A period of oocyte growth is followed by a process called oocyte maturation (the resumption of meiosis) which occurs prior to ovulation and is a prerequisite for successful fertilization. Our studies using fish models have revealed that oocyte maturation is a three-step induction process involving gonadotropin (LH), maturation-inducing hormone (MIH), and maturation-promoting factor (MPF). LH acts on the ovarian follicle layer to produce MIH (17α, 20β-dihydroxy-4-pregnen-3-one, 17α, 20β-DP, in most fishes). The interaction of ovarian thecal and granulosa cell layers (two-cell type model), is required for the synthesis of 17α,20β-DP. The dramatic increase in the capacity of postvitellogenic follicles to produce 17α,20β-DP in response to LH is correlated with decreases in P450c17 (P450c17-I) and P450 aromatase (oP450arom) mRNA and increases in the novel form of P450c17 (P450c17-II) and 20β-hydroxysteroid dehydrogenase (20β-HSD) mRNA. Transcription factors such as Ad4BP/SF-1, Foxl2, and CREB may be involved in the regulation of expression of these steroidogenic enzymes. A distinct family of G-protein-coupled membrane-bound MIH receptors has been shown to mediate non-genomic actions of 17α, 20β-DP. The MIH signal induces the de novo synthesis of cyclin B from the stored mRNA, which activates a preexisting 35 kDa cdc2 kinase via phosphorylation of its threonine 161 by cyclin-dependent kinase activating kinase, thus producing the 34 kDa active cdc2 (active MPF). Upon egg activation, MPF is inactivated by degradation of cyclin B. This process is initiated by the 26S proteasome through the first cut in its NH2 terminus at lysine 57.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1440-169X.2008.01019.x

Regulation of oocyte maturation in fish.

Publisher Summary This chapter discusses that the gonads potentiality to produce steroids, and the regulation of the syntheses. The nature, shape, and intensity of a hormonal signal, ready to be received by a target cell, is the result of an intricate series of positive and negative regulations. In the case of hormonal steroids in fish, only some aspects of this complex have been considered. Once a steroid is secreted, several mechanisms may inactivate it before it reaches its target. Little is known of catabolism of sexual steroids in teleosts. Most available data are concerned with the total radioactivity found in tissues after fish are fed labeled steroid. The biological significance of glucuronidation or sulfonation remains to be explored. Although the conjugated steroids are usually considered to be inactive, recent studies attribute a pheromonal role to glucuronides. In other respects, the binding to plasma proteins may lead to a reversible inactivation, although, in mammals, it has been suggested that steroid secretion may be enhanced by the presence of serum steroid-binding proteins. Finally, the conversion of plasma steroids into biologically active metabolites can occur in some target tissues. The actual physiological role of gonadal steroids in fish is discussed with emphasis on gametogenesis.

7 The Gonadal Steroids

The nature of the steroids secreted by gonads of fish differs significantly from those of the mammals. The ‘classical teleost steroids’, oestradiol, testosterone, 11-ketotestosterone and 17,20βP, have been measured in a wide variety of teleosts but do not always reflect biological activities. There is increasing evidence that teleost gonads may produce a number of ‘non-classical steroids’ which may play an important role in their reproductive biology. Such products include metabolites reduced at C5 to 5α or 5β, at C3 to 3α or 3β, or hydroxylated at 6-, 7-, or 21. Conjugation, as either glucuronides or sulphates, may contribute either to localization of action within the gonad or to production of pheromones during the immediate pre-spawning period. Although it is often possible only to measure the steroids for which assays are readily available, it is important to recognize that there may be production of steroids that are not detected by such assays, but which nevertheless play a major role in reproductive activity. In evolutionary terms, the teleost hydroxylases probably originated in the very early fishes and show parallels with their analogues in amphibians and mammals. Gene sequencing may reveal a possible common ancestor for all vertebrate 6, 7 and 11-hydroxylases.

‘Classical’ and ‘non-classical’ reproductive steroids in fish

The most commonly observed reproductivedysfunctions in cultured fish are theunpredictability of final oocyte maturation(FOM) in females, and the diminished volume andquality of sperm in males. Gonadotropin-releasing hormone agonists (GnRHa)have been used extensively in order tostimulate the release of pituitary luteinizinghormone (LH) required to induce FOM, ovulationand spermiation. Because multiple hormonaltreatments are often necessary for a successfulresponse, fish must be monitored and handledextensively, which is labor intensive,stressful to the fish and can often result inbroodstock mortalities. To ameliorate thisproblem, sustained-release delivery systems forGnRHa have been developed during the last twodecades and have been increasingly applied incontrolling reproduction of a variety ofcultured fish. Solid implants of cholesterolor poly[ethylene-vinyl acetate], andbiodegradable microspheres ofpoly[lactide-glycolide] or poly[fatty aciddimer-sebasic acid] release GnRHa for a periodof time (from a few days to many weeks.) GnRHa-delivery systems do not causedesensitization of the pituitary gonadotrophsin fish, and by stimulating a sustainedelevation of plasma LH they induce the naturalprogression of plasma steroid increasesassociated with FOM and spermiation. Thismethod has been used with very encouragingresults in females of more than 40 culturedspecies and has been effective in inducing FOM,ovulation or spawning in fish with synchronous,group-synchronous and asynchronous ovariandevelopment. In males, GnRHa-delivery systemshave been tested in more than 20 species,producing significant increases in miltproduction for up to 5 weeks. Future researchshould focus on the optimization of thistechnology in terms of (a) using the mostpotent GnRHa, (b) identifying the mostappropriate GnRHa release kinetics according tothe reproductive biology of different species,and (c) determining minimum effective doses. Developments in these areas will greatlyenhance the effectiveness and efficiency ofGnRHa-delivery systems, while at the same timereducing their cost thus making them moreaffordable to the aquaculture industry.

P.A. Hardiman

Papers

Hormone changes during ovulation in the rainbow trout (Salmo gairdneri Richardson)