Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Sodium-dependent sugar and amino acid transport in isolated goldfish intestinal epithelium: electrophysiological evidence against direct interactions at the carrier level

Abstract

The effects of mucosal application of monosaccharides and amino acids on transepithelial and membrane potentials in isolated goldfish intestinal epithelium were investigated.

Isosmotic replacement of mucosal mannitol by sugars orl-amino acids resulted in a rapid depolarization of the mucosal membrane potential ψmc followed by a slow repolarization. Phlorizin inhibited the responses to sugar but not those to amino acids.

d-Amino acids did not induce any electrical response in the epithelium. Dose-response curves forl-amino acids showed simple saturation.

Simultaneous application ofl-amino acid and glucose induced transepithelial responses of about 80% of the sum of the separate responses to the application of amino acid or glucose alone. Simultaneous application of different amino acids in saturating concentrations did not increase the magnitude of the electrical responses.

From the measured changes in potentials we calculated the change in electromotive force across the mucosal (ΔE m) and serosal (ΔE s) membrane. The change inE m induced by combined application of alanine and glucose was 90% of the sum of the calculated values induced by glucose and alanine alone. The response ofE s to both substrates was accelerated with respect to that of separate substrates alone.

We conclude that by application of glucose in addition to alanine the influx of sodium is increased, thereby stimulating the basolaterally located electrogenic Na+/K+-pump. There are no indications for direct interaction of sugars and amino acids at the mucosal membrane of the intestinal epithelial cell.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Albus H, Bakker R, Siegenbeek van Heukelom J (1983) Circuit analysis of membrane potentials changes due to electrogenic sodium-dependent sugar transport in goldfish intestinal epithelium. Pflügers Arch 398:1–9

  2. 2.

    Albus H, Groot JA, Siegenbeek van Heukelom J (1979) Effects of glucose and ouabain on transepithelial electrical resistance and cell volume in stripped and unstripped goldfish intestine. Pflügers Arch 383:55–66

  3. 3.

    Albus H, Siegenbeek van Heukelom J (1976) The electrophysiological characteristics of glucose absorption of the goldfish intestine as compared to mammalian intestines. Comp Biochem Physiol 54A:113–119

  4. 4.

    Alvarado F (1966) Transport of sugars and amino acids in the intestine: site of inhibition byd-galactose. Science 151:1010–1013

  5. 5.

    Alvarado F (1971) Interrelation of transport systems for sugars and amino acids in small intestine. In: Armstrong WM, Nunn AS (eds) Intestinal transport of electrolytes, amino acids and sugars. Charles Thomas, Springfield, IL, USA, pp 281–318

  6. 6.

    Buclon M (1974) Bioelectric potentials and the transfer of amino acids across the digestive epithelium of the tench (Tinca tinca). J Physiol (Paris) 68:157–180

  7. 7.

    Chez RA, Schultz SG, Curran PF (1966) Effect of sugars on intestinal transport of alanine in intestine. Science 153:1012–1013

  8. 8.

    Crane RK (1965) Na-dependent transport in the intestine and other animal tissues. Fed Proc 24:1000–1005

  9. 9.

    Crane RK (1977) The gradient hypothesis and other models of carrier-mediated active transport. Rev Physiol Biochem Pharmacol 78:101–159

  10. 10.

    Freel RW, Goldner AM (1981) Sodium-coupled nonelectrolyte transport across epithelia: emerging concenpts and directions. Am J Physiol 241:G451–G460

  11. 11.

    Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. I. Basic phenomena. Pflügers Arch 393:179–189

  12. 12.

    Groot JA (1981) Cell volume regulation in goldfish intestinal mucosa. Pflügers Arch 392:57–66

  13. 13.

    Gunter-Smith PJ, Grasset E, Schultz SG (1982) Sodium-coupled amino acid and sugar transport by Necturus small intestine: An equivalent electrical circuit analysis of a rheogenic co-transport system. J Membr Biol 66:25–39

  14. 14.

    Kimmich GA, Randles J (1973) Interaction between Na-dependent transport systems for sugars and amino acids. Evidence against a role for the sodium gradient. J Membr Biol 12:47–68

  15. 15.

    Kohn PG, Smyth DH, Wright EM (1968) Effects of amino acids, dipeptides and disaccharides on the electrical potential across rat small intestine. J Physiol (Lond) 196:723–746

  16. 16.

    Lee CO, Amstrong WMcD (1972) Activities of sodium and potassium ions in epithelial cells of small intestine. Science 175:1261–1264

  17. 17.

    Munck BG (1972) Amino acid transport by rat small intestine. Galactose inhibition of transepithelial net transport as a result of stimulation of bidirectional efflux from the epithelium. Biochim Biophys Acta 266:639–648

  18. 18.

    Munck BG (1980) Transport of sugars and amino acids across guinea pig small intestine. Biochim Biophys Acta 597:411–417

  19. 19.

    Munck BG (1981) Intestinal absorption of amino acids. In: Johnson LR (ed) Physiology of the gastro-intestinal tract. Raven Press, New York, pp 1097–1122

  20. 20.

    Newey H, Smyth DH (1964) Effects of sugars on intestinal transfer o amino acids. Nature 202:400–401

  21. 21.

    O'Doherty J, Garcia-Diaz JF, Armstrong WMcD (1979) Sodium-selective liquid ion-exchanger microelectrodes for intracellular measurements. Science 203:1349–1351

  22. 22.

    Okada Y, Tschuchiya W, Irimajiri A, Inouye A (1977) Electrical properties and active solute transport in rat small intestine. I. Poten tial profile changes associated with sugar and amino acid transport. J Membr Biol 31:205–219

  23. 23.

    Paterson JYF, Sepúlveda FV, Smith MW (1979) Two-carrier influx of neutral amino acids into rabbit ileal mucosa. J Physiol (Lond) 292:339–350

  24. 24.

    Paterson JYF, Sepúlveda FV, Smith MW (1980) A sodium-independent low affinity transport system for neutral amino acids in rabbit ileal mucosa. J Physiol (Lond) 298:333–346

  25. 25.

    Read CP (1967) Studies on membrane transport. I. A common transport system for sugars and amino acids? Biol Bull 133:630–642

  26. 26.

    Robinson JWL, Alvarado F (1971) Interaction between the sugar and amino acid transport systems at the small intestinal brush border: A comparative study. Pflügers Arch 326:48–75

  27. 27.

    Robinson JWL, Alvarado F (1977) Comparative aspects of the interactions between sugar and amino acid transport systems. In: Kramer M, Lauterbach F (eds) Intestinal permeation. Excerpta Medica Foundation, Amsterdam, pp 145–163

  28. 28.

    Rose RC, Schultz SG (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

  29. 29.

    Samarzija I, Frömter E (1982a) Electrophysiological analysis of rat renal sugar and amino acid transport. III. Neutral amino acids. Pflügers Arch 393:199–209

  30. 30.

    Samarzija I, Frömter E (1982b) Electrophysiological analysis of rat renal sugar and amino acid transport. IV. Basic amino acids. Pflügers Arch 393:210–214

  31. 31.

    Samarzija I, Frömter E (1982c) Electrophysiological analysis of rat renal sugar and amino acid transport. V. Acidic amino acids. Pflügers Arch 393:215–221

  32. 32.

    Samarzija I, Hinton BT, Frömter E (1982) Electrophysiological analysis of rat renal sugar and amino acid transport. II. Dependence on various transport parameters and inhibitors. Pflügers Arch 339:190–197

  33. 33.

    Schultz SG (1977) Sodium-coupled solute transport by small intestine: a status report. Am J Physiol 233:E249–E254

  34. 34.

    Schultz SG, Curran PF (1970) Coupled transport of sodium and organic solutes. Physiol Rev 50:637–718

  35. 35.

    Schultz SG, Zalusky R (1965) Interactions between active sodium transport and active amino acid transport in isolated rabbit ileum. Nature 205:292–294

  36. 36.

    Sepúlveda FV, Smith MW (1978) Discrimination between different entry mechanisms for neutral amino acids in rabbit ileal mucosa. J Physiol (Lond) 282:73–90

  37. 37.

    Siegenbeek van Heukelom J, Van den Ham MD, Albus H, Groot JA (1981) Microscopical determination of the filtration permeability Pf of the mucosal surface of the goldfish intestinal epithelium. J Membr Biol 63:31–39

  38. 38.

    White JF, Armstrong WMcD (1971) Effect of transported solutes on membrane potentials in bullfrog small intestine. Am J Physiol 221:194–201

Download references

Author information

Correspondence to H. Albus.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Albus, H., Lippens, F. & Siegenbeek van Heukelom, J. Sodium-dependent sugar and amino acid transport in isolated goldfish intestinal epithelium: electrophysiological evidence against direct interactions at the carrier level. Pflügers Arch. 398, 10–17 (1983). https://doi.org/10.1007/BF00584706

Download citation

Key words

  • Monosaccharides
  • Amino acids
  • Cotransport
  • Na+/K+-pump
  • Intestine
  • Goldfish