Gene Expression Networks Underlying Ovarian Development in Wild Largemouth Bass (Micropterus salmoides)

Abstract

BackgroundOocyte maturation in fish involves numerous cell signaling cascades that are activated or inhibited during specific stages of oocyte development. The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation.MethodsTranscriptomic analysis was performed on eight morphologically diverse stages of the ovary, including primary and secondary stages of oocyte growth, ovulation, and atresia. Ovary histology, plasma vitellogenin, 17β-estradiol, and testosterone were also measured to correlate with gene networks.ResultsGlobal expression patterns revealed dramatic differences across ovarian development, with 552 and 2070 genes being differentially expressed during both ovulation and atresia respectively. Gene set enrichment analysis (GSEA) revealed that early primary stages of oocyte growth involved increases in expression of genes involved in pathways of B-cell and T-cell receptor-mediated signaling cascades and fibronectin regulation. These pathways as well as pathways that included adrenergic receptor signaling, sphingolipid metabolism and natural killer cell activation were down-regulated at ovulation. At atresia, down-regulated pathways included gap junction and actin cytoskeleton regulation, gonadotrope and mast cell activation, and vasopressin receptor signaling and up-regulated pathways included oxidative phosphorylation and reactive oxygen species metabolism. Expression targets for luteinizing hormone signaling were low during vitellogenesis but increased 150% at ovulation. Other networks found to play a significant role in oocyte maturation included those with genes regulated by members of the TGF-beta superfamily (activins, inhibins, bone morphogenic protein 7 and growth differentiation factor 9), neuregulin 1, retinoid X receptor, and nerve growth factor family.ConclusionsThis study offers novel insight into the gene networks underlying vitellogenesis, ovulation and atresia and generates new hypotheses about the cellular pathways regulating oocyte maturation.

Global differential gene expression in the pituitary gland and the ovaries of pre- and postpubertal Brahman heifers

“…An increase of GABA transporters' activity at the onset of puberty might decrease GABA concentration in stalk-median eminence (Terasawa, 2005). Not only expressed in mammalian central nervous system, GABA and GABA receptors have also been demonstrated in relatively high concentration in the human ovary, rat ovary, and rat fallopian tube as well as other mammalian reproductive tissues (Martin del Rio and Caballero, 1980;Erdö and László, 1984;Akinci and Schofield, 1999;Biggs et al, 2013;Martyniuk et al, 2013). Our study was the first to reveal the expression of GAT2 in B. indicus ovaries.…”

Dietary exposure of 17-alpha ethinylestradiol modulates physiological endpoints and gene signaling pathways in female largemouth bass (Micropterus salmoides)

“…3) and contained oocytes in earlier stages of development (primary growth). At the initiation of the experiment, all fish were presumed to be in the late stages of vitellogenesis, based on the water temperature and month (March) (Martyniuk et al 2013). These data suggest that the long term feeding of EE2 may cause a shutdown of steroidogenesis and oocyte growth in the ovary.…”

“…Enrichment analysis in Pathway Studio V9 was performed by gene set enrichment analysis (GSEA) and sub-network enrichment analysis (SNEA) algorithms using the Mann-Whitney test with an alpha level of p< 0.05 (Kotelnikova et al 2012; Sivachenko et al 2007; Sivachenko et al 2005; Subramanian et al 2005). Recently these approaches have been applied to studies conducted in LMB (Doyle et al 2013; Martyniuk et al 2013). GSEA is an analytical method used to evaluate microarray data at the level of gene sets.…”

Effects of short-term exposure to the model anti-androgen, flutamide on reproductive function based endpoints in female Murray rainbowfish (Melanotaenia fluviatilis)

“…Recently, molecular studies revealed altered expression of genes involved in activin signalling in sexually mature zebrafish after treatment with 1750 mg/L of flutamide for 96 h (MartinovicWeigelt et al, 2011). Activins have been known to play an important role in the process of oocyte maturation (Martyniuk et al, 2013;Pang and Ge, 1999). Similar studies in Murray rainbowfish can provide better understanding on the molecular basis of ovarian histopathological changes revealed after flutamide exposure.…”