Skip to main content
Log in

Gonadotropic cells in the Atlantic salmon, Salmo salar

An experimental immunocytological, electron microscopical study

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The gonadotropin-producing cells (GTH-cells) in the Atlantic salmon were studied light and electron microscopically before, during and after spawning, and after injections of luteinizing hormone-releasing hormone (LH-RH). The double immunofluorescent technique was applied using rabbit anti-carp GTH as the first antibody. Numerous immunofluorescent cells were observed throughout the pars distalis, but very few in the pars intermedia. These cells are basophilic and PAS-positive, and ultrastructurally classified as globular gonadotropes. Only one gonadotropic cell type could be identified; its size, morphology and fine structure vary considerably. In the same specimen the GTH-cells can be predominantly globular or vesicular in appearance, depending on the reproductive phase of the fish. At spawning and after LH-RH injection, many GTH-cells reach a vacuolar stage; the content of the vacuoles is not immunofluorescent. Another cell type, which resembles GTH-cells in semithin sections, did not show gonadotropic properties; its nature and functional significance are unknown. In addition, the present study revealed an increase in the synthetic and exocytotic activity of prolactin cells after LH-RH injections. It is suggested that LH-RH mediates this effect via LH and eventually via estradiol.

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

  • Abraham, M.: Ultrastructure of the cell types and of the neurosecretory innervation in the pituitary of Mugil cephalus L. from freshwater, the sea, and a hypersaline lagoon. II. The proximal pars distalis. Gen. comp. Endocr. 24, 121–132 (1974)

    Google Scholar 

  • Båge, G., Ekengren, B., Fernholm, B., Fridberg, G.: The pituitary gland of the roach Leuciscus rutilus. I. The rostral pars distalis and its innervation. Acta zool. (Stockh.) 55, 25–45 (1974a)

    Google Scholar 

  • Båge, G., Ekengren, B., Fernholm, B., Fridberg, G.: The pituitary gland of the roach Leuciscus rutilus. II. The proximal pars distalis and its innervation. Acta zool. (Stockh.) 55, 191–204 (1974b)

    Google Scholar 

  • Baker, B.I., Keshavanath, P., Sundararaj, B.I.: The cell-types in the adenohypophysis of the Indian catfish Heteropneustes fossilis (Bloch). Cell Tiss. Res. 148, 347–358 (1974a)

    Google Scholar 

  • Baker, B.I., Leatherland, J.L., Scott, A.P.: The release of secretory products from the corticotrophic cells of Salmo gairdneri in vitro. Cell Tiss. Res. 151, 481–487 (1974b)

    Google Scholar 

  • Ball, J.N., Baker, B.I.: The pituitary gland: anatomy and histophysiology. In: Fish physiology (W.S. Hoar and D.J. Randall, eds.), Vol. II, pp. 1–110 New York-London: Acad. Press 1969

    Google Scholar 

  • Ball, J.N., Ensor, D.M.: Aspects of the action of prolactin on sodium metabolism in cyprinodont fishes. In: La specificité zoologique des hormones hypophysaire et de leur activités. Colloque Intern. Centre Natl. Rech. Sci. (Paris) 1969

  • Batten, T., Ball, J.N., Benjamin, M.: Ultrastructure of the adenohypophysis in the teleost Poecilia latipinna. Cell Tiss. Res. 161, 239–261 (1975)

    Google Scholar 

  • Benjamin, M.: The adenohypophysis of the flounder, Pleuronectes flesus, and the minnow, Phoxinus phoxinus. Cell Tiss. Res. 157, 391–409 (1975)

    Google Scholar 

  • Billard, R., Breton, B., Dubois, M.P.: Immunocytologie et histochimie des cellules gonadotropes et thyréotropes hypophysaires chez la carpe, Cyprinus carpio. C.R. Acad. Sci. (Paris) 272, 981–983 (1971)

    Google Scholar 

  • Burzawa-Gérard, E., Fontaine, Y.A.: Activités biologiques d'un facteur hypophysaire gonadotrope purifié de poisson téléostéen. Gen. comp. Endocr. 5, 87–95 (1965)

    Google Scholar 

  • Burzawa-Gérard, E., Fontaine, Y.A.: The gonadotropins of lower vertebrates. Gen. comp. Endocr., Suppl. 3, 715–728 (1972)

    Google Scholar 

  • Burzawa-Gérard, E., Fontaine, Y.A.: Formation d'une molécule hybride donnée d'une activité gonadotrope sur la grenouille, à partir de la sous-unité α de l'hormone lutéinisante bovine et d'une sous-unité de l'hormone gonadotrope d'un poisson téléostéen. C.R. Acad. Sci. (Paris) 282, 97–100 (1976)

    Google Scholar 

  • Chester Jones, I., Ball, J.N., Sandor, T., Henderson, I.W., Baker, B.I.: The endocrinology of fish. In: Chemical zoology (M. Florkin and B.T. Scheer, eds.), Vol. 8. New York-London: Acad. Press 1973

    Google Scholar 

  • Chestnut, C.W.: The pituitary gland of coho salmon (Oncorhynchus kisutch Walbaum) and its function in gonad maturation and thyroid activity. Ph.D.Thesis, Simon Fraser University, Burnaby, 1–130 (1970)

    Google Scholar 

  • Cook, H., Overbeeke, A.P. van: Ultrastructure of the pituitary gland (pars distalis) in sockeye salmon (Oncorhynchus nerka) during gonad maturation. Z. Zellforsch. 130, 338–350 (1972)

    Google Scholar 

  • Doerr-Schott, J.: Immunohistochemical detection, by light and electron microscopy, of pituitary hormones in cold-blooded vertebrates I. Fish and Amphibians. Gen. comp. Endocr. 28, 487–512 (1976)

    Google Scholar 

  • Donaldson, E.M. Reproductive endocrinology of fishes. Amer. Zool. 13, 909–927 (1973)

    Google Scholar 

  • Egami, N., Ishii, S.: Hypophyseal control of reproductive function in teleost fishes. Gen. comp. Endocr., Suppl. 1, 248–253 (1962)

    Google Scholar 

  • Ekengren, B., Peute, J., Fridberg, G.: The distribution and the nature of the gonadotropic cells in the rostral pars distalis of the Atlantic salmon, Salmo salar. Ann. biol. anim. Bioch. Biophys., in press (1978)

  • Follénius, E.: Ultrastructure des types cellulaires de l'hypophyse de quelques poissons téléostéens. Archs. Anat. micr. Morph. exp. 52, 429–468 (1963)

    Google Scholar 

  • Fontaine, Y.A., Burzawa-Gérard, E.: Esquisse de l'évolution des hormones gonadotropes et thyréotropes des vertébrés. Gen. comp. Endocr. 32, 341–347 (1977)

    Google Scholar 

  • Goos, H.J.Th., Murathanoglu, O.: Localisation of gonadotropin releasing hormone (GRH) in the forebrain and neurohypophysis of the trout (Salmo gairdneri). Cell Tiss. Res. 181, 163–168 (1977)

    Google Scholar 

  • Goos, H.J.Th., Seldenrijk, R., Peute, J.: The gonadotropic cells in the pituitary of the Black Molly, Mollienisia latipinna, and other teleosts, identified by the immunofluorescence technique in normal and androgen-treated animals. Cell Tiss. Res. 167, 211–219 (1976)

    Google Scholar 

  • Holmes, R.L., Ball, J.N.: The pituitary gland: a comparative account. London: Cambridge University Press 1974

    Google Scholar 

  • Hopkins, C.R.: The fine structural localisation of acid phosphatase in the prolactin cell of the teleost pituitary following the stimulation and inhibition of secretory activity. Tiss. and Cell 1 (4) 653–671 (1969)

    Google Scholar 

  • Kaul, S., Vollrath, L.: The goldfish pituitary I. Cytologie. Cell Tiss. Res. 154, 211–230 (1974)

    Google Scholar 

  • Knowles, F., Vollrath, L.: Neurosecretory innervation of the eels Anguilla and Conger. II. The structure and innervation of the pars distalis at different stages of the life-cycle. Phil. Trans. B 250, 329–342 (1966)

    Google Scholar 

  • Lam, T.J., Pandy, S., Nagahama, Y., Hoar, W.S.: Effect of synthetic luteinizing hormone-releasing hormone (LH-RH) on ovulation and pituitary cytology in the goldfish, Carassius auratus. Canad. J. Zool. 54, 816–824 (1976)

    Google Scholar 

  • Leatherland, J.F.: Studies on the structure and ultrastructure of the intact and “methallibure”-treated meso-adenohypophysis of the viviparous teleost Cymatogaster aggregata Gibbons. Z. Zellforsch. 98, 122–134 (1969)

    Google Scholar 

  • Leatherland, J.F.: Structure and ultrastructure of the neurohypophysis in the viviparous teleost, Cymatogaster aggregata Gibbons. Canad. J. Zool. 48, 1087–1091 (1970)

    Google Scholar 

  • Leatherland, J.F.: Histophysiology and innervation of the pituitary gland of the goldfish, Carassius auratus L.: a light and electron microscope investigation. Canad. J. Zool. 50, 835–844 (1972)

    Google Scholar 

  • Leatherland, J.F., Lin, L.: Fine structure of the rostral pars distalis follicle cells in homotransplanted pituitaries of rainbow trout, Salmo gairdneri. Canad. J. Zool. 54, 122–132 (1976)

    Google Scholar 

  • Leatherland, J.F., McKeown, B.A.: Effect of ambient salinity on prolactin and growth hormone secretion and on hydro-mineral regulation in kokanee salmon smolts (Oncorhynchus nerka). J. comp. Physiol. 89, 215–226 (1974)

    Google Scholar 

  • Leatherland, J.F., McKeown, B.A., John, T.M.: Circadian rhythm of plasma prolactin, growth hormone, glucose and free fatty acid in juvenile kokanee salmon, Oncorhynchus nerka. Comp. Biochem. Physiol. 47 A, 821–828 (1974)

    Google Scholar 

  • Leonardelli, J.: Modification des neurones hypothalamiques à LH-RH après injection intraventriculaire de prolactine chez le cobaye. Ann. Endocr. (Paris) 38, 235–242 (1977)

    Google Scholar 

  • Leray, C., Stahl, A.: Le complexe préoptico-neurohypophysaire chez les poissons étudié à l'aide d'un nouveau colorant du neurosécrétat. Rec. Trav. St. Mar. End. Bull. 23, 153–159 (1961)

    Google Scholar 

  • Mattheij, J.A.M.: The gonadotropic cells in the adenohypophysis of the blind Mexican cave fish, Anoptichthys jordani. Z. Zellforsch. 105, 91–106 (1970)

    Google Scholar 

  • McKeown, B.A., Leatherland, J.F.: Fine structure of the adenohypophysis in immature sockeye salmon, Oncorhynchus nerka. Z. Zellforsch. 140, 459–471 (1973)

    Google Scholar 

  • McKeown, B.A., Overbeeke, A.P. van: Immunohistochemical identification of pituitary hormone producing cells in the sockeye salmon (Oncorhynchus nerka, Walbaum). Z. Zellforsch. 112, 350–362 (1971)

    Google Scholar 

  • Nagahama, Y.: Histo-physiological studies on the pituitary gland of some teleost fishes, with special reference to the classification of hormone-producing cells in the adenohypophysis. Bull. Fish. Hokkaido Univ. 21, 1–63 (1973)

    Google Scholar 

  • Nagahama, Y., Nishioka, R.S., Bern, H.A.: Responses of prolactin cells of two euryhaline marine fishes Gillichthys mirabilis and Platichthys stellatus to environmental salinity. Z. Zellforsch. 136, 153–167 (1973)

    Google Scholar 

  • Nagahama, Y., Nishioka, R.S., Bern, H.A., Gunther, R.L.: Control of prolactin secretion in teleosts, with special reference to Gillichthys mirabilis and Tilapia mossambica. Gen. comp. Endocr. 25, 166–188 (1975)

    Google Scholar 

  • Nagahama, Y., Yamamoto, K.: Fine structure of the glandular cells in the adenohypophysis of the kokanee Oncorhynchus nerka. Bull. Fish. Hokkaido Univ. 20, 159–168 (1969)

    Google Scholar 

  • Öztan, N.: The structure of the hypothalamic neurosecretory cells of Zoarces viviparus L. under the conditions of constant dark and light during the reproductive cycle. Z. Zellforsch. 75, 66–82 (1966)

    Google Scholar 

  • Olivereau, M.: Cytologie de l'hypophyse du Cyprin (Carassius auratus L). C.R. Acad. Sci. (Paris) 255, 2007–2009 (1962)

    Google Scholar 

  • Olivereau, M.: Action de la prolactine chez l'Anguille intacte et hypophysectomisée. I. Système hypophyso-thyroidien et pigmentation. Gen. comp. Endocr. 6, 130–143 (1966)

    Google Scholar 

  • Olivereau, M.: Observations sur l'hypophyse de l'Anguille femelle, en particulier lors de la maturation sexuelle. Z. Zellforsch. 80, 286–306 (1967)

    Google Scholar 

  • Olivereau, M.: Etude cytologique de l'hypophyse du Muge, en particulier en relation avec la salinité extérieure. Histochemie 87, 545–561 (1968)

    Google Scholar 

  • Olivereau, M.: Les cellules gonadotropes hypophysaires du Saumon de l'Atlantique: Unicité ou Dualité? Gen. comp. Endocr. 28, 82–95 (1976)

    Google Scholar 

  • Olivereau, M., Fontaine, M.: Etude cytologique de l'hypophyse de l'Anguille femelle mûre. C.R. Soc. Biol. (Paris) 160, 1374–1378 (1966)

    Google Scholar 

  • Olivereau, M., Herlant, M.: Etude de l'hypophyse de l'Anguille mâle au cours de la reproduction. C.R. Soc. Biol. (Paris) 154, 706 (1960)

    Google Scholar 

  • Olivereau, M., Ridgway, G.J.: Cytologie hypophysaire et antigen sérique en relation avec la maturation sexuelle chez Oncorhynchus species. C.R. Acad. Sci. (Paris) 254, 753–755 (1962)

    Google Scholar 

  • Peute, J., Bruyn, M.G.A. de, Seldenrijk, R., Oordt, P.G.W.J. van: Cytophysiology and innervation of gonadotropic cells in the pituitary of the Black Molly (Poecilia latipinna). Cell Tiss. Res. 174, 35–54 (1976)

    Google Scholar 

  • Peute, J., Goos, H.J.Th., Bruyn, M.G.A. de, Oordt, P.G.W.J. van: Ultrastructure and hormone content of the gonadotropic cells of the rainbow trout pituitary during the annual cycle. Ann. Biol. anim. Bioch. Biophys., in press (1978)

  • Sage, M., Bern, H.A.: Cytophysiology of the teleost pituitary. Int. Rev. Cytol. 31, 339–376 (1971)

    Google Scholar 

  • Schreibman, M.P., Leatherland, J.F., McKeown, B.A.: Functional morphology of the teleost pituitary gland. Amer. Zool. 13, 719–742 (1973)

    Google Scholar 

  • Sundararaj, B.I., Anand, T.C., Donaldson, E.M.: Effects of partially purified salmon pituitary gonadotropin on ovarian maintenance, ovulation, and vitellogenesis in the hypophysectomized catfish, Heteropneustes fossilis (Bloch). Gen. comp. Endocr. 18, 102–114 (1972)

    Google Scholar 

  • Weiss, M.: The release of pituitary secretion in the platyfish Xiphophorus maculatus (Guenther). Z. Zellforsch. 68, 783–794 (1965)

    Google Scholar 

  • Zambrano, D.: The nucleus lateralis tuberis system of the gobiid fish Gillichthys mirabilis. III. Functional modifications of the neurons and gonadotropic cells. Gen. comp. Endocr. 17, 164–182 (1971)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The authors are indebted to Dr. N. Johansson and superintendent N. Steffner for generously providing facilities at their institutes in Älvkarleby. They also wish to thank Mrs. Y. Lilliemarck and Mrs. V. Lundin for their skillful technical assistance. The grants made available by the Swedish Natural Science Research Council (No. 2124-037) are also gratefully acknowledged. Thanks are also due to Mrs. S.M. McNab for linguistic assistance

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ekengren, B., Peute, J. & Fridberg, G. Gonadotropic cells in the Atlantic salmon, Salmo salar . Cell Tissue Res. 191, 187–203 (1978). https://doi.org/10.1007/BF00222419

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00222419

Keywords

Navigation