Abstract
BackgroundLeukocytes are found within the testis of most, if not all, mammals and are involved in immunological surveillance, physiological regulation and tissue remodelling. The testis of seasonal breeding fish undergoes a regression process. In the present study, the second reproductive cycle (RC) of the protandrous seasonal teleost fish, gilthead seabream, was investigated and the presence of leukocytes analysed. Special attention has been paid to the testicular degenerative process which is particularly active in the last stage of the second RC probably due to the immediacy of the sex change process.MethodsSexually mature specimens (n = 10–18 fish/month) were sampled during the second RC. Some specimens were intraperitoneally injected with bromodeoxyuridin (BrdU) before sampling. Light and electron microscopy was used to determine the different stages of gonadal development and the presence of leukocytes and PCR was used to analyse the gene expression of a testis-differentiating gene and of specific markers for macrophages and B and T lymphocytes. Immunocytochemistry and flow cytometry were performed using a specific antibody against acidophilic granulocytes from the gilthead seabream. Cell proliferation was detected by immunocytochemistry using an anti-BrdU antibody and apoptotic cells by in situ detection of DNA fragmentation.ResultsThe fish in the western Mediterranean area developed as males during the first two RCs. The testis of all the specimens during the second RC underwent a degenerative process, which started at post-spawning and was enhanced during the testicular involution stage, when vitellogenic oocytes appeared in the ovary accompanied by a progressive increase in the ovarian index. However, only 40% of specimens were females in the third RC. Leukocytes (acidophilic granulocytes, macrophages and lymphocytes) were present in the gonad and acidophilic granulocyte infiltration occurred during the last two stages. At the same time DMRT1 gene expression decreased.ConclusionsThe results demonstrate that innate and adaptive immune cells are present in the gonads of gilthead seabream. Moreover, the whole fish population underwent a testicular degenerative process prior to sex change, characterized by high rates of apoptosis and necrosis and accompanied by an infiltration of acidophilic granulocytes and a decrease in DMRT1 levels.
Highlights
Leukocytes are found within the testis of most, if not all, mammals and are involved in immunological surveillance, physiological regulation and tissue remodelling
Based on the morphological changes observed in the testicular area, the second reproductive cycle (RC) can be divided into four stages: spermatogenesis, spawning, post-spawning and testicular involution
As regards morphology during the testicular involution stage, the testicular area could be divided into two areas (Fig. 1d): (i) the testicular peripheral area located at the edge of the gonad and formed by a dense tissue with no tubular lumen and a germinal compartment composed of spermatogonia stem cells and some primary spermatogonia cysts, similar to that observed at postspawning (Fig. 1d,e), and (ii) the testicular internal area located next to the efferent duct and the ovary and formed by wide necrotic areas (Fig. 1d, f) composed of cell debris and surrounded by well developed interstitial tissue with large clusters of eosinophilic cells (Fig. 1f)
Summary
Leukocytes are found within the testis of most, if not all, mammals and are involved in immunological surveillance, physiological regulation and tissue remodelling. Leukocytes (macrophages, lymphocytes and mast cells) are found within the testes of most, if not all, mammals and are involved in immunological surveillance, physiological regulation and tissue remodelling [1,2,3,4]. The major focus of gonadal leukocyte research has been mammals, studies in other vertebrates may shed some light on the evolutionary mechanisms involved in the dysregulation of normal gonad physiology. Most of the fish models used to analyze the genes involved in sex determination and differentiation are gonochorism [6]. Sex-determining genes have not been described in fish, some candidates have been proposed [6]. Its expression can be regulated by hormonal treatments that usually succeed in producing phenotypical sex change [8]
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