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Relationships among sodium current, permeability, and Na activities in control and glucocorticoid-stimulated rabbit descending colon

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Effects of a potent synthetic glucocorticoid, methylprednisolone (MP), on transepithelial Na transport were examined in rabbit descending colon. Current-voltage (I–V) relations of the amiloride-sensitive apical Na entry pathway were measured in colonic tissues of control and MP-treated (40 mg im for 2 days) animals. Tissues were bathed mucosally by solutions of various Na activities, (Na)m, ranging from 6.2 to 75.6mm, and serosally by a high K solution. TheseI–V relations conformed to the “constant field” flux equation permitting determination of the permeability of the apical membrane to Na,P mNa , and the intracellular Na activity, (Na)c. The following empirical relations were observed for both control and MP-treated tissues: (i) Na transport increases hyperbolically with increasing (Na)m obeying simple Michaelis-Mentin kinetics; (ii)P mNa decreased hyperbolically with increasing (Na)m, but was unrelated to individual variations in (Na)c; (iii) (Na)c increased hyperbolically with (Na)m; (iv) both spontaneous and steroid-stimulated variations in Na entry rate could be attributed entirely to parallel variations inP mNa at each mucosal Na activity. Comparison of these empirical, kinetic relations between control and MP-treated tissues revealed: (i) maximal Na current andP mNa were greater in MP tissues, but the (Na)m's at which current andP mNa were half-maximal were markedly reduced; (ii) (Na)c was significantly increased in MP tissues at each (Na)m while the (Na)m at half-maximal (Na)c was unchanged. These results provide direct evidence that glucocorticoids cause marked stimulation of Na absorption across rabbit colon primarily by increasing the Na permeability of the apical membrane. While the mechanism for the increased permeability remains to be determined, the altered relation betweenP mNa and (Na)m suggests possible differences in the conformation or environment of the Na channel in MP-treated tissues.

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References

  • Bastl, C.P., Barnett, C.A., Schmidt, T.J., Litwack, G. 1984. Glucocorticoid stimulation of sodium absorption in colonic epithelia is mediated by corticosteroid IB receptor.J. Biol. Chem. 259:1186–1195

    PubMed  Google Scholar 

  • Bastl, C.P., Binder, H.J., Hayslett, J.P. 1980. Role of glucocorticoids and aldosterone in maintenance of colonic cation transport.Am. J. Physiol. 238:F181-F186

    PubMed  Google Scholar 

  • Charney, A.N., Kinsey, M.D., Meyers, L., Gianella, R.A., Gots, R.E. 1975. Na−K-activated adenosine triphosphatase and intestinal electrolyte transport: Effect of adrenal steroids.J. Clin. Invest. 56:653–660

    PubMed  Google Scholar 

  • Charney, A.N., Wallach, J., Ceccarelli, S., Donowitz, M., Costenbader, C.L. 1981. Effects of spironolactone and amiloride on corticosteroid-induced changes in colonic function.Am. J. Physiol. 241:G300-G305

    PubMed  Google Scholar 

  • Clauss, W., Durr, J., Skadhauge, E., Hornicke, H. 1985. Effects of aldosterone and dexamethasone on apical membrane properties and Na-transport of rabbit distal colon in vitro.Pfluegers Arch. 403:186–192

    Google Scholar 

  • Cuthbert, A.W., Edwardson, J.M., Bindsley, N., Skadhauge, E. 1982. Identification of potential components of the transport mechanism for Na+ in the hen colon and coprodaeum.Pfluegers Arch. Gesamte Physiol. 392:347–351

    Google Scholar 

  • Davis, C.W., Finn, A.L. 1982. Sodium transport inhibition by amiloride reduces basolateral membrane potassium conductance in tight epithelia.Science 216:525–527

    PubMed  Google Scholar 

  • DeLong, J., Civan, M.M. 1984. Apical sodium entry in split frog skin: Current-voltage relationship.J. Membrane Biol. 82:25–40

    Google Scholar 

  • Eaton, D.C. 1981. Intracellular sodium ion activity and sodium transport in rabbit urinary bladder.J. Physiol. (London) 316:527–544

    Google Scholar 

  • Eaton, D.C., Frace, A.M., Silverthorn, S.U. 1982. Active and passive Na+ fluxes across the basolateral membrane of rabbit urinary bladder.J. Membrane Biol. 67:219–229

    Google Scholar 

  • Frizzell, R.A., Koch, M.J., Schultz, S.G. 1976. Ion transport by rabbit colon: I. Active and passive components.J. Membrane Biol. 27:297–316

    Google Scholar 

  • Frizzell, R.A., Schultz, S.G. 1978. Effect of aldosterone on ion transport by rabbit colonin vitro.J. Membrane Biol. 39:1–26

    Google Scholar 

  • Fuchs, W., Larsen, E.H., Lindemann, B. 1977. Current-voltage curve of sodium channels and concentration dependence of sodium permeability in frog skin.J. Physiol. (London) 267:137–166

    Google Scholar 

  • Garty, H., Edelman, I.S. 1983. Amiloride-sensitive trypsinization of apical sodium channels. Analysis of hormonal regulation of sodium transport in toad bladder.J. Gen. Physiol. 81:785–803

    PubMed  Google Scholar 

  • Goldman, D. 1943. Potential, impedance and rectification in membranes.J. Gen. Physiol. 27:37–60

    Article  Google Scholar 

  • Halm, D.R., Dawson, D.C. 1983. Cation activation of the basolateral sodium-potassium pump in turtle colon.J. Gen. Physiol. 82:315–329

    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. (London) 108:37–77

    Google Scholar 

  • Hudson, R.L., Schultz, S.G. 1984. Sodium-coupled sugar transport: Effects on intracellular sodium activities and sodiumpump activity.Science 224:1237–1239

    Google Scholar 

  • Klemperer, G., Garcia-Diaz, J.F., Essig, A. 1984. Effects of high serosal K concentrations on electrophysiological parameters of frog skin.J. Gen. Physiol. 84:29a

    Google Scholar 

  • Lewis, S.A. 1983. Control of Na+ and water absorption across vertebrate “tight” epithelia by ADH and aldosterone.J. Exp. Biol. 106:9–24

    PubMed  Google Scholar 

  • Lewis, S.A., DeMoura, J.L.C. 1984. Incorporation of cytoplasmic vesicles into apical membrane of mammalian urinary bladder.Nature (London) 297:685–688

    Google Scholar 

  • Lewis, S.A., Eaton, D.C., Diamond, J.M. 1976. The mechanism, of Na+ transport by rabbit urinary bladder.J. Membrane Biol. 28:41–70

    Google Scholar 

  • Lewis, S.A., Hanrahan, J.W., Van Driessche, W. 1984. Channels across epithelial cell layers.In: Current Topics in Membranes and Transport, W.D. Stein, editor. Vol. 21, pp. 253–293 Academic, New York

    Google Scholar 

  • Lewis, S.A., Wills, N.K. 1983. Apical membrane permeability and kinetic properties of the sodium pump in rabbit urinary bladder.J. Physiol. (London) 341:169–184

    Google Scholar 

  • Lewis, S.A., Wills, N.K., Eaton, D.C. 1978. Basolateral membrane potential of a tight epithelium: Ionic diffusion and electrogenic pumps.J. Membrane Biol. 41:117–148

    Google Scholar 

  • Loo, D.D.F., Lewis, S.A., Ifshin, M.S., Diamond, J.M. 1983. Turnover membrane insertion and degradation of sodium channels in rabbit urinary bladder.Science 221:1288–1290

    PubMed  Google Scholar 

  • Marver, D. 1984. Assessment of mineralocorticoid activity in the rabbit colon.Am. J. Physiol. 246:F437-F446

    PubMed  Google Scholar 

  • Nagel, W. 1977. Effect of high K upon the frog skin intracellular potential.Pfluegers Arch. 369:R22

    Google Scholar 

  • Nagel, W., Garcia-Diaz, J.F., Essig, A. 1983. Contribution of junctional conductance to the cellular voltage-divider ratio in frog skins.Pfluegers Arch. 399:336–341

    Google Scholar 

  • Nielsen, R. 1979. Coupled transepithelial sodium and potassium transport across isolated frog skin: Effect of oubain, amiloride, and the polyene antibiotic filipin.J. Membrane Biol. 51:161–184

    Google Scholar 

  • O'Neil, R.G. 1986. Adrenal steroid regulation of potassium transport.In: Potassium: Physiology and Pathophysiology. G. Giebisch, editor. Academic, New York (in press)

    Google Scholar 

  • O'Neil, R.G., Hayhurst, R.A. 1985. Sodium-dependent modulation of the renal Na−K-ATPase: Influence of mineralocorticoids on the cortical collecting duct.J. Membrane Biol. 85:169–179

    Google Scholar 

  • Palmer, L.G. 1984. Use of potassium depolarization to study apical transport properties in epithelia.In: Current Topics in Membranes and Transport. J.B. Wade and S.A. Lewis, editors. Vol. 20, pp. 105–121. Academic, New York

    Google Scholar 

  • Palmer, L.G. 1985. Modulation of apical Na permeability of the toad urinary bladder by intracellular Na, Ca and H.J. Membrane Biol. 83:57–69

    Google Scholar 

  • Palmer, L.G., Edelman, I.S. 1981. Control of apical sodium permeability in the toad urinary bladder by aldosterone.Ann. N.Y. Acad. Sci. 372:1–14

    Google Scholar 

  • Palmer, L.G., Edelman, I.S., Lindemann, B. 1980. Current-voltage analysis of apical sodium transport in toad urinary bladder: Effects of inhibitors of transport and metabolism.J. Membrane Biol. 57:59–71

    Google Scholar 

  • Palmer, L.G., Li, J.H.-Y., Lindemann, B., Edelman, I. 1982. Aldosterone control of the density of sodium channels in the toad urinary bladder.J. Membrane Biol. 64:91–102

    Google Scholar 

  • Petty, K.J., Kokko, J.P., Marver, D. 1981. Secondary effect of aldosterone on Na−K ATPase activity in the rabbit cortical collecting tubule.J. Clin. Invest. 68:1514–1521

    Google Scholar 

  • Reuss, L., Lewis, S.A., Wills, N.K., Helman, S.I., Cox, T.C., Boron, W.F., Siebens, A.W., Guggino, W.B., Giebisch, G., Schultz, S.G. 1984. Ion transport processes in basolateral membranes of epithelia.Fed. Proc. 43:2488–2502

    PubMed  Google Scholar 

  • Sansom, S.C., O'Neil, R.G. 1985. Mineralocorticoid regulation of apical cell membrane Na+ and K+ transport of the cortical collecting duct.Am. J. Physiol. 248:F858-F868

    Google Scholar 

  • Sansom, S.C., O'Neil, R.G. 1986. Effects of mineralocorticoids on active and passive transport properties of the basolateral membrane of the cortical collecting duct.Am. J. Physiol. (in Press)

  • Schultz, S.G. 1985. Regulatory mechanisms in sodium-absorbing epithelia.In: The Kidney: Physiology and Pathophysiology. D.W. Seldin and G. Giebisch, editors. Ch. 10, pp. 189–198 Raven, New York.

    Google Scholar 

  • Segel, I.H. 1975. Enzyme Kinetics. John Wiley & Sons, New York

    Google Scholar 

  • Sellin, J.H., Desoigne, R.C. 1983. Methylprednisolone increases absorptive capacity in rabbit ileumin vitro.Am. J. Physiol. 245:G562-G567

    PubMed  Google Scholar 

  • Sellin, J.H., Desoigne, R.C. 1985. Steroids alter ion transport and absorptive capacity in proximal and distal colon.Am. J. Physiol. 249:G113-G119

    PubMed  Google Scholar 

  • Tang, J., Abramcheck, F.J., VanDrissche, W., Helman, S.I. 1985. Electrophysiology and noise analysis of K+-depolarized epithelia of frog skin.Am. J. Physiol. 249:C421-C429

    PubMed  Google Scholar 

  • Taylor, A. 1981. Role of cytosolic calcium and sodium-calcium exchange in regulation of transepithelial sodium and water absorption.In: Ion Transport by Epithelia. S.G. Schultz, editor. pp. 233–259. Raven, New York

    Google Scholar 

  • Thomas, S.R., Suzuki, Y., Thompson, S.M., Schultz, S.G. 1983. Electrophysiology ofNecturus urinary bladder: I. “Instantaneous” current-voltage relations in the presence of varying mucosal sodium concentrations.J. Membrane Biol. 73:157–175

    Article  Google Scholar 

  • Thompson, S.M. 1986a. Relations between chord and slope conductances and equivalent electromotive forces.Am. J. Physiol. 250:C333-C339

    PubMed  Google Scholar 

  • Thompson, S.M. 1986b. Differential effects of amiloride on aldosterone and methylprednisolone (MP) stimulation of sodium permeability in rabbit distal colon.Fed. Proc. (in press)

  • Thompson, S.M., Sellin, J.H. 1984. Effects of methylprednisolone on Na transport in rabbit colon.Fed. Proc. 43:1086

    Google Scholar 

  • Thompson, S.M., Suzuki, Y., Schultz, S.G. 1982a. The electrophysiology of rabbit descending colon: I. Instantaneous transepithelial current-voltage relations and the current-voltage relations of the Na-entry mechanism.J. Membrane Biol. 66:41–54

    Article  Google Scholar 

  • Thompson, S.M., Suzuki, Y., Schultz, S.G. 1982b. The electrophysiology of rabbit descending colon: II. Current-voltage relations of the apical membrane, the basolateral membrane, and the parallel pathways.J. Membrane Biol. 66:55–61

    Article  Google Scholar 

  • Turnheim, K., Frizzell, R.A., Schultz, S.G. 1978. Interaction between cell sodium and the amiloride-sensitive sodium entry step in rabbit colon.J. Membrane Biol. 39:233–256

    Google Scholar 

  • Turnheim, K., Hudson, R.L., Schultz, S.G. 1986. Effect of Na deprivation on intracellular Na activity in descending rabbit colon.Biochim. Biophys. Acta (submitted)

  • Turnheim, K., Thompson, S.M., Schultz, S.G. 1983. Relation between intracellular sodium and active sodium transport in rabbit colon: Current-voltage relations of the apical sodium entry mechanisms in the presence of varying luminal sodium concentrations.J. Membrane Biol. 76:299–309

    Article  Google Scholar 

  • Van Driessche, W., Lindemann, B. 1979. Concentration dependence of currents through single sodium-selective pores in frog skin.Nature (London) 282:519–520

    Google Scholar 

  • Will, P.C., DeLisle, R.C., Cortright, R.N., Hopfer, U. 1981. Induction of amiloride-sensitive sodium transport in the intestines by adrenal steroids.Ann. N.Y. Acad. Sci. 372:64–76

    PubMed  Google Scholar 

  • Wills, N.K., Lewis, S.A., Eaton, D.C. 1979. Active and passive properties of rabbit descending colon: A microelectrode and nystatin study.J. Membrane Biol. 45:81–108

    Google Scholar 

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Thompson, S.M., Sellin, J.H. Relationships among sodium current, permeability, and Na activities in control and glucocorticoid-stimulated rabbit descending colon. J. Membrain Biol. 92, 121–134 (1986). https://doi.org/10.1007/BF01870702

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