Dataset Information

Expression Patterns and Gonadotropin Regulation of the TGF-β II Receptor (Bmpr2) during Ovarian Development in the Ricefield Eel Monopterus albus.

ABSTRACT: Bmpr2 plays a central role in the regulation of reproductive development in mammals, but its role during ovarian development in fish is still unclear. To ascertain the function of bmpr2 in ovarian development in the ricefield eel, we isolated and characterized the bmpr2 cDNA sequence; the localization of Bmpr2 protein was determined by immunohistochemical staining; and the expression patterns of bmpr2 in ovarian tissue incubated with FSH and hCG in vitro were analyzed. The full-length bmpr2 cDNA was 3311 bp, with 1061 amino acids encoded. Compared to other tissues, bmpr2 was abundantly expressed in the ovary and highly expressed in the early yolk accumulation (EV) stages of the ovary. In addition, a positive signal for Bmpr2 was detected in the cytoplasm of oocytes in primary growth (PG) and EV stages. In vitro, the expression level of gdf9, the ligand of bmpr2, in the 10 ng/mL FSH treatment group was significantly higher after incubation for 4 h than after incubation for different durations. However, bmpr2 expression in the 10 ng/mL FSH treatment group at 2 h, 4 h and 10 h was significantly lower. Importantly, the expression level of bmpr2 and gdf9 in the 100 IU/mL hCG group had similar changes that were significantly decreased at 4 h and 10 h. In summary, Bmpr2 might play a pivotal role in ovarian growth in the ricefield eel, and these results provide a better understanding of the function of bmpr2 in ovarian development and the basic data for further exploration of the regulatory mechanism of gdf9 in oocyte development.

SUBMITTER: He Z

PROVIDER: S-EPMC9739225 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Expression Patterns and Gonadotropin Regulation of the TGF-β II Receptor (Bmpr2) during Ovarian Development in the Ricefield Eel Monopterus albus.

He Zhi Z Zheng Li L Chen Qiqi Q Xiong Sen S He Zhide Z Hu Jiaxiang J Ma Zhijun Z Zhang Qian Q He Jiayang J Ye Lijuan L He Liang L Luo Jie J Gu Xiaobin X Zhang Mingwang M Tang Ziting Z Jiao Yuanyuan Y Pu Yong Y Xiong Jinxin J Gao Kuo K Lai Bolin B Yang Shiyong S Yang Deying D Yan Taiming T

International journal of molecular sciences 20221205 23

Bmpr2 plays a central role in the regulation of reproductive development in mammals, but its role during ovarian development in fish is still unclear. To ascertain the function of bmpr2 in ovarian development in the ricefield eel, we isolated and characterized the bmpr2 cDNA sequence; the localization of Bmpr2 protein was determined by immunohistochemical staining; and the expression patterns of bmpr2 in ovarian tissue incubated with FSH and hCG in vitro were analyzed. The f ...[more]

PMID: 36499673

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Project description:BackgroundThe ricefield eel is a protogynous hermaphroditic Synbranchiform species that changes sex naturally from female to male, which offers an interesting model for studying gonadal (particularly ovarian) differentiation in vertebrates. In the present study, transcriptome sequencing of the gonad of ricefield eel larvae was performed to explore the molecular mechanisms underlying the ovarian differentiation and development.ResultsA total of 301,267,988 clean reads were generated from cDNA libraries of gonadal tissues of ricefield eel larvae at 6, 9, 12, and 20 days post hatching (dph), which contained undifferentiated gonads, differentiating ovaries, ovaries with oogonia, and ovaries with meiotic oocytes, respectively. De-novo assembly of all the clean reads generated a total of 265,896 unigenes with a mean size of 720 bp and a N50 of 1107 bp. RT-qPCR analysis of the developmental expression of 13 gonadal development-related functional genes indicated that RNA-seq data are reliable. Transcriptome data suggest that high expression of female development-related genes and low expression of male development-related genes in the early gonads of ricefield eel larvae participate in the cascade of sex differentiation leading to the final female phenotype. The contrasting expression patterns of genes involved in retinoid acid (RA) synthesis and degradation might result in peak production of RA at 12 dph in the gonad of ricefield eel larvae, and induce molecular events responsible for the initiation of meiosis before the meiotic signs could be observed at 20 dph. In addition, only stra6 but not stra8 could be identified in gonadal transcriptome data of ricefield eel larvae, and the expression pattern of stra6 paralleled those of genes involved in RA synthesis, suggesting that stra6 may be a downstream target of RA and play a role in RA metabolism and/or meiotic initiation in the gonad of ricefield eel larvae.ConclusionsThe present study depicted the first large-scale RNA sequencing of the gonad of ricefield eel larvae, and identified many important functional genes, GO terms and KEGG pathways involved in gonadal development and germ cell meiosis. Results of the present study will facilitate future study on the ovarian differentiation of ricefield eels and other teleosts as well.

Project description:BackgroundThe ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the large-scale artificial breeding. Many studies including transcriptomes of mixed gonadal samples from different individuals have been aimed to elucidate mechanisms underlying the sex change. However, the key physiological factors involved in the initiation of sex change remain to be identified. RESULTS: The present study performed transcriptomic analysis on gonadal samples of different sexual stages obtained through biopsy from the same fish undergoing sex change. A total of 539,764,816 high-quality reads were generated from twelve cDNA libraries of gonadal tissues at female (F), early intersexual (EI), mid-intersexual (MI), and late intersexual (LI) stages of three individual sex-changing fish. Pairwise comparisons between EI and F, MI and EI, and LI and MI identified 886, 319, and 10,767 differentially expressed genes (DEGs), respectively. Realtime quantitative PCR analysis of 12 representative DEGs showed similar expression profiles to those inferred from transcriptome data, suggesting the reliability of RNA-seq data for gene expression analysis. The expression of apoeb, csl2, and enpp2 was dramatically increased and peaked at EI while that of cyp19a1a, wnt4a, fgf16, and foxl2a significantly downregulated from F to EI and remained at very low levels during subsequent development until LI, which suggests that apoeb, csl2, enpp2, cyp19a1a, wnt4a, fgf16, and foxl2a may be closely associated with the initiation of sex change of ricefield eels.ConclusionsCollectively, results of the present study confirmed that the down-regulation of female-related genes, such as cyp19a1a, wnt4a, fgf16, and foxl2a, is important for the sex change of ricefield eels. More importantly, some novel genes, including apoeb, csl2, and enpp2, were shown to be expressed with peak values at EI, which are potentially involved in the initiation of sex change. The present transcriptomic data may provide an important research resource for further unraveling the mechanisms underlying the sex change and testicular development in ricefield eels as well as other teleosts.

Project description:BackgroundAn increasing number of long noncoding RNAs (lncRNAs) have been found to play important roles in sex differentiation and gonad development by regulating gene expression at the epigenetic, transcriptional and posttranscriptional levels. The ricefield eel, Monopterus albus, is a protogynous hermaphroditic fish that undergoes a sequential sex change from female to male. However, the roles of lncRNA in the sex change is unclear.ResultsHerein, we performed RNA sequencing to analyse lncRNA expression patterns in five different stages of M. albus development to investigate the roles of lncRNAs in the sex change process. A total of 12,746 lncRNAs (1503 known lncRNAs and 11,243 new lncRNAs) and 2901 differentially expressed lncRNAs (DE-lncRNAs) were identified in the gonads. The target genes of the DE-lncRNAs included foxo1, foxm1, smad3, foxr1, camk4, ar and tgfb3, which were mainly enriched in signalling pathways related to gonadal development, such as the insulin signalling pathway, MAPK signalling pathway, and calcium signalling pathway. We selected 5 highly expressed DE-lncRNAs (LOC109952131, LOC109953466, LOC109954337, LOC109954360 and LOC109958454) for full length amplification and expression pattern verification. They were all expressed at higher levels in ovaries and intersex gonads than in testes, and exhibited specific time-dependent expression in ovarian tissue incubated with follicle-stimulating hormone (FSH) and human chorionic gonadotropin (hCG). The results of quantitative real-time PCR (qRT-PCR) analysis and a dual-luciferase assay showed that znf207, as the gene targeted by LOC109958454, was expressed in multiple tissues and gonadal developmental stages of M. albus, and its expression was also inhibited by the hormones FSH and hCG.ConclusionsThese results provide new insights into the role of lncRNAs in gonad development, especially regarding natural sex changes in fish, which will be useful for enhancing our understanding of sequential hermaphroditism and sex changes in the ricefield eel (M. albus) and other teleosts.

Project description:BackgroundThe expression and biological functions of circular RNAs (circRNAs) in reproductive organs have been extensively reported. However, it is still unclear whether circRNAs are involved in sex change. To this end, RNA sequencing (RNA-seq) was performed in gonads at 5 sexual stages (ovary, early intersexual stage gonad, middle intersexual stage gonad, late intersexual stage gonad, and testis) of ricefield eel, and the expression profiles and potential functions of circRNAs were studied.ResultsSeven hundred twenty-one circRNAs were identified, and the expression levels of 10 circRNAs were verified by quantitative real-time PCR (qRT-PCR) and found to be in accordance with the RNA-seq data, suggesting that the RNA-seq data were reliable. Then, the sequence length, category, sequence composition and the relationship between the parent genes of the circRNAs were explored. A total of 147 circRNAs were differentially expressed in the sex change process, and GO and KEGG analyses revealed that some differentially expressed (such as novel_circ_0000659, novel_circ_0004005 and novel_circ_0005865) circRNAs were closely involved in sex change. Furthermore, expression pattern analysis demonstrated that both circSnd1 and foxl2 were downregulated in the process of sex change, which was contrary to mal-miR-135b. Finally, dual-luciferase reporter assay and RNA immunoprecipitation showed that circSnd1 and foxl2 can combine with mal-miR-135b and mal-miR-135c. These data revealed that circSnd1 regulates foxl2 expression in the sex change of ricefield eel by acting as a sponge of mal-miR-135b/c.ConclusionOur results are the first to demonstrate that circRNAs have potential effects on sex change in ricefield eel; and circSnd1 could regulate foxl2 expression in the sex change of ricefield eel by acting as a sponge of mal-miR-135b/c. These data will be useful for enhancing our understanding of sequential hermaphroditism and sex change in ricefield eel or other teleosts.

Dataset Information

Expression Patterns and Gonadotropin Regulation of the TGF-β II Receptor (Bmpr2) during Ovarian Development in the Ricefield Eel Monopterus albus.

Publications

Expression Patterns and Gonadotropin Regulation of the TGF-β II Receptor (Bmpr2) during Ovarian Development in the Ricefield Eel <i>Monopterus albus</i>.

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