Cell-cell interactions in the testis of teleosts and elasmobranchs.
In this paper we present the state of knowledge on cell-cell interactions in the testis of two groups of anamniote vertebrates--teleosts and elasmobranchs--which include most fish. In these fish, the structural organization of the testis differs fundamentally from that which characterizes amniotes in which the germinal tissue is located in tubules open at both ends and consists of a permanent population of Sertoli cells associated with successive stages of germ cell development. In fish, the spermatogenic unit of testis is the spermatocyst, which corresponds to one germ cell or to a clone of isogenetic germ cells, enclosed by one or several Sertoli cells, which form the wall of the cyst. In fish testis, the Sertoli cells do not represent a permanent population of cells. Although both are of the cystic type, the teleost and elasmobranch testes are differently organized. In elasmobranchs, primary spermatogonia and Sertoli cells lie initially free within the interstitial tissue, before becoming sequestered by a basement membrane; the testis is then composed of a mass of spermatocysts which contain many Sertoli cells, each being associated with a clone of germ cells. In contrast, in teleosts, the cysts are confined to large elongated structures limited by a basement membrane. These structures are either lobules originating under the albuginea or tubules which, in contrast to those of mammals, are anastomosed. In the lobules, the spermatocysts start to develop at the blind end of the lobules and migrate towards the efferent system, whereas in the tubules, the spermatocysts are located against the basement membrane, all along the tubules and do not migrate. In elasmobranchs, unlike teleosts, Leydig cells are either absent from the interstitial tissue or rare and undifferentiated and their role in steroid production is at best marginal. While many studies have focused on topographical and functional interactions between the diverse cell types present in mammalian testis, only a few studies have brought particular attention to these aspects in fish. In fish, like in mammals, testicular cell-cell interactions are based on structural elements and chemical factors. Occasionally, various adhering junctions have been observed, essentially in teleosts, between Sertoli cells, between Sertoli cells and germ cells, between germ cells themselves, and interstitial cells. Furthermore, in some teleost species, using horseradish peroxidase or lanthanum salts, the presence of tight junctions between Sertoli cells has been correlated to the occurrence of a Sertoli barrier. In these species, the barrier develops after meiosis so that only haploid germ cells are shielded from the vascular system. In fish, recent development of techniques which enable the preparation and in vitro culture of enriched populations of testicular cells and of spermatocysts, has allowed investigations on functional aspects of cell-cell interactions. In particular, data have been obtained, in the trout, on the control of spermatogonia proliferation by Sertoli cell-conditioned media and, in the dogfish, on the steroidogenic activity of Sertoli cells, in relation to the differentiation stage of the associated germ cells. Furthermore information exists, in the trout, showing that intratubular macrophages may participate in the re-initiation of spermatogonial proliferation. In conclusion, the cytoarchitecture of fish testis, as compared to that of mammals, presents original features which provide unique opportunities to develop fruitful studies for a better understanding of the complex control mechanisms underlying testicular function in vertebrates.
Loir
M
M
INRA Station de Physiologie des Poissons, Université de Rennes I, Bretagne, France.
Sourdaine
P
P
Mendis-Handagama
S M
SM
Jégou
B
B
D000818:Animals; D002450:Cell Communication; D018940:Elasmobranchii / Q000502:physiology*; D005399:Fishes / Q000502:physiology*; D005854:Germ Cells; D007985:Leydig Cells / Q000502:physiology; D008264:Macrophages / Q000502:physiology; D008297:Male; D012708:Sertoli Cells / Q000502:physiology; D013091:Spermatogenesis; D013737:Testis / Q000166:cytology / Q000502:physiology / Q000648:ultrastructure*