Skip to main content
Log in

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

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References cited

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Gratzner, H. 1982. Monoclonal antibody against 5-bromo- and 5-iodo-deoxyuridine: a new reagent for detection of DNA replication. Science 218: 474–475.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

  • 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 

  • Laurent, P. and Dunel, S. 1980. Morphology of gill epithelia in fish. Am. J. Physiol. 238 (Regulatory Integrative Comp. Physiol. 7V: R147–R159.

  • Laurent, P. and Hebibi, N. 1989. Gill morphometry and fish osmoregulation. Can. J. Zool. 67: 3055–3063.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Laurent, P. and Perry, S.F. 1991. Environmental effects on fish gill morphology. Physiol. Zool. 64: 4–25.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • MacCormick, J.H. 1990. Cortisol directly stimulates differentiation of chloride cells in Tilapia opercular membrane. Am. J. Physiol. 159: R857–R863.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Madsen, S.S. 1990b. Enhanced hypoosmoregulatory response to growth hormone after cortisol treatment in immature Salmo gairdneri. Fish Physiol. Biochem. 8: 271–279.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Morgan, M. 1974a. The development of gill arches and gill blood vessels of the rainbow trout, Salmo gairdneri. J. Morphol. 142: 351–364.

    Article  Google Scholar 

  • Morgan, M. 1974b. Development of the secondary lamellae of the gills of the trout, Salmo gairdneri. Cell Tiss. Res. 151: 509–523.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sandor, T., DiBatista, J.A. and Medhi, A.Z. 1984. Glucocorticoid receptors in the gill tissue of fish. Gen. Comp. Endocrinol. 53: 353–364.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Weatherley, A.P. and Gill, H.S. 1987. The Biology of Fish Growth. Academic Press, New York.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laurent, P., Dunel-Erb, S., Chevalier, C. et al. Gill epithelial cells kinetics in a freshwater teleost, Oncorhynchus mykiss during adaptation to ion-poor water and hormonal treatments. Fish Physiol Biochem 13, 353–370 (1994). https://doi.org/10.1007/BF00003415

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00003415

Keywords

Navigation