Journal of Comparative Physiology B

, Volume 164, Issue 1, pp 47–54 | Cite as

Characterization of esophageal desalination in the seawater eel,Anguilla japonica

  • K. Nagashima
  • M. Ando
Article

Abstract

To characterize mechanisms of esophageal desalination, osmotic water permeability and ion fluxes were measured in the isolated esophagus of the seawater eel. The osmotic permeability coefficient in the seawater eel esophagus was 2·10-4 cm·s-1. This value was much lower than those in tight epithelial, although the eel esophagus is a leaky epithelium with a tissue resistance of 77 ohm·cm-2. When the esophagus was bathed in normal Ringer solutions on both sides no net ion and water fluxes were observed. However, when mucosal NaCl concentration was increased by a factor of 3, Na+ und Cl- ions were transferred from mucosa to serosa (desalination). If only Na+ or Cl- concentration in the mucosal fluid was increased by a factor of 3, net Na+ and Cl- fluxes were reduced to 30–40%, indicating that 60–70% of the net Na+ and Cl- fluxes are coupled mutually. The coupled NaCl transport seems to be effective in desalting the luminal high NaCl. The remaining 30–40% of the total Na+ and Cl- fluxes seems to be due to a simple diffusion, because these components are independent of each other and follow their electrochemical gradients, and also because these fluxes remain even after treatment with NaCN or ouabain. A half of the coupled NaCl transport could be explained by a Na+/H+−Cl-/HCO 3 - double exchanger on the apical membrane of the esophageal epithelium, because mucosal amiloride and 4.4′-diisothiocyanatostilbene-2,2′-disulphonic acid inhibited the net Na+ and Cl- fluxes by approximately 30%. The other half of the coupled NaCl transport, which follows their electrochemical gradients, still remains to be explained.

Key words

Esophagus Desalination Coupled NaCl transport Water permeability Eel,Anguilla japonica 

Abbreviations

DIDS

4,4′-diisothiocyanatostilbene-2,2′-disulphonic acid

NMDG

N-methyl-d-glucosamine

PCl

Cl- permeability coefficient

PD

transepithelial potential difference

PNa

Na+ permeability coefficient

Posm

osinotic permeability coefficient

TALH

thick ascending limb of Henle's loop

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References

  1. Ando M (1975) Intestinal water and chloride pump in relation to seawater adaptation of the eel,Anguilla japonica. Comp Biochem Physiol 52A:229–233Google Scholar
  2. Ando M (1983) Potassium-dependent chloride and water transport across the seawater eel intestine. J Membr Biol 73:125–130Google Scholar
  3. Ando M, Kobayashi M (1978) Effects of stripping of the outer layers of the eel intestine on salt and water transport. Comp Biochem Physiol 61 A:497–501Google Scholar
  4. Ando M, Subramanyam MVV (1990) Bicarbonate transport systems in the intestine of the seawater eel. J Exp Biol 150:381–394Google Scholar
  5. Brodsky WA, Schilb TJ (1965) Osmotic properties of isolated turtle bladder. Am J Physiol 208:46–57Google Scholar
  6. Burg MB, Green N (1973) Function of the thick ascending limb of Henle's loop. Am J Physiol 224:659–668Google Scholar
  7. Cabantchik ZI, Rothstein A (1972) The nature of the membrane sites controlling anion permeability of human red blood cells as determined by studies with disulfonic stilbene derivatives. J Membr Biol 10:215–255Google Scholar
  8. Cremaschi D, Meyer G, Botta G, Rossetti C (1987) The nature of the neutral Na+−Cl--coupled entry at the apical membrane of rabbit gall bladder epithelium: II. Na+−Cl- symport is independent of K+. J Membr Biol 95:219–228Google Scholar
  9. Curran PF, Solomon AK (1957) Ion and water fluxes in the ileum of rats. J Gen Physiol 41:143–168Google Scholar
  10. Diamond JM (1962) The reabsorptive function of the gall-bladder. J Physiol (Lond) 161:442–473Google Scholar
  11. Diamond JM (1964) The mechanism of isotonic water transport. J Gen Physiol 48:15–42Google Scholar
  12. Frizzell RA, Koch MJ, Schultz SG (1976) Ion transport by rabbit colon. I. Active and passive components. J Membr Biol 27:297–316Google Scholar
  13. Frizzell RA, Schultz SG (1972) Ionic conductances of extracellular shunt pathway in rabbit ileum. Influence of shunt on transmural sodium transport and electrical potential differences. J Gen Physiol 59:318–346Google Scholar
  14. Frömter E, Diamond J (1972) Route of passive ion permeation in epithelia. Nature 235:9–13Google Scholar
  15. Haas M, Dunham PB, Forbush III B (1991) [3H] bumetanide binding to mouse kidney membranes: identification of corresponding membrane proteins. Am J Physiol 260: C791-C804Google Scholar
  16. Hirano T, Mayer-Gostan N (1976) Eel esophagus as an osmoregulatory organ. Proc Natl Acad Sci USA 73:1348–1350Google Scholar
  17. House CR, Green K (1965) Ion and water transport in isolated intestine of the marine teleost,Cottus scorpius. J Exp Biol 42:177–189Google Scholar
  18. Huf EG, Parrish J, Weatherford C (1951) Active salt and water uptake by isolated frog skin. Am J Physiol 164:137–142Google Scholar
  19. Kirsch R (1978) Role of the esophagus in osmoregulation in teleost fishes. In: Jorgensen CB, Skadhauge E (eds) Osmotic and volume regulation. Academic Press New York, pp 138–154Google Scholar
  20. Kleyman TR, Cragoe EJ Jr (1988) Amiloride and its analogs as tools in the study of ion transport. J Membr Biol 105:1–21Google Scholar
  21. Marsh DJ, Spring KR (1985) Polarity of volume-regulatory increase byNecturus gallbladder epithelium. Am J Physiol 249:C471-C475Google Scholar
  22. Parmelee JT, Renfro JL (1983) Esophageal desalination of seawater in flounder: role of active sodium transport. Am J Physiol 245:R888-R893Google Scholar
  23. Shi L-B, Fushimi K, Verkman AS (1991) Solvent drag measurement of transcellular and basolateral membrane NaCl reflection coefficient in kidney proximal tubule. J Gen Physiol 98:379–398Google Scholar
  24. Simonneaux V, Barra JA, Humbert W, Kirsch R (1987) The role of mucus in ion absorption by the oesophagus of the sea-water eel (Anguilla anguilla L). Electrophysiological, structural and cytochemical investigation. J Comp Physiol B 157:187–199Google Scholar
  25. Villegas L, Sananes L (1968) Independence between ionic transport and net water flux in frog gastric mucosa. Am J Physiol 214:997–1000Google Scholar
  26. Vulliemin P, Durand-Arczynska W, Durand J (1983) Electrical properties and electrolyte transport in bovine tracheal epithelium: effects of ion substitutions, transport inhibitors and histamine. Pflügers Arch 396:54–59Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • K. Nagashima
    • 1
  • M. Ando
    • 1
  1. 1.Laboratory of Physiology, Faculty of Integrated Arts and SciencesHiroshima UniversityHiroshimaJapan

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