Progestin is an essential factor for the initiation of the meiosis in spermatogenetic cells of the eel

Abstract

Meiosis is an indispensable process of sexual reproduction. However, detailed information on the regulatory mechanisms that initiate meiosis is not available. Progestins are important steroids regulating final maturation in male and female vertebrates. In male teleosts, it is known that progestin induces spermiation and sperm maturation. However, a role for progestin in early spermatogenesis or meiosis has not yet been described. In this study, we examined the functions of progestin on the initiation of meiosis in male Japanese eel. A natural progestin in teleost fish 17␣,20␤-dihydroxy-4-pregnen-3-one (DHP) and its receptors were present in the testis at an early stage of spermatogenesis. By using an eel testicular culture system, DHP was shown to induce DNA replication in spermatogonia. Although 11-ketotestosterone, a known initiator of spermatogenesis, also stimulated DNA synthesis in spermatogonia, antibodies against DHP prevented DNA replication when added during the period in which meiosis was initiated. DHP treatment also induced the expression of meiosis-specific markers, such as DmcI and Spo11. Furthermore, Spo11 expression and synaptonemal complexes, specific features of the meiotic prophase, were detected in testicular fragments cultured with DHP in some germ cells that showed morphological characteristics of undifferentiated spermatogonia. We conclude that DHP, a progestin, is an essential factor for the initiation of meiosis.in vitro culture ͉ Japanese eel ͉ spermatogenesis ͉ androgen ͉ Spo11

Suppression subtractive hybridization (SSH) for isolation and characterization of genes related to testicular development in the giant tiger shrimp Penaeus monodon

“…In fish, progestin also plays an important role in spermiation and sperm maturation (10). The effects of 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) in the male Japanese eel were found to induce DNA replication in spermatogonia, but prevent DNA replication at the initiation of meiosis (10).…”

“…In fish, progestin also plays an important role in spermiation and sperm maturation (10). The effects of 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) in the male Japanese eel were found to induce DNA replication in spermatogonia, but prevent DNA replication at the initiation of meiosis (10). Two totally distinct classes of putative membrane-bound progestin receptors have been reported in vertebrates; progestin membrane receptor component (PGMRC; subtypes 1 and 2) and membrane progestin receptors (mPR; subtypes α, β, γ).…”

Trypsin is a multifunctional factor in spermatogenesis

“…We found for example that spermatogonial stem cell renewal is regulated by an estrogen, estradiol-17␤ (E2) (5), that the initiation of spermatogonial proliferation is regulated by an androgen, 11-ketotestosterone (11KT) (3), and that the initiation of meiosis and sperm maturation are regulated by a progestin, 17␣, 20␤-dihydroxy-4-pregnen-3-one (DHP) (6). It is generally accepted that the biological activity of steroid hormones is mediated via changes in the expression of steroid target genes.…”

17,20β-P and cortisol are the main in vitro metabolites of 17-hydroxy-progesterone produced by spermiating testes of Micropogonias furnieri (Desmarest, 1823) (Perciformes: Sciaenidae)

“…The important increase in 17,20β-P levels in blood plasma during the whole spermatogenesis and spermiation stages compared to the undetectable levels at the first development stages sustain the idea that this progestin is involved in the regulation of these two stages of testicular development. It is interesting to note that the presence of 17,20β-P has been considered essential at the beginning of the meiosis process in eels (Miura et al, 2006). This suggests that during the phase in which germ cells enter in meiosis some levels of 17,20β-P are needed to sustain the process and could explain the relative high levels observed in M. furnieri during spermatogenesis.…”

“…The occurrence of a small peak of 17,20β-P at early phases of testes development and the fact that trout non-flagellated germ cells were able to produce 17,20β-P in vitro when its precursor was added (Vizziano et al, 1996), suggested that early events of germ cell development could be regulated by this progestin. Indeed, 17,20β-P has been proposed as a meiosis regulator in the Japanese eel (Miura et al, 2006) and its effect on the proliferation of early spermatogonia in zebrafish was recently demonstrated (Chen et al, 2013). Moreover, membrane progestin receptors type β (mPRβ) were detected in zebrafish spermatogonia and spermatocytes using immunochemistry analyses (Hanna & Zhu, 2009), while receptors type α (mPRα) were already expressed in the Micropogonias undulatus testes in a stage when only spermatogonia and spermatocytes were present (Tubbs et al, 2010).…”