Abstract
In teleosts, the onset of puberty in females is marked by the appearance of the first wave of pre-vitellogenic (PV) follicles from the pool of primary growth (PG) follicles (follicle activation) in the ovary during sexual maturation. To understand the mechanisms underlying follicle activation and therefore puberty onset, we undertook this transcriptomic study to investigate gene expression profiles in the event. Our analysis revealed a total of 2,027 up-regulated and 859 down-regulated genes during the PG-PV transition. Gene Ontology (GO) analysis showed that in addition to basic cellular functions such as gene transcription, cell differentiation, and cell migration, other biological processes such as steroidogenesis, cell signaling and angiogenesis were also enriched in up-regulated genes; by comparison, some processes were down-regulated including piRNA metabolism, gene silencing and proteolysis. Further Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis identified a variety of signaling pathways that might play pivotal roles in PG-PV transition, including MAPK, TGF-β, Hedgehog, FoxO, VEGF, Jak-STAT, and phosphatidylinositol signaling pathways. Other pathways of particular interest included endocytosis and glycosaminoglycan biosynthesis. We also analyzed expression changes of genes expressed in different compartments viz. oocytes and follicle cells. Interestingly, most oocyte-specific genes remained unchanged in expression during follicle activation whereas a great number of genes specifically expressed in the follicle cells showed significant changes in expression. Overall, this study reported a comprehensive analysis for genes, biological processes and pathways involved in follicle activation, which also marks female puberty onset in the zebrafish when occurring for the first time in sexual maturation.
Highlights
IntroductionIn each mammalian ovarian cycle, a limited number of primordial follicles are recruited to undergo a gonadotropin-independent growth phase (primary and secondary follicles) leading to antral formation (initial recruitment)
In each mammalian ovarian cycle, a limited number of primordial follicles are recruited to undergo a gonadotropin-independent growth phase leading to antral formation
To confirm the RNA sequencing (RNA-seq) result, we evaluated 6 up-regulated genes and 6 downregulated genes using Real-Time Quantitative PCR (RT-qPCR)
Summary
In each mammalian ovarian cycle, a limited number of primordial follicles are recruited to undergo a gonadotropin-independent growth phase (primary and secondary follicles) leading to antral formation (initial recruitment). Studies in different fish species have provided lines of evidence for roles of pituitary hormones especially gonadotropins (FSH and LH), gonadal steroids and growth factors in regulating the event. A classical experiment of hypophysectomy in the goldfish showed an arrest of folliculogenesis at the transition from PG to previtellogenic (PV, the beginning of SG with cortical alveoli) stage without pituitary, strongly suggesting important roles for pituitary hormones in controlling follicle activation [8] This idea has been supported by studies in other species. Recent in vitro studies in the coho salmon (Oncorhynchus kisutch) confirmed the stimulatory effect of 11-KT on PG follicles and their transition to PV follicles These studies provided evidence for sequential roles of androgens and estrogens in early follicle development. IGF-I, but not insulin and leptin, increased the size of eel PG follicles in vitro [14]
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