Abstract
Spermatogenesis is a unique developmental sequence involving multiple cell to cell interactions and several categories of regulatory molecules. In contrast to conventional mammalian models in which testicular organization is highly complex, the testis of the dogfish shark Squalus acanthias is technically advantageous for elucidating stage-dependent structural and functional charactericsics and for in vitro regulatory studies. Using incorporation of [3H]thymidine into acid-insoluble molecules as a measure of DNA synthesis by spermatocysts (germ cell/Sertoli cell units) of premeiotic stages, we obtained evidence of a growth inhibitory bioactivity (chalone) within the testis. This activity is differentially distributed (postmeiotic > meiotic > premeiotic), suggesting that more advanced developmental stages, which are upstream in the vascular pathway within the testis, may control the size of the proliferating spermatocyst population and, hence, the advance of less mature stages. These data provide direct evidence for humoral communication between stages of spermatogenesis.
Resumé
La spermatogenèse est un processus original du développement impliquant, dans sa régulation, des multiples interactions cellulaires et des molécules de différentes familles. A l'opposé des modèles biologiques mammaliens conventionnels, pour lesquels l'organisation testiculaire est très complexe, le testicule de l'aiguillat, Squalus acanthias, offre des avantages méthodologiques pour la caractérisation structurale et fonctionnelle des stades de développement, et la mise en oeuvre d'études de régulation in vitro. En utilisant l'incorporation d'[3H]thymidine dans la fraction acido-précipitable comme estimation de synthèse d'ADN par des spermatocystes (unités cellules germinales/cellules de Sertoli) prémeïotiques, nous avons mis en évidence l'existence d'une activité inhibitrice testiculaire de croissance (chalone). Cette activité est distribuée de manière différentielle entre stades: postmeïotique > meïotique > prémeïotique; ce qui suggère que les stades de développement les plus avancés, stades situés en amont de la vascularisation testiculaire, peuvent contrôler la taille de la population proliférante de spermatocystes et, de là, le développment de stades plus précoces. Ces résultats apportent l'évidence directe d'une communication humorale entre stades spermatogénétiques.
Similar content being viewed by others
References cited
Arrau, J., Bustos-Obregón, E. and Cabello, R. 1988. Inhibition of growth and differentiation of fetal hamster gonads grafted into the adult testis. Int. J. Androl. 11: 327–338.
Bellve, A.R. and Zheng, W. 1989. Growth factors as autocrine and paracrine modulators of male gonadal functions. J. Reprod. Fertil. 85: 771–793.
Betka, M., Haverly, J.E. and Callard, G.V. 1991. Quantitative and qualitative analysis of spermatocyst proteins during spermatogenesis. J. Cell Biol. 115: 50a.
Bullough, W.S. 1967. The Evolution of Differentiation. Academic Press, London, 206 pp.
Bustos-Obregón, E. 1989. G1 spermatogonial chalone. Arch. Biol. Med. Exp. Santiago. 22: 15–23.
Callard, G.V. 1991a. Spermatogenesis. In Vertebrate Endocrinology: Fundamentals and Biomedical Implications. Vol. 4, part A. pp. 104–154. Edited by P. Pang and M.S. Schreibman. Academic Press, San Diego.
Callard, G.V. 1991b. Reproduction in male elasmobranch fishes. In Oogenesis, Spermatogenesis and Reproduction. pp. 104–154. Edited by R.K.H. Kinne, E. Kinne-Saffran and K.W. Beyenbach. Karger, Basel.
Callard, G.V. and DuBois, W. 1988. Methods for isolation and culture of staged spermatogenic lobules and staged Sertoli cells from dogfish testis. Bull. Mount Desert Island Biol. Lab. 27: 30–32.
Callard, G.V., Pudney, J.A., Mak, P. and Canick, J. 1985. Stage-dependent changes in steroidogenic enzymes and estrogen receptors during spermatogenesis in the testis of the dogfish, Squalus acanthias. Endocrinology 117: 1328–1335.
Clarke, Ch.L. and Sutherland, R.L. 1990. Progestin regulation of cellular proliferation. Endocr. Rev. 11: 266–301.
Clermont, Y. and Mauger, A. 1974. Existence of a spermatogonial chalone in the rat testis. Cell Tiss. Kinet. 7: 165–172.
Cuevas, M.E. and Callard, G.V. 1992a. Androgen and progesterone receptors in shark (Squalus) testis: characteristics and stage-related distribution. Endocrinology 130: 2173–2182.
Cuevas, M.E. and Callard, G.V. 1992b. In vitro steroid secretion by staged spermatocysts (Sertoli/germ cell units) of dogfish (Squalus acanthias) testis. Gen. Comp. Endocrinol. 88: 151–165.
Cuevas, M.E., Miller, W. and Callard, G.V. 1992. Sulfoconjugation of steroids and the vascular pathway of communication in dogfish testis. J. Exp. Zool. 264: 119–129.
Dissell-Emiliani, F.M.F., Grootenhuis, A.J., deJong, F.H. and deRooij, D.G. 1989. Inhibin reduces spermatogonial numbers of testes of adult mice and chinese hamsters. Endocrinology 125: 1899–1903.
DuBois, W., Mak, P. and Callard, G.V. 1989. Sertoli cell functions during spermatogenesis: the shark testis model. Fish Physiol. Biochem. 7: 221–227.
DuBois, W. and Callard, G.V. 1991. Culture of intact Sertoli/germ cell units and isolated Sertoli cells from Squalus testis: I. Evidence of stage-related functions in vitro. J. Exp. Zool. 258: 359–372.
Haverly, J.E., Betka, M. and Callard, G.V. 1991. Stage-dependency of gelatinolytic proteinase activities during spermatogenesis. Am. Zool. 31: 67A.
Holstein, A.F. 1969. Zur frage der lokalen steuerung der spermatogenese beim dornhai (Squalus acanthias L.). Z. Zellforsch. Mikrosko Anato 93: 265–281.
Martinova, Y., Zheng, W. and Bellve, A.R. 1991. Seminiferous growth factor stimulates DNA synthesis in spermatogonial stem cell. 31st Ann. Mtg. Am. Soc. Cell Biol., Boston.
Mather, J.P., Attie, K.M., Woodruff, T.K., Rice, G.C. and Phillips, D.M. 1990. Activin stimulates spermatogonial proliferation in germ cell-Sertoli cell cocultures from immature rat testis. Endocrinology 127: 3206–3214.
Parvinen, W., Soder, O., Mali, P., Froysa, B. and Ritzen, E.M. 1991a. In vitro stimulation of stage-specific DNA synthesis in rat seminiferous segments by interleukin-1α. Endocrinology 129: 1614–1620.
Parvinen, W., Pelto-Huikko, M., Soder, O., Schultz, R., Kaipia, A., Mali, P., Toppari, J., Lonnerberg, P., Ritzen, E.M., Ebendal, T., Olson, L., Hokfelt, T. and Person, H. 1991b. Expression of β-nerve growth factor and its receptor in rat seminiferous epithelium: specific function at the onset of meiosis. J. Cell Biol. 117: 629–641.
Piferrer, F. and Callard, G.V. 1992. Paracrine regulation of premeiotic germ cell proliferation in the testis of the spiny dogfish, Squalus acanthias. Bull. Mount Desert Island Biol. Lab. 31: 49–50.
Pudney, J. and Callard, G.V. 1984a. Development of the agranular endoplasmic reticulum in the Sertoli cells of the shark (Squalus acanthias) during spermatogenesis. Anat. Rec. 209: 311–321.
Pudney, J. and Callard, G.V. 1984b. Identification of Leydig-like cells in the sterstitium of the shark testis (Squalus acanthias). Anat. Rec. 209: 321–330.
Redding, J.M., DuBois, W. and Callard, G.V. 1990. Regulation of DNA synthesis in cultured spermatocysts (Sertoli/germ cell units) from dogfish testis. Am. Zool. 30.
Redding, J.M. and Callard, G.V. 1991. Regulation of DNA and protein synthesis in the dogfish (Squalus acanthias testis. Bull. Mount Desert Island Biol. Lab. 30: 30–32.
Setchell, B.P. 1984. The Mammalian Testis. Cornell Univ. Press, Ithaca.
Skinner, M.K. 1991. Cell-cell interactions in the testis. End. Rev. 12: 45–77.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Piferrer, F., Redding, M., DuBois, W. et al. Stimulatory and inhibitory regulation of DNA synthesis during spermatogenesis: studies in Squalus acanthias . Fish Physiol Biochem 11, 293–298 (1993). https://doi.org/10.1007/BF00004578
Issue Date:
DOI: https://doi.org/10.1007/BF00004578