Fish Physiology and Biochemistry

, Volume 13, Issue 5, pp 353–370 | Cite as

Gill epithelial cells kinetics in a freshwater teleost, Oncorhynchus mykiss during adaptation to ion-poor water and hormonal treatments

  • Pierre Laurent
  • Suzanne Dunel-Erb
  • Claudine Chevalier
  • Jacques Lignon


The aim of this work was to determine the kinetics of the dramatic development of the gill chloride cells (CCs) during adaptation of the salmonid Oncorhynchus mykiss to an ion-poor environment.

To monitor cell division, the incorporation in the mitotic cell DNA of bromo-deoxyuridine (BrdUrd) was visualized with a monoclonal antibody. The density of labelled nuclei was used as an index of cellular division (proliferation), concomitantly with morphometry of phenotypic changes monitored with SEM.

In the filament epithelium, a phase of CC differentiation occurred within 12h after the transfer, followed by a delayed phase of cell proliferation (48h). In the lamellar epithelium, the present study demonstrates the absence of cell proliferation after ion-poor water transfer. The conclusion is that proliferation (mitosis) is important in the primary filament whereas differentiation and migration (from the filament) is the main mechanism for the appearance of CCs on the secondary lamellae.

The present study suggests that cortisol promoted differentiation, but not division, of cells. CCs, presumably premature, were stained by anti-cortisol monoclonal antibody indicating the presence of cortisol. No mature CCs were stained.

Growth hormone (oGH, ratGH) increased the rate of cell division both in lamellar and filament epithelium.


TEM SEM LM chloride cell cortisol growth hormone morphometry ion poor water 


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References cited

  1. Avella, M., Masoni, A., Bornancin, M. and Mayer-Gostan, N. 1987. Gill morphology and sodium influx in the rainbow trout (Salmo gairdneri) acclimated to artificial freshwater environments. J. Exp. Zool. 242: 159–169.CrossRefGoogle Scholar
  2. Barton, B.A., Peter, R.E. and Paulencu, C.R. 1980. Plasma cortisol levels and fingerling rainbow trout (Salmo gairdneri) at rest and subjected to handling, confinement, transport, and stocking. Can. J. Fish. Aqu. Sci. 37: 805–811.CrossRefGoogle Scholar
  3. Barton, B.A., Schreck, C. and Barton, L.D. 1987. Effects of chronic cortisol administration and daily acute stress on growth, physiological condition, and stress responses in juvenile rainbow trout. Dis. Aquat. Org. 2: 173–185.Google Scholar
  4. Chakraborti, P.K., Weisbart, M. and Chakraborti, A. 1987. The presence of corticosteroid receptor activity in the gills of the brook trout, Salvelinus fontinalis. Gen. Comp. Endocrinol. 66: 323–332.PubMedCrossRefGoogle Scholar
  5. Chrétien, M. and Pisam, M. 1986. Cell renewal and differentiation in the gill epithelium of fresh- or salt-water-adapted euryhaline fish as revealed by [3H]thymidine autoradiography. Biol. Cell. 56: 137–150.Google Scholar
  6. Clarke, W.C., Farmer, S.W. and Hartwell, K.M. 1977. Effect of pituitary growth hormone on growth of Tilapia mossambica and on growth and sea water adaptation of sockeye salmon (Oncorhynchus nerka). Gen. Comp. Endocrinol. 33: 174–178.PubMedCrossRefGoogle Scholar
  7. Dunel, S. 1975. Contribution à l'étude structurale et ultrastructurale de la pseudobranchie et de son innervation chez les Téléostéens. Ph. D. Thesis. University of Strasbourg.Google Scholar
  8. Ellwart, J. and Dörmer, P. 1985. Effect of 5-fluoro-2′-deoxyridine (FdUrd) on 5-bromo-2′-deoxyuridine (BrdUrd) incorporation into DNA measured with a monoclonal BrdUrd antibody and BrdUrd/Hoechst quenching effect. Cytometry 6: 513–520.PubMedCrossRefGoogle Scholar
  9. Gratzner, H., Leif, R.C., Ingram, D.J. and Castro, A. 1975. The use of antibody specific for bromodeoxyuridine for the fluorescent determination of DNA replication in single cell and chromosome. Exp. Cell. Res. 95: 88.PubMedCrossRefGoogle Scholar
  10. Gratzner, H. 1982. Monoclonal antibody against 5-bromo- and 5-iodo-deoxyuridine: a new reagent for detection of DNA replication. Science 218: 474–475.PubMedGoogle Scholar
  11. Hootman, S.R. and Philpott, C.W. 1979. Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from the gills of euryhaline teleost. Anat. Rec. 193: 99–130.PubMedCrossRefGoogle Scholar
  12. Kikuyama, S., Kubota, T., Watanabe, M., Ishibiki, K. and Abe, O. 1988. Cell kinetic study of human carcinomas using bromodeoxyuridine. Cell Tiss. Kinet. 21: 15.Google Scholar
  13. Komourdijan, M.P., Saunders, R.L. and Fenwick, J.C. 1976. The effect of porcine somatotropin on growth and survival of Atlantic salmon (Salmo salar). Can. J. Zool. 54: 534–535.Google Scholar
  14. Laurent, P. 1984. Gill internal morphology. In Fish Physiology. Vol. 10A, pp. 73–183. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.Google Scholar
  15. Laurent, P. and Dunel, S. 1978. Relations anatomiques des ionocytes (cellules à chlorure) avec le compartiment veineux branchial: Définition de deux types d'épithélium de la branchie des poissons. C.R. Hebd. Séances Acad. Sci., Ser. D286: 1447–1450.Google Scholar
  16. Laurent, P. and Dunel, S. 1980. Morphology of gill epithelia in fish. Am. J. Physiol. 238 (Regulatory Integrative Comp. Physiol. 7V: R147–R159.Google Scholar
  17. Laurent, P. and Hebibi, N. 1989. Gill morphometry and fish osmoregulation. Can. J. Zool. 67: 3055–3063.CrossRefGoogle Scholar
  18. Laurent, P., Höbe, H. and Dunel-Erb, S. 1985. The role of environmental sodium chloride relative to calcium in gill morphology of freshwater salmonid fish. Cell Tiss. Res. 240: 675–692.CrossRefGoogle Scholar
  19. Laurent, P. and Perry, S.F. 1990. Effects of cortisol on gill chloride cell morphology and ionic uptake in the freshwater trout, Salmo gairdneri. Cell Tiss. Res. 259: 429–442.CrossRefGoogle Scholar
  20. Laurent, P. and Perry, S.F. 1991. Environmental effects on fish gill morphology. Physiol. Zool. 64: 4–25.Google Scholar
  21. Leino, R.L., McCormick, J.H. and Jensen, K.M. 1987. Changes in gill histology of fathead minnows and yellow perch transferred to soft water or acidified soft water with particular reference to chloride cells. Cell Tiss. Res. 250: 389–399.CrossRefGoogle Scholar
  22. MacCormick, J.H. 1990. Cortisol directly stimulates differentiation of chloride cells in Tilapia opercular membrane. Am. J. Physiol. 159: R857–R863.Google Scholar
  23. Madsen, S.S. 1990a. Cortisol treatment improves the development of hypoosmoregulatory mechanisms in the euryhaline rainbow trout, Salmo gairdneri. Fish Physiol. Biochem. 8: 45–52.Google Scholar
  24. Madsen, S.S. 1990b. Enhanced hypoosmoregulatory response to growth hormone after cortisol treatment in immature Salmo gairdneri. Fish Physiol. Biochem. 8: 271–279.Google Scholar
  25. Madsen, S.S. 1990c. The role of cortisol and growth hormone in SW adaptation and development of hypoosmoregulatory mechanism in seawater trout parr. Gen. Comp. Endocrinol. 79: 1–11.PubMedCrossRefGoogle Scholar
  26. Morgan, M. 1974a. The development of gill arches and gill blood vessels of the rainbow trout, Salmo gairdneri. J. Morphol. 142: 351–364.CrossRefGoogle Scholar
  27. Morgan, M. 1974b. Development of the secondary lamellae of the gills of the trout, Salmo gairdneri. Cell Tiss. Res. 151: 509–523.CrossRefGoogle Scholar
  28. Perry, S.F., Goss, G.G. and Laurent, P. 1992. The interrelationships between gill chloride cell morphology and ionic uptake in four freshwater teleosts: the effects of cortisol. Can. J. Zool. 70: 1765–1786.Google Scholar
  29. Perry, S.F. and Laurent, P. 1989. Adaptational responses of rainbow trout to lowered external NaCl Concentration: Contribution of the branchial chloride cell. J. Exp. Biol. 147: 147–168.Google Scholar
  30. Perry, S.F. and Laurent, P. 1993. Environmental effects on fish gill structure and function. In Fish Ecophysiology. pp. 231–263. Chapman and Hall, London.Google Scholar
  31. Pickering, A.D., Pottinger, T.G., Sumpter, J.P., Carragher, J.F. and Le Bail, P.Y. 1991. Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 83: 86–93.PubMedCrossRefGoogle Scholar
  32. Pisam, M. and Rambourg, A. 1991. Mitochondria-rich cells in the gill epithelium of teleost fishes: an ultrastructural approach. Int. Rev. Cytol. 130: 191–232.CrossRefGoogle Scholar
  33. Rahim, S.M., Delaunoy, J.-P. and Laurent, P. 1988. Identification and immunocytochemical localization of two different carbonic anhydrase isoenzymes in teleostean fish erythrocytes and gill epithelia. Histochemistry 89: 451–459.PubMedCrossRefGoogle Scholar
  34. Ricardi, A., Danova, M., Wilson, G., Ucci, G., Dormer, P., Mazzini, G., Brugnatelli, S., Girino, M., McNally, M.J. and Ascari, E. 1988. Cell kinetics in human malignancies studied with in vivo administration of bromodeoxyuridine and flow cytometry. Cancer Res. 48: 6238.Google Scholar
  35. Richman, N.H., III, and Zaugg, W.S. 1987. Effects of cortisol and growth hormone on osmoregulation in pre- and desmoltified coho salmon (Oncorhynchus kisutch). Gen. Comp. Endocrinol. 65: 189–198.PubMedCrossRefGoogle Scholar
  36. Sandor, T., DiBatista, J.A. and Medhi, A.Z. 1984. Glucocorticoid receptors in the gill tissue of fish. Gen. Comp. Endocrinol. 53: 353–364.PubMedCrossRefGoogle Scholar
  37. Silvestrini, R., Costa, A., Veroni, S., Del Bino, G. and Persici, P. 1988. Comparative analysis of different approaches to investigate cell kinetics. Cell Tiss. Kinet. 21: 123.Google Scholar
  38. Weatherley, A.P. and Gill, H.S. 1987. The Biology of Fish Growth. Academic Press, New York.Google Scholar
  39. Yao, K., Niu, P., Le Gac, F. and Le Bail, P.Y. 1991. Presence of specific growth hormone binding sites in rainbow trout (Oncorhynchus mykiss) tissues: Characterization of the hepatic receptor. Gen. Comp. Endocrinol. 81: 72–82.PubMedCrossRefGoogle Scholar

Copyright information

© Kugler Publications 1994

Authors and Affiliations

  • Pierre Laurent
    • 1
  • Suzanne Dunel-Erb
    • 1
  • Claudine Chevalier
    • 1
  • Jacques Lignon
    • 1
  1. 1.Laboratoire de Morphologie Fonctionnelle des Adaptations Centre d'Ecologie et de Physiologie EnergétiquesC.N.R.S.Strasbourg CedexFrance

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