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Active sodium transport and the electrophysiology of rabbit colon

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Summary

The electrophysiologic properties of rabbit colonic epithelial cells were investigated employing microelectrode techniques. Under open-circuit conditions, the transepithelial electrical potential difference (PD) averaged 20 mV, serosa positive, and the intracellular electrical potential (ψ mc ) averaged −32 mV, cell interior negative with respect to the mucosal solution; under short-circuit conditions,ψ mc averaged −46 mV. The addition of amiloride to the mucosal solution abolishes the transepithelialPD and active Na transport, andψ mc is hyperpolarized to an average value of −53 mV. These results indicate that Na entry into the mucosal cell is a conductive process which, normally, depolarizesψ mc .

The data obtained were interpreted using a double-membrane equivalent electrical circuit model of the “active Na transport pathway” involving two voltage-independent electromotive forces (emf's) and two voltage-independent resistances arrayed in series. Our observations are consistent with the notions that:

  1. (a)

    The emf's and resistances across the mucosal and baso-lateral membranes are determined predominantly by the emf (64mV) and resistance of the Na entry process and the emf (53 mV) and resistance of the process responsible for active Na extrusion across the baso-lateral membranes: that is, the electrophysiological properties of the cell appear to be determined solely by the properties and processes responsible for transcellular active Na transport. The emf of the Na entry process is consistent with the notion that the Na activity in the intracellular transport pool is approximately one-tenth that in the mucosal solution or about 14mM.

  2. (b)

    In the presence of amiloride, the transcellular conductance is essentially abolished and the total tissue conductance is the result of ionic diffusion through paracellular pathways.

  3. (c)

    The negative intracellular potential (with respect to the mucosal solution) is due primarily to the presence of a low resistance paracellular “shunt” pathway which permits electrical coupling between the emf at the baso-lateral membrane and the potential difference across the mucosal membrane; in the absence of this shunt, the “well-type” electrical potential profile characteristic of rabbit colonic cells would be ‘converted’ into a “staircase-type” profile similar to those reported for frog skin and toad urinary bladder by some investigators.

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References

  • 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

    Google Scholar 

  • Biber, T.U.L., Sanders, M.L. 1973. Influence of transepithelial potential difference on the sodium uptake at the outer surface of the isolated frog skin.J. Gen. Physiol. 61:529

    Google Scholar 

  • Boulpaep, E.L. 1976. Electrical phenomena in the nephron.Kidney Int. 9:88

    Google Scholar 

  • Cereijido, M., Curran, P.F. 1965. Intracellular electrical potentials in frog skin.J. Gen. Physiol. 48:543

    Google Scholar 

  • Chen, J.S., Walser, M. 1975. Sodium fluxes through the active transport pathway in toad bladder.J. Membrane Biol. 21:87

    Google Scholar 

  • Civan, M.M. 1970. Effects of active sodium transport on current-voltage relationship of toad bladder.Am.J. Physiol. 219:234

    Google Scholar 

  • 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

    Google Scholar 

  • Engbaek, L., Hoshiko, T. 1957. Electrical potential gradients through frog skin.Acta Physiol. Scand. 39:348

    Google Scholar 

  • Essig, A., Caplan, S.R. 1968. Energetics of active transport processes.Biophys. J. 8:1434

    Google Scholar 

  • Finkelstein, A. 1964. Carrier model for active transport of ions across a mosaic membrane.Biophys. J. 4:421

    Google Scholar 

  • Finkelstein, A., Mauro, A. 1963. Equivalent circuits as related to ionic systems.Biophys. J. 3:215

    Google Scholar 

  • Flemström, G., Sachs, G. 1975. Ion transport by amphibian antrum in vitro. I. General characteristics.Am. J. Physiol. 228:1188

    Google Scholar 

  • Frazier, H.S. 1962. The electrical potential profile of the isolated toad bladder.J. Gen. Physiol. 59:794

    Google Scholar 

  • Frizzell, R.A., Koch, M.J., Cooper, D., Schultz, S.G. 1975. Ion transport by rabbit colon: Effect of amiloride.Fed. Proc. 34:285

    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

    Google Scholar 

  • Frizzell, R.A., Schultz, S.G. 1976. Ion transport by rabbit colon: Effect of amphotericin B.Fed. Proc. 35:602

    Google Scholar 

  • Frömter, E. 1972. The route of passive ion movement though the epithelium of Necturus gallbladder.J. Membrane Biol. 8:259

    Google Scholar 

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

  • Fuchs, W., Larsen, E.H., Lindemann, B. 1975. Estimation of intracellular Na-activity and of Na-permeability from current-voltage curves of Na-channels in frog skin.Pfluegers Arch. 355:R 71

    Google Scholar 

  • Garrahan, P.J., Glynn, I.M. 1967. The incorporation of inorganic phosphate into adenosine triphosphate by reversal of the sodium pump.J. Physiol. (London) 192:237

    Google Scholar 

  • Handler, J.S., Preston, A.S., Orloff, J. 1972. Effect of ADH, aldosterone, ouabain and amiloride on toad bladder epithelial cells.Am. J. Physiol. 222:1071

    Google Scholar 

  • Helman, S.I. 1972. Determination of electrical resistance of the isolated cortical collecting tubule and its possible anatomic location.Yale J. Biol. Med. 45:339

    Google Scholar 

  • Helman, S.J., Fisher, R.S. 1976. Localization and determination of the driving force for sodium transport by the frog skin.Fed. Proc. 35:702

    Google Scholar 

  • Helman, S.I., O'Nell, R.G., Fisher, R.S. 1975. Determination of theE Na of frog skin from studies of its current-voltage relationship.Am. J. Physiol. 229:947

    Google Scholar 

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

    Google Scholar 

  • Higgins, J.T., Frömter, E. 1974. Potential profile in Necturus urinary bladder.Pfluegers Arch. 347:R 32

    Google Scholar 

  • 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

    Google Scholar 

  • Hoshiko, T. 1961. Electrogenesis in frog skin.In: Biophysics of Physiological and Pharmacological Actions. p. 31. American Association for the Advancement of Science, Washington

    Google Scholar 

  • Katchalsky, A., Curran, P.F. 1965. Nonequilibrium Thermodynamics in Biophysics. Harvard University Press, Cambridge

    Google Scholar 

  • Kedem, O., Caplan, S.R. 1965. Degree of coupling and its relation to efficiency of energy conversion.Trans. Faraday Soc. 61:1897

    Google Scholar 

  • 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. Munksgaard, Copenhagen

    Google Scholar 

  • Lewis, S.A., Diamond, J.M. 1976. Na+ transport by rabbit urinary bladder, a tight epithelium.J. Membrane Biol. 28:1

    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 

  • Lindemann, B., Driessche, W., van 1977. Sodium-specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover.Science 195:292

    Google Scholar 

  • Lindemann, B., Voute, C. 1976. Structure and function of the epidermis.In: Frog Neurobiology. R. Llinas and W. Precht, editors. Chapter 5, p. 169. Springer-Verlag, Berlin

    Google Scholar 

  • Macknight, A.D.C., Civan, M.M., Leaf, A. 1975. The sodium transport pool in toad urinary bladder epithelial cells.J. Membrane Biol. 20:365

    Google Scholar 

  • Mandel, L.J., Curran, P.F. 1972. Response of the frog skin to steady-state voltage clamping. I. The shunt pathway.J. Gen. Physiol. 59:503

    Google Scholar 

  • Mitchell, P. 1970. Reversible coupling between transport and chemical reactions.In: Membranes and Ion transport. E.E. Bittar, editor. Vol. 1, p. 192. Wiley-Interscience, London

    Google Scholar 

  • Nagel, W. 1976. The intracellular electrical potential profile of the frog skin epithelium.Pfluegers Arch. 365:135

    Google Scholar 

  • Nagel, W., Dörge, A. 1970. Effect of amiloride on sodium transport of frog skin. I. Action on intracellular sodium content.Pfluegers Arch. 317:84

    Google Scholar 

  • Oster, G., Perelson, A., Katchalsky, A. 1971. Network thermodynamics.Nature (London) 234:393

    Google Scholar 

  • Oster, G.F., Perelson, A.S., Katchalsky, A. 1973. Network thermodynamics: Dynamic modeling of biophysical systems.Q. Rev. Biophys. 6:1

    Google Scholar 

  • Peusner, L. 1970. The Principles of Network Thermodynamics: Theory and Biophysical Applications. Ph.D. Thesis. Harvard University, Cambridge

    Google Scholar 

  • Reuss, L., Finn, A.L. 1974. Passive electrical properties of toad urinary bladder epithelium.J. Gen. Physiol. 64:1

    Google Scholar 

  • Reuss, L., Finn, A.L. 1975. Dependence of serosal membrane potential on mucosal membrane potential in toad urinary bladder.Biophys. J. 15:71

    Google Scholar 

  • Rick, R., Dörge, A., Nagel, W. 1975. Influx and efflux of sodium at the outer surface of frog skin.J. Membrane Biol. 22:183

    Google Scholar 

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

    Google Scholar 

  • Saito, T., Lief, P.D., Essig, A. 1974. Conductance of active and passive pathways in the toad bladder.Am. J. Physiol. 226:1265

    Google Scholar 

  • Schultz, S.G. 1972. Electrical potential differences and electromotive forces in epithelial tissues.J. Gen. Physiol. 59:794

    Google Scholar 

  • Schultz, S.G., Frizzell, R.A. 1976. Ionic permeability of epithelial tissues.Biochim. Biophys. Acta 443:181

    Google Scholar 

  • Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1977. An equivalent electrical circuit model for sodium transporting epithelia.J. Theoret. Biol. (in press)

  • Schultz, S.G., Zalusky, R. 1964. Ion transport in rabbit ileum. I. Short-circuit current and Na fluxes.J. Gen. Physiol. 47:567

    Google Scholar 

  • Ussing, H.H. 1960. The Alkali Metal Ions in Biology. Springer-Verlag, Berlin

    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., Windhager, E.E. 1964. Nature of shunt path and active sodium transport path through frog skin epithelium.Acta Physiol. Scand. 61:484

    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 

  • Vieira, F.L., Caplan, S.R., Essig, A. 1972a. Energetics of sodium transport in frog skin. I. Oxygen consumption in the short-circuited state.J. Gen. Physiol. 59:60

    Google Scholar 

  • Vieira, F.L., Caplan, S.R., Essig, A. 1972b. Energetics of sodium transport in frog skin. II. The effects of electrical potential on oxygen consumption.J. Gen. Physiol. 59:77

    Google Scholar 

  • Whittembury, G. 1964. Electrical potential profile of the toad skin epithelium.J. Gen. Physiol. 47:795

    Google Scholar 

  • Yonath, J., Civan, M.M. 1971. Determination of the driving force of the Na+ pump in toad bladder by means of vasopressin.J. Membrane Biol. 5:366

    Google Scholar 

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  1. Hugh N. Nellans

    Present address: Departments of Medicine and Physiology, University of Rochester, School of Medicine and Dentistry, 14642, Rochester, New York

Authors and Affiliations

  1. Department of Physiology, University of Pittsburgh School of Medicine, 15261, Pittsburgh, Pennsylvania

    Stanley G. Schultz, Raymond A. Frizzell & Hugh N. Nellans

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  2. Raymond A. Frizzell
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Schultz, S.G., Frizzell, R.A. & Nellans, H.N. Active sodium transport and the electrophysiology of rabbit colon. J. Membrain Biol. 33, 351–384 (1977). https://doi.org/10.1007/BF01869524

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  • DOI: https://doi.org/10.1007/BF01869524

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