartment of the epithelium of frog skin.J. Physiol. (London) 237:555
Chen, J.S., Walser, M. 1975. Sodium fluxes through the active transport pathway in toad bladder.J. Membrane Biol. 21:87
Cuthbert, A.W., Shum, W.K. 1977. Does intracellular sodium modify membrane permeability to sodium ions?Nature (London) 266:468
Dahl, J.L., Hokin, L.E. 1974. The sodium-potassium adenosinetriphosphatase.Annu. Rev. Biochem. 43:327
Dörge, A., Nagel, W. 1970. Effect of amiloride on sodium transport in frog skin. II. Sodium transport pool and unidirectional fluxes.Pfluegers Arch. 321:91
Dunham, P.B., Hoffman, J.F. 1971. Active cation transport and ouabain binding in high potassium and low potassium red blood cells of sheep.J. Gen. Physiol. 58:94
Ehrlich, E.N., Crabbé, J. 1968. The mechanism of action of amipramizide.Pfluegers Arch. 321:91
Erlij, D., Smith, M.W. 1973. Sodium uptake by frog skin and its modification by inhibitors of transepithelial sodium transport.J. Physiol. (London) 228:221
Essig, A., Leaf, A. 1963. The role of potassium in active transport of sodium by the toad bladder.J. Gen. Physiol. 46:505
Finkelstein, A., Holz, R. 1973. Aqueous pores created in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B.In: Membranes—A Series of Advances. Vol.2, p. 377. G. Eisenman, editor. Marcel Dekker, New York
Finn, A.L. 1974. Transepithelial potential difference in toad urinary bladder is not due to ionic diffusion.Nature (London) 250:495
Finn, A.L. 1975. The action of ouabain on sodium transport in toad urinary bladder. Evidence for two pathways for sodium entry.J. Gen. Physiol. 65:503
Frizzell, R.A., Jennings, B. 1977. Potassium influx across basolateral membranes of rabbit colon: Relation to sodium absorption.Fed. Proc. 36:360
Frizzell, R.A., Koch, M.J., Cooper, D.H., Schultz, S.G. 1975. Ion transport by rabbit colon: Effect of amiloride.Fed. Proc. 34:285
Frizzell, R.A., Koch, M.J., Schultz, S.G. 1976. Ion transport by rabbit colon. I. Active and passive components.J. Membrane Biol. 27:297
Frizzell, R.A., Schultz, S.G. 1972. Ionic conductances of extracellular shunt pathway in rabbit ileum. Influence of shunt on transmural sodium transport and electrical potential differences.J. Gen. Physiol. 59:318
Frizzell, R.A., Schultz, S.G. 1976. Ion transport by rabbit colon: Effect of amphotericin B.Fed. Proc. 35:602
Frizzell, R.A., Schultz, S.G. 1978. Effect of aldosterone on ion transport by rabbit colonin vitro.J. Membrane Biol. 39:1
Glynn, I.M., Karlish, S.J.D. 1975. The sodium pump.Annu. Rev. Physiol. 37: 13
Helman, S.I., Nagel, W. 1977. Microelectrode studies of frog skin: Effects of ouabain.Fed. Proc. 36: 632
Hong, C.D., Essig, A. 1976. Effects of 2-deoxy-d-glucose, amiloride, vasopressin, and ouabain on active conductance andE Na in the toad bladder.J. Membrane Biol. 28:121
Joiner, C.H., Lauf, P.K. 1977. Relationship between K pump flux (i M P K ) and3H-ouabain binding rate (OBR) in human and sheep red cells.Fed. Proc. 36:653
Koefoed-Johnsen, V., Ussing, H. H. 1958. The nature of the frog skin potential.Acta Physiol. Scand. 42:298
Larsen, E.H. 1973. Effect of amiloride, cyanide and ouabain on the active transport pathway in toad skin.In: Transport Mechanisms in Epithelia. H.H. Ussing and N.A. Thorn, editors, p. 131. Copenhagen, Munksgaard
Leb, D.E., Edwards, C., Lindley, B., Hoshiko, T. 1965. Interaction between the effects of inside and outside Na and K on bullfrog skin potential.J. Gen. Physiol. 49:309
Leblanc, G., Morel, F. 1975. Na and K movements across the membranes of frog skin associated with transient current changes.Pfluegers Arch. 358:159
Lewis, S.A., Eaton, D.C., Clausen, C.J., Diamond, J.M. 1977. Nystatin as a probe for investigating the electrical properties of a tight epithelium.J. Gen. Physiol. (in press)
Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41
Macknight, A.D.C., Civan, M.M., Leaf, A. 1975a. Some effects of ouabain on cellular ions and water in epithelial cells of toad urinary bladder.J. Membrane Biol. 20:387
Macknight, A.D.C., Civan, M.M., Leaf, A. 1975b. The sodium transport pool in toad urinary bladder epithelial cells.J. Membrane Biol. 20:365
MacRobbie, E.A.C., Ussing, H.H. 1961. Osmotic behavior of the epithelial cells of frog skin,Acta Physiol. Scand. 53:348
Morel, F., Leblanc, G. 1975. Transient current changes and Na compartmentalization in frog skin epithelium.Pfluegers Arch. 358:135
Moreno, J.H., Reisin, I.L., Rodriguez Boulan, E., Rotunna, C.A., Cereijido, M. 1973. Barriers to sodium movement across frog skin.J. Membrane Biol. 11:99
Nagel, W., Dörge, A. 1970. Effect of amiloride on sodium transport of frog skin. I. Action on intracellular sodium content.Pfluegers Arch. 317:84
Rick, R., Dörge, A., Nagel, W. 1975. Influx and efflux of sodium at the outer surface of frog skin.J. Membrane Biol. 22:183
Robinson, B.A., Macknight, A.D.C. 1976. Relationships between serosal medium potassium concentration and sodium transport in toad urinary bladder. II. Effects of different medium potassium concentrations on epithelial cell composition.J. Membrane Biol. 26:239
Schultz, S.G., Curran, P.F., Chez, R.A., Fuisz, R.E. 1967. Alanine and sodium fluxes across the mucosal border of rabbit ileum.J. Gen. Physiol. 50:1241
Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1977. Active sodium transport and the electrophysiology of rabbit colon.J. Membrane Biol. 33:351
Schultz, S.G., Zalusky, R. 1964. Ion transport in rabbit ileum. I. Short-circuit current and Na fluxes.J. Gen. Physiol. 47:567
Snell, F.M., Chowdhury, T.K. 1965. Contralateral effects of sodium and potassium on the electrical potential in frog skin and toad bladder.Nature (London) 207:45
Turnheim, K., Frizzell, R.A., Schultz, S.G. 1977. Effect of anions on amiloride-sensitive, active sodium transport across rabbit colon,in vitro: Evidence for “trans-inhibition of the Na entry mechanism”.J. Membrane Biol. 37:63
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
Whittam, R., Chipperfield, A.R. 1975. The reaction mechanism of the sodium pump.Biochim. Biophys. Acta. 415:149
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Turnheim, K., Frizzell, R.A. & Schultz, S.G. Interaction between cell sodium and the amiloride-sensitive sodium entry step in rabbit colon. J. Membrain Biol. 39, 233–256 (1978). https://doi.org/10.1007/BF01870333
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DOI: https://doi.org/10.1007/BF01870333