Investigating the Molecular Mechanisms of Oocyte Maturation and Ovulation in Nile Tilapia: A Focus on the Steroidogenic Enzyme Cyp17a2

Previous research has demonstrated the significant role of progestins and glucocorticoids in fish oocyte maturation and ovulation. To further elucidate the molecular mechanisms of these processes, thorough investigations were conducted by using a cyp17a2 mutant in Nile tilapia (Oreochromis niloticus). This study revealed abundant expression of Cyp17a2 in ovarian somatic cells of tilapia. cyp17a2-deficient females exhibited reduced levels of 17,20β-Dihydroxy-4-pregnen-3-one (DHP) and cortisol/cortisone, leading to delayed meiotic initiation and impaired oocyte maturation and spawning activities. Interestingly, supplementation with human chorionic gonadotrophin (hCG), DHP, and cortisol induced germinal vesicle breakdown (GVBD) and promoted the release of oocytes along with follicular cell layers in cyp17a2-/- females. Additionally, cyp17a2-/- and rescued-cyp17a2-/- females showed higher transcription levels of sterodiogenic enzymes for 17β-Estradiol (E2) production compared to spawning wild-type females. Moreover, the decreased Akt phosphorylation caused by cyp17a2 deficiency and inhibitor treatment resulted in a decrease in oocyte maturation induced by hCG. Conversely, activation of the Phosphoinositide 3-kinase/protein kinase B (PI3K-Akt) signaling pathway partially rescued the impairment on oocyte maturation caused by cyp17a2 mutation. Overall, this work provides the functional evidence that supports the hypothesis regarding the significant involvement of Cyp17a2 in DHP and cortisol biosynthesis, thereby facilitating oocyte maturation and ovulation by activating the PI3K-Akt signaling pathway in fish.