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The role of mucus in ion absorption by the oesophagus of the sea-water eel (Anguilla anguilla L.)

Electrophysiological, structural and cytochemical investigations

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Summary

  1. 1.

    The structure of mucus in the oesophagus of the sea-water adapted eel, consists of a framework of fibers decreasing in density and thickness from the anterior to the posterior oesophagus.

  2. 2.

    With seawater in the lumen the mucus layer supports, in vitro, about 45% of the lumen to serosa gradient of sodium ion activity along the whole oesophagus. It supports different chloride ion activity gradients: about 80% in the anterior and about 45% in the middle and posterior oesophagus. These results are confirmed by X-ray micro-analysis.

  3. 3.

    Experiments without lumen-to-serosa gradients demonstrate a linked sodium and chloride active absorption appearing in the middle oesophagus and increasing towards the posterior oesophagus.

  4. 4.

    Na+−K+-ATPase is cytochemically demon-strated but could not be inhibited by ouabaïn during in vitro experiments, due to its particular localization.

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Abbreviations

SW :

seawater

FW :

freshwater

SEM :

scanning electron microscope

TEM :

transmission electron microscope

ISM :

ion-selective microelectrode

References

  • Allen A, Pain RH, Robson TR (1976) Model for the structure of the gastric mucous gel. Nature 264:88–89

    Google Scholar 

  • Allen A, Flemström G, Garner A, Silen W, Turnberg LA (1984) Mechanisms of mucosal protection in the upper gastrointestinal tract. Raven Press, New York

    Google Scholar 

  • Armstrong W McD, Garcia-Diaz JF (1980) Ion-selective micro-electrodes: theory and technique. Federation Proc 39:2851–2859

    Google Scholar 

  • Bert P (1871) Sur les phénomènes et les causes de la mort des animaux d'eau douce que l'on plonge dans l'eau de mer. CR Acad Sci Paris 75:382–385, 464–467

    Google Scholar 

  • Clamp JR, Cooper B, Creeth M, Ene D, Barrett J, Gouth M (1983) The presence of polysaccharides in normal human gastric mucus. Biochem J 215:421–423

    Google Scholar 

  • Ernst SA (1972) Transport adenosine triphosphatase cytochemistry. 1. Biochemical characterization of a cytochemical medium for the ultrastructural localization of ouabaïne-sensitive, potassium-dependent phosphatase activity in the avian salt gland. J Histochem Cytochem 20:13–22

    Google Scholar 

  • Engelhardt W von, Rechkemmer G (1983) Absorption of inorganic ions and short-chain fatty acids in the colon of mammals. In: Gilles-Baillien M, Gilles R (eds) Intestinal Transport. Springer, Berlin Heidelberg New York, pp 26–45

    Google Scholar 

  • Fauconneau B, Saglio P (1984) Protein-bound and free amino acid content in the skin mucus of the European eelAnguilla anguilla (L.). Comp Biochem Physiol 77B:513–516

    Google Scholar 

  • Field M, Karnaky KJ, Smith PL, Bolton JE, Kinter WB (1978) Ion transport across the isolated intestinal mucosa of the winter flounder,Pseudopleuronectes americanus. I. Functional and structural properties of cellular and paracellular pathways for Na and Cl. J Membrane Biol 41:265–293

    Google Scholar 

  • Flood PR (1981) On the ultrastructure of mucus. Biomed Res 2:49–53

    Google Scholar 

  • Flood PR, Fiala-Medioni A (1981) Ultrastructure and histochemistry of the food trapping mucous film in benthic filter-feeders (Ascidians). Acta Zool 62:53–65

    Google Scholar 

  • Frizzell RA, Field M, Schultz SG (1979) Sodium-coupled chloride transport by epithelial tissues. Am J Physiol 236:F1-F8

    Google Scholar 

  • Garner A, Flemström G, Allen A, Heylings JR McQueen S (1984) Gastric mucosal protective mechanisms: roles of epithelial bicarbonate and mucus secretions. Scand J Gastroenterol 19:79–86

    Google Scholar 

  • Gilles-Baillien M (1983) Several compartments involved in intestinal transport. In: Gilles-Baillien M, Gilles R (eds) Intestinal transport. Springer, Berlin Heidelberg New York, pp 103–119

    Google Scholar 

  • Humbert W, Kirsch R, Meister MF (1984) Scanning electron microscopic study of the oesophageal mucous layer in the eel,Anguilla anguilla, L. J Fish Biol 25:117–122

    Google Scholar 

  • Jehl B, Bauer B, Dörge A, Rick K (1981) The use of propane/isopentane mixtures for rapid freezing of biological specimens. J Microsc 123:307–309

    Google Scholar 

  • Kirsch R, Guinier D, Meens R (1975) L'équilibre hydrique de l'anguille européenne (Anguilla anguilla L.). Etude du rôle de l'oesophage dans l'utilisation de l'eau de boisson et étude de la perméabilité osmotique branchiale. J Physiol (Paris) 70:605–626

    Google Scholar 

  • Kirsch R (1978) Role of the oesophagus in osmoregulation in teleost fishes. In: Jorgensen CB, Skadhauge E (eds) Osmotic and volume regulation. Alfred Benzon Symposium XI, Munskgaard. Academic Press, New York, pp 138–154

    Google Scholar 

  • Kirsch R, Meister MF (1982) Progressive processing of ingested water in the gut of sea-water teleosts. J Exp Biol 98:67–81

    Google Scholar 

  • Kirsch R, Humbert W, Rodeau JL (1984) Control of the blood osmolarity in fishes, with references to the functional anatomy of the gut. In: Pequeux A, Gilles R, Bolis A (eds) Osmo-regulation in estuarine and marine animals. Springer, Berlin Heidelberg New York, pp 67–92

    Google Scholar 

  • Kirsch R, Humbert W, Simonneaux V (1985) The gut as an osmoregulatory organ: comparative aspects and special references to fishes. In: Gilles R, Gilles-Baillien M (eds) Transport processes, Iono- and osmoregulation. Springer, Berlin Heidelberg New York, pp 265–277

    Google Scholar 

  • Kirschner LB (1978) External charged layer and Na+ regulation. In: Jorgensen CB, Skadhauge E (eds) Osmotic and volume regulation. Alfred Benzon symposium XI, Munskgaard. Academic Press, New York, pp 310–321

    Google Scholar 

  • Laurent P, Kirsch R (1975) Modifications structurales de l'oesophage liées à l'osmorégulation chez l'anguille. CR Acad Sci Paris 280:2227–2229

    Google Scholar 

  • Lee CO (1981) Determination of selectivity coefficients of ion-selective microelectrodes. In: Sykova E, Hnick P, Vyklicky L (eds) Ion-selective microelectrodes and their use in excitable tissues. Plenum Press, New York, pp 47–52

    Google Scholar 

  • Lemoine AM, Olivereau M (1973a) Variations de la teneur en acide N-acetyl-neuraminique de la branchie de l'anguille au cours des changements de salinité. CR Soc Biol 167:411–416

    Google Scholar 

  • Lemoine AM, Olivereau M (1973b) Variations de la teneur en acide N-acetyl-neuraminique de l'intestin de l'anguille, au cours des changements de salinité. CR Soc Biol 167:644–649

    Google Scholar 

  • Marriott C (1983) The effects of drugs on the structure and secretion of mucus. Pharm Int Dec 1983:320–323

    Google Scholar 

  • Marshall WS (1978) On the involvement of mucous secretion in teleost osmoregulation. Can J Zool 56:1088–1091

    Google Scholar 

  • Meier PC, Lanter F, Ammann D, Steiner RA, Simon W (1982) Applicability of available ion-selective liquid-membrane microelectrodes to intracellular ion-activity measurements. Pflügers Arch 393:23–30

    Google Scholar 

  • Meister MF, Humbert W, Kirsch R, Vivien-Roëls B (1983) Structure and ultrastructure of the oesophagus in sea-water and fresh-water teleosts (Pisces). Zoomorphology 102:33–51

    Google Scholar 

  • Nonnotte G (1983) Fonctions de la peau des téléotéens: étude expérimentale des échanges respiratoires et des échanges ioniques. Thèse, Strasbourg

  • Olivereau M, Lemoine AM (1972) Effects des variations de la salinité externe sur la teneur en acide N-acetyl-neuraminique (ANAN) de la peau chez l'Anguille. J Comp Physiol 79:411–422

    Google Scholar 

  • Parmelee JT, Renfro JL (1983) Esophageal desalination of sea-water in flounder: role of active sodium transport. Am J Physiol 245:R888–R893

    Google Scholar 

  • Parson R (1959) Handbook of electrochemical constants. Butterworths, London

    Google Scholar 

  • Pärt P, Lock RAC (1983) Diffusion of calcium, cadmium and mercury in a mucous solution from rainbow trout. Comp Biochem Physiol 76C:259–263

    Google Scholar 

  • Portier P, Duval M (1922) Variations de la pression osmotique du sang de l'anguille essuyée en fonction des modifications de la salinité du milieu exterieur. CR Acad Sci Paris 175:1100–1105

    Google Scholar 

  • Robinson RA, Stokes RH (1959) Electrolyte solutions. Butter-worths, London

    Google Scholar 

  • Sakata T, Engelhardt von W (1981) Luminal mucin in the large intestine of mice, rats and guinea pigs. Cell Tissue Res 219:629–635

    Google Scholar 

  • Shelhamer JH, Marom Z, Logun C, Kaliner M (1984) Human respiratory mucous glycoproteins. Exp Lung Res 7:149–162

    Google Scholar 

  • Shephard KL (1981) The influence of mucus on the diffusion of water across fish epidermis. Physiol Zool 54:224–229

    Google Scholar 

  • Shephard KL (1982) The influence of mucus on the diffusion of ions across the oesophagus of fish. Physiol Zool 55:23–34

    Google Scholar 

  • Shephard KL (1984a) Diffusion of chloride ions in the mucus of the oesophagus ofEnophrys bison, a marine teleost fish. Pflügers Arch 402:207–210

    Google Scholar 

  • Shephard KL (1984b) The influence of mucus on the diffusion of the chloride ions across the oesophagus of the minnow (Phoxinus phoxinus L.). J Physiol 346:449–460

    Google Scholar 

  • Shiau YF, Fernandez P, Jackson MJ, McMonagle S (1985) Mechanisms maintaining a low-pH microclimate in the intestine. Am J Physiol 248:G608–G617

    Google Scholar 

  • Singh B, Thakur R (1975) A histochemical study on the respiratory epithelia of an eel fish,Amphipnous cuchia. Acta Hist 54:161–167

    Google Scholar 

  • Skadhauge E (1974) Coupling of transmural flows of NaCl and water in the intestine of the eel (Anguilla anguilla). J Exp Biol 60:535–546

    Google Scholar 

  • Schlichter LC (1982) Unstirred mucous layers: ion exchange properties and effect on ion regulation inLymnea stagnalis. J Exp Biol 98:363–372

    Google Scholar 

  • Stith BJ (1984) Biochemical examination ofRana pipiens epithelial mucus. J Comp Physiol B 155:89–96

    Google Scholar 

  • Thomas RC (1978) Ion-Sensitive Intracellular Microelectrodes. Academic Press, London New York San Fransisco

    Google Scholar 

  • Yamamoto M, Hirano T (1978) Morphological changes in the oesophageal epithelium of the eel,Anguilla japonica during adaptation to sea water. Cell Tissue Res 192:25–38

    Google Scholar 

Download references

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Simonneaux, V., Barra, J.A., Humbert, W. et al. The role of mucus in ion absorption by the oesophagus of the sea-water eel (Anguilla anguilla L.). J Comp Physiol B 157, 187–199 (1987). https://doi.org/10.1007/BF00692363

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  • DOI: https://doi.org/10.1007/BF00692363

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