17 alpha,20 beta-dihydroxy-4-pregnen-3-one, a maturation-inducing hormone in fish oocytes: mechanisms of synthesis and action.

Meiotic maturation of fish oocytes is induced by the action of maturation-inducing hormone (MIH). 17 alpha,20 beta-Dihydroxy-4-pregnen-3-one (17 alpha,20 beta-DP) was identified as the MIH of several fish species, including salmonid fishes. The interaction of two ovarian follicle cell layers, the thecal and granulosa cell layers, is required for the synthesis of 17 alpha,20 beta-DP; the thecal layer produces 17 alpha-hydroxyprogesterone that is converted to 17 alpha,20 beta-DP in granulosa cells by the action of 20 beta-hydroxysteroid dehydrogenase (20 beta-HSD). The preovulatory surge of LH-like gonadotropin (GTH II) is responsible for rapid expression of 20 beta-HSD mRNA transcripts in granulosa cells. 17 alpha,20 beta-DP acts via a receptor on the plasma membrane of oocytes. A specific 17 alpha,20 beta-DP receptor has been identified and characterized from defolliculated oocytes of several fish species. The concentrations of 17 alpha,20 beta-DP membrane receptor increase immediately prior to oocyte maturation. The pertussis toxin-sensitive inhibitory G protein is involved in the signal transduction pathway of 17 alpha,20 beta-DP. The early steps following 17 alpha,20 beta-DP action involve the formation of the major mediator of this steroid, maturation-promoting factor, which consists of cdc2 kinase (34 kDa) and cyclin B (46-48 kDa). Immature oocytes contain only monomeric 35 kDa cdc2 and do not stockpile cyclin B, although immature oocytes contain mRNA for cyclin B. 17 alpha,20 beta-DP induces oocytes to synthesize cyclin B, which in turn activates preexisting 35 kDa cdc2 through its threonine 161 phosphorylation by a threonine kinase (M015), producing the 34-kDa active cdc2. 17 alpha,20 beta-DP-induced oocyte maturation is blocked by cordycepin, a polyadenylation inhibitor. Furthermore, cyclin B mRNA was polyadenylated during 17 alpha,20 beta-DP-induced oocyte maturation. These findings suggest that 17 alpha,20 beta-DP initiates translation of cyclin B mRNA through cytoplasmic 3' poly(A) elongation.