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Sodium-coupled amino acid and sugar transport byNecturus small intestine

An equivalent electrical circuit analysis of a rheogenic co-transport system

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Summary

Necturus small intestine actively absorbs sugars and amino acids by Na-coupled mechanisms that result in increases in the transepithelial electrical potential difference (ψ ms) and the short-circuit current (I sc) which can be attributed entirely to an increase in the rate of active Na absorption. Studies employing conventional microelectrodes indicate that the addition of alanine or galactose to the mucosal solution is followed by a biphasic response. Initially, there is a rapid depolarization of the electrical potential difference across the apical membrane (ψ ms) which reverses polarity (i.e. cell interior becomes positive with respect to the mucosal solution) and a marked decrease in the ratio of the effective resistance of the mucosal membrane to that of the serosal membrane (R m/R s); these events do not appear to be dependent on the availability of metabolic energy. These initial, rapid events are followed by a slow increase in (R m/R s) toward control values which is paralleled by a repolarization ofψ ms and increases inψ ms andI sc; this slow series of events is dependent upon the availability of metabolic energy.

The results of these studies indicate that: (i) the Na-coupled mechanisms that mediate the entry of sugars and amino acids across the apical membrane are “rheogenic” (conductive) and result in a decrease inR m and a depolarization ofψ ms; and (ii) the subsequent increase in (R m/R s) and repolarization ofψ ms are the results of a decrease inR s which is associated with an increase in the activity of the Na pump at the basolateral membrane.

The physiologic implications of these findings are discussed and an equivalent electrical circuit model for “rheogenic” Na-coupled solute transport processes is analyzed.

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References

  • Barry, R.J.L., Eggenton, J. 1972. Membrane potentials of epithelial cells in rat small intestine.J. Physiol. (London) 277:201–216

    Google Scholar 

  • Degnan, K.J., Zadunaisky, J.A. 1976. The electrical properties and active ion transport across the urinary bladder of the urodele,Amphiuma means.J. Physiol. (London) 265:207–230

    Google Scholar 

  • DeLong, J., Civan, M.M. 1978. Dissociation of cellular K+ accumulation from net Na+ transport by toad urinary bladder.J. Membrane Biol. 42:19–43

    Google Scholar 

  • Duffey, M.E., Turnheim, K., Frizzell, R.A., Schultz, S.G. 1978. Intracellular chloride activities in rabbit gallbladder: Direct evidence for the role of the sodium gradient in energizing “uphill” chloride transport.J. Membrane Biol. 42:229–245

    Google Scholar 

  • Finkelstein, A., Mauro, A. 1963. Equivalent circuits as related to ionic systems.Biophys. J. 3:215–233

    Google Scholar 

  • Frizzell, R.A., Field, M., Schultz, S.G. 1979. Sodium-coupled chloride transport by epithelia tissues.Am. J. Physiol. 236:F1-F8

    PubMed  Google Scholar 

  • Fromm, M., Schultz, S.G. 1981. Some properties of KCl-filled microelectrodes: Correlation of potassium “leakage” with tip resistance.J. Membrane Biol. 62:239–244

    Google Scholar 

  • Frömter, E. 1977. Magnitude and significance of the paracellular shunt path in rat kidney proximal tubule.In: Intestinal Permeation. H. Kramer and E. Lauterbach, editors. pp. 166–178. Excerpta Medica, Amsterdam

    Google Scholar 

  • Frömter, E. 1979. Solute transport across epithelia: What can we learn from micropuncture studies on kidney tubules.J. Physiol. (London) 288:1–31

    Google Scholar 

  • Garcia-Diaz, J.F., O'Doherty, J., Armstrong, W.McD. 1978. Potential profile, K and Na activities inNecturus small intestine.Physiologist 21:41

    PubMed  Google Scholar 

  • Gilles-Ballien, M., Schoffeniels, E. 1965. Site of action ofl-alanine andd-glucose on the potential differences across the intestine.Arch. Int. Physiol. Biochim. 73:355–357

    PubMed  Google Scholar 

  • Gunter-Smith, P.J., Grasset, E., Schultz, S.G. 1980. The electrophysiology of Na-coupled alanine transport inNecturus small intestine.J. Gen. Physiol. 74:11a

    Google Scholar 

  • Gunter-Smith, P.J., Schultz, S.G. 1982. Potassium transport and intracellular potassium activities in rabbit gallbladder.J. Membrane Biol. (in press)

  • Gunter-Smith, P.J., White, J.F. 1979. Contributions of villus and intervillus epithelium to intestinal transmural p.d. and response to theophylline and sugar.Biochim. Biophys. Acta 557:425–435

    PubMed  Google Scholar 

  • Helman, S.I., Nagel, W., Fisher, R.S. 1979. Ouabain on active transepithelial sodium transport in frog skin. Studies with microelectrodes.J. Gen. Physiol. 74:105–127

    PubMed  Google Scholar 

  • Higgins, T.J., Gebler, B., Frömter, E. 1977. Electrical properties of amphibian urinary bladder epithelia. I. The cell potential profile ofNecturus maculosus.Pfluegers Arch. 371:87–97

    Google Scholar 

  • Hoshi, T., Sudo, K., Suzuki, Y. 1976. Characteristics of changes in the intracellular potential associated with transport of neutral, dibasic and acidic amino acids inTriturus proximal tubule.Biochim. Biophys. Acta 448:492–504

    PubMed  Google Scholar 

  • Kristensen, L.O. 1980. Energization of alanine transport in isolated rat hepatocytes.J. Biol. Chem. 255:5236–5243

    PubMed  Google Scholar 

  • Lee, C.O., Armstrong, W.McD. 1972. Activities of sodium and potassium ions in epithelial cells of small intestine.Science 175:1261–1264

    PubMed  Google Scholar 

  • Lew, V.L., Beauge, L. 1979. Passive cation fluxes in red cell membranes.In: Membrane Transport in Biology. G. Giebisch, D.C. Tosteson, and H.H. Ussing, editors. Vol. 2, pp. 81–115. Springer-Verlag, Berlin

    Google Scholar 

  • Lyon, I., Sheerin, H.E. 1971. Studies on transmural potentialsin vitro in relation to intestinal absorption. VI. The effect of sugars on electrical potential profiles in jejunum and ileum.Biochim. Biophys. Acta 249:1–4

    PubMed  Google Scholar 

  • MacRobbie, E.A.C., Ussing, H.H. 1961. Osmotic behaviour of the epithelial cells of frog skin.Acta Physiol. Scand. 53:348–365

    PubMed  Google Scholar 

  • Maruyama, T., Hoshi, T. 1972. The effect ofd-glucose on the electrical potential profile across the proximal tubule of newt kidney.Biochim. Biophys. Acta 282:214–225

    PubMed  Google Scholar 

  • Okada, Y., Irimajiri, A., Inouye, A. 1977a. Electrical properties and active solute transport in rat small intestine: II. Conductive properties of transepithelial routes.J. Membrane Biol. 31:221–232

    Google Scholar 

  • Okada, Y., Tsuchiya, W., Irimajiri, A., Inouye, A. 1977b. Electrical properties and active solute transport in rat small intestine: I. Potential profile changes associated with sugar and amino acid transport.J. Membrane Biol. 31:205–219

    Google Scholar 

  • Rose, R.C., Schultz, S.G. 1971. Studies on the electrical potential profile across rabbit ileum. Effects of sugars and amino acids on transmural and transmucosal electrical potential differences.J. Gen. Physiol. 57:639–663

    PubMed  Google Scholar 

  • Schultz, S.G. 1977. Sodium-coupled solute transport by small intestine: A status report.Am. J. Physiol. 233:E249-E254

    PubMed  Google Scholar 

  • Schultz, S.G. 1979. Application of equivalent electrical circuit models to study of sodium transport across epithelial tissues.Fed. Proc. 38:2024–2029

    PubMed  Google Scholar 

  • Schultz, S.G. 1980. Basic Principles of Membrane Transport. Cambridge University Press, New York

    Google Scholar 

  • Schultz, S.G., Curran, P.F. 1970. Coupled transport of sodium and organic solute.Physiol. Rev. 50:637–718

    PubMed  Google Scholar 

  • Schultz, S.G., Frizzell, R.A., Nellans, H.N. 1974. Ion transport by mammalian small intestine.Annu. Rev. Physiol. 36:51–91

    Google Scholar 

  • Schultz, S.G., Zalusky, R. 1964a. Ion transport in isolated rabbit ileum. I. Short-circuit current and Na fluxes.J. Gen. Physiol. 47:567–584

    PubMed  Google Scholar 

  • Schultz, S.G., Zalusky, R. 1964b. Ion transport in isolated rabbit ileum. II. The interaction between active sodium transport and active sugar transport.J. Gen. Physiol. 47:1043–1059

    PubMed  Google Scholar 

  • Stark, G. 1973. Rectification phenomena in carrier-mediated ion transport.Biochim. Biophys. Acta 289:323–332

    Google Scholar 

  • Sten-Knudsen, O. 1978. Passive Transport Processes.In: Membrane Transport in Biology. G. Giebisch, D.C. Tosteson and H.H. Ussing, editors. Vol. 1, pp. 5–113. Springer-Verlag, Berlin

    Google Scholar 

  • Stirling, C.E. 1967. High-resolution radioautography of phloridzin-H3 in rings of hamster intestine.J. Cell Biol. 35:605–618

    PubMed  Google Scholar 

  • White, J.F. 1977. Alterations in electrophysiology of isolated amphibian small intestine produced by removing the muscle layers.Biochim. Biophys. Acta 467:91–102

    PubMed  Google Scholar 

  • White, J.F., Armstrong, W.McD. 1971. Effect of transported solutes on membrane potentials in bullfrog small intestine.Am. J. Physiol. 221:194–201

    PubMed  Google Scholar 

  • Wright, E.M. 1966. The origin of the glucose dependent increase in the potential difference across the tortoise small intestine.J. Physiol. (London) 185:486–500

    Google Scholar 

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Gunter-Smith, P.J., Grasset, E. & Schultz, S.G. Sodium-coupled amino acid and sugar transport byNecturus small intestine. J. Membrain Biol. 66, 25–39 (1982). https://doi.org/10.1007/BF01868479

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  • DOI: https://doi.org/10.1007/BF01868479

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