Corticosteroid plasma kinetics and gonadal receptor gene expression during the reproductive cycle in female Eurasian Perch: Investigation of the roles of corticosteroids in vitellogenesis

Eurasian perch, Perca fluviatilis, is a carnivorous fish that has been appreciated by anglers and consumers, particularly in western Europe, and is mainly cultivated in intensive recirculating aquaculture systems (RAS) [1]. These systems allow for a rapid fish growth rate within shorter periods of production year round under optimal human-controlled conditions, notably by controlling both the photoperiod and temperature [2]. However, achieving such productivity with optimal egg quality remains challenging [3]. To better understand the deterioration of reproductive performance in perch in RAS, further information is required regarding the physiological regulation of reproduction in these fish.

One of the known sources of reproductive failure in fish is the internal physiological response to perceived stressors, which is hormonally controlled by corticosteroid hormones. The reported effects of corticosteroids on GnRH and gonadotropin production have led to recent interest in the possible roles of corticosteroids in fish reproduction [4,5]. However, to date, little information is available on the exact roles of these steroids in reproduction in female fish. As an example, no study has reported the variations in the plasma levels of the four main corticosteroids during oogenesis in any teleost thus far. Eurasian perch is a group-synchronous spawner. Its reproductive cycle is initiated with primary oocyte growth, followed by vitellogenesis, and ends with final oocyte maturation (FOM) in preparation for ovulation [6,7]. In yellow perch, Perca flavescens, a percid that is closely phylogenetically related to Eurasian perch, the involvement of four main corticosteroids (11-deoxycorticosterone or DOC, 11-deoxycortisol or 11-D, cortisol or F, and corticosterone or CortS) in FOM induction as maturation-inducing hormones (MIHs) was proposed following some in vitro assays [8,9]. Receptor-binding affinity assays have indeed highlighted the link between corticosteroid receptors (CRs) and FOM [10]. It was revealed that 11-deoxycortisol, corticosterone and, to a higher extent, cortisol are able to transactivate two of the identified CRs, namely, glucocorticoid receptors 1 and 2 (GR1 and GR2, respectively) [11], whereas only DOC and, to a lower extent, cortisol can activate the other identified CR, namely, mineralocorticoid receptor (MR) [12,13]. Interestingly, in vitro studies also showed that DOC and 11-D can bind to MIH receptors on maturing oocytes from spotted seatrout [14]. The latter information and the previous findings in yellow perch were both sufficient to suggest that corticosteroids are MIHs. However, our recent study using domesticated female Eurasian perch revealed that none of the suspected four corticosteroids is actually an MIH, while 17α,20βdihydroxy-4-pregnen-3-one (DHP) seems to fill that role [15]. In available data on the plasma levels of cortisol, the most abundant circulating corticosteroid in teleosts [13], and the plasma levels of 11-D in wild female perch, the highest levels were measured around FOM and spawning, which is the peri-ovulatory period [16]. This does not allow us to completely eliminate other possible roles of these corticosteroids during that period. In addition to possible roles in these final stages, roles of cortisol in vitellogenesis have been proposed in some studies, as cortisol was found to inhibit E2-mediated vitellogenesis in the liver of the rainbow trout Oncorhynchus mykiss by suppressing the expression of hepatic estrogen receptors (ER) via hepatic GR [17]. In contrast, cortisol was found to upregulate hepatic vitellogenin production in the Arctic char Salvelinus alpinus. The physiological effect of cortisol remains species dependent, as it mediates variable stress-coping mechanisms in fish [18]. In domesticated perch, cortisol levels were found to be higher than basal levels (>10 ng/ml) around vitellogenesis [19]. Hence, it is logical to suggest the possible involvement of cortisol in this stage. Finally, at the onset of oogenesis, cortisol has been shown to participate in the endocrine regulation of puberty in eels [20]. Altogether, the current literature suggests that corticosteroids, notably cortisol, may play roles during critical stages of the reproductive cycle in female perch.

In addition to cortisol, three other corticosteroids (11-D, DOC and CortS) are detected in the blood circulation of teleosts, but their levels or even presence highly depend on the fish species and on the reproductive stage [5]. In studies performed on wild female perch, 11-deoxycortisol is usually assessed along with cortisol and is found in detectable levels throughout the reproductive cycle [21]. 11-Deoxycortisol has been previously detected in several other teleosts, such as salmonids [5] and rainbow trout [22]. In fact, 11-deoxycortisol is produced from DOC, and both of these hormones are highly upregulated during reproduction [5,23]. Finally, corticosterone is detected at high levels that fluctuate during the reproductive cycle in elasmobranchs [24], but the variations in corticosterone levels that occur during the reproductive cycle in teleosts are unknown. All the previous information suggests a possible physiological function for these corticosteroids, which might help to overcome the reproductive limitations of teleosts in RAS in the future. The objective of the present study is thus to investigate the involvement of the four main corticosteroids (F, 11-D, DOC, and CortS) in addition to other classical sex hormones of known function (17-beta estradiol (E2), testosterone (T), prostaglandin E2 (PGE2) and DHP) in oogenesis in Eurasian perch. To address this question, i) we measured the plasma levels of these corticosteroids throughout the reproductive cycle, ii) we measured the relative gonadal expression of the CRs identified thus far and some steroidogenic enzymes (17alpha hydroxylase and 11βHSD2), and iii) we investigated the in vitro effects of these corticosteroids on vitellogenesis given the sparse available information on the possible role of these steroids in this step of the reproductive cycle.

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