The expression of nuclear and membrane estrogen receptors in the European eel throughout spermatogenesis

Abstract

Estradiol (E) can bind to nuclear estrogen receptors (ESR) or membrane estrogen receptors (GPER). While mammals possess two nuclear ESRs and one membrane GPER, the European eel, like most other teleosts, has three nuclear ESRs and two membrane GPERs, as the result of a teleost specific genome duplication. In the current study, the expression of the three nuclear ESRs (ESR1, ESR2a and ESR2b) and the two membrane GPERs (GPERa and GPERb) in the brain-pituitary-gonad (BPG) axis of the European eel was measured, throughout spermatogenesis. The eels were first transferred from freshwater (FW) to seawater (SW), inducing parallel increases in E plasma levels and the expression of ESRs. This indicates that salinity has a stimulatory effect on the E signalling pathway along the BPG axis. Stimulation of sexual maturation by weekly injections of human chorionic gonadotropin (hCG) induced a progressive decrease in E plasma levels, and different patterns of expression of ESRs and GPERs in the BPG axis. The expression of nuclear ESRs increased in some parts of the brain, suggesting a possible upregulation due to a local production of E. In the testis, the highest expression levels of the nuclear ESRs were observed at the beginning of spermatogenesis, possibly mediating the role of E as spermatogonia renewal factor, followed by a sharply decrease in the expression of ESRs. Conversely, there was a marked increase observed in the expression of both membrane GPERs throughout spermatogenesis, suggesting they play a major role in the final stages of spermatogenesis.

Transcriptome profiling of laser-captured germ cells and functional characterization of zbtb40 during 17alpha-methyltestosterone-induced spermatogenesis in orange-spotted grouper (Epinephelus coioides)

“…the proliferation of gonocyte and spermatogonia, spermiation, sperm transport, and epididymal sperm maturation [26]. In eels, estrogen receptors are also expressed in the testis and are required for spermatogonial renewal [27,28]. The high expression of estrogen receptors suggest that estrogen signals are also needed for spermatogenesis in grouper.…”

Development of innovative methods for induction of European eel (Anguilla anguilla) spermatogenesis

“…Although speculative, this could indicate a weakening of dopamine-mediated neuroendocrine inhibition of eel puberty. The pituitary is a major target for estrogen in European eel (Morini et al 2017b). In our data, esr1 expression increased significantly in the pituitary after the T10 treatment (Fig.…”

“…Furthermore, higher plasma androgen levels have been correlated with European eel SPGA proliferation in previous studies (Peñaranda et al 2016). As mentioned above, increases in steroid levels have been reported in European eel after salinity acclimation (Morini et al 2017b;Peñaranda et al 2016;Baeza et al 2014); however, the duration of these increases has not been reported.…”

“…26). This result may suggest stimulation of maturation, as the expression of esr1 has been shown to increase in the pituitary of European eel males early on in artificial maturation (Morini et al 2017b).…”

“…Although estrogens and specifically estradiol-17β (E2) are commonly associated with female vertebrates, it has shown strong presence and importance in male teleost as well (Miura et al 1999;Amer et al 2001). As seen for T, E2 also increased in European eel males as a response to saltwater acclimation (Morini et al 2017b), and T and E2 have been shown to affect GnRH levels in European eel brain and pituitary (Montero et al 1995). In Japanese eels, E2 has been shown to stimulate mitotic divisions in the testis and thus induce spermatogonia stem cell renewal (Miura et al 1999).…”