Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo

Cheng, Juanru; Pan, Yu; Yang, Sufang; Wei, Yaochang; Lv, Qiao; Xing, Qinghua; Zhang, Ruimen; Sun, Le; Qin, Guangsheng; Shi, Deshun; Deng, Yanfei

doi:10.1016/j.jsbmb.2021.105944

Cited by 9 publications

(4 citation statements)

References 58 publications

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“…In cattle, Pparg activation blocked follicle development (Ferst et al, 2020). In mammals, Pparg participate in follicular atresia by influencing boxidation of fatty acids, synthesis of cholesterol and sex steroid hormones (Cheng et al, 2021). In this experiment, transcriptome and real-time PCR results showed that Pparg in FO group decreased significantly, and negatively correlated with the serum E2 levels.…”

Section: Growth Performance and Ovarian Development In Spotted Scatmentioning

confidence: 60%

Ovary transcriptomic analysis reveals regulation effects of dietary fish oil on hormone, lipid, and glucose metabolism in female adult spotted scat (Scatophagus argus)

Wang

Liu

et al. 2022

Front. Mar. Sci.

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In the aquaculture industry, fish oil is widely used as a nutritional supplement to promote the gonadal maturation of broodstocks, while the mechanism of fish oil on ovary development remain unclear. Herein, female adult spotted scat (Scatophagus argus) with most ovaries at phase II were fed with diets containing 8% soybean oil (SO) or 8% fish oil (FO) for 60 days. The final average fish body weight was similar between FO and SO groups. The average gonadosomatic index (GSI) of FO group was higher (non-significant) than that of SO group. Finally, the phase IV ovary of the FO and SO groups were 7 and 5 out of 10, respectively. The serum estradiol (E2) level of the FO group was significantly higher than that of the SO group. The proportions of n-3 long-chain polyunsaturated fatty acids (LC-PUFA, such as docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA)) in the ovaries were much higher in the FO group than in the SO group. These results suggest that the maturity level of the FO group is relatively higher than that of the SO group. Transcriptome sequencing was used to detect the ovary gene expression. Comparatively, the ovary transcriptome analysis showed 68 up-regulated and 193 down-regulated genes in the FO group. The expression levels of Jund and Jun necessary for the ovary maturation were up-regulated in the FO group, while Pparγ and Cxcl12, which could inhibit the ovary development, were down-regulated in the FO group. Cyp3a27 coding the enzyme for degrading the estrogen was significantly down-regulated in the FO group and coincided with the increase of its serum E2. Kif5b which could regulate the glucose metabolism was up-regulated in the FO group. Serum insulin level was also increased in the FO group. Additionally, Aldh3a2 and Plin2 related to lipid metabolism were significantly down-regulated in the FO group. Briefly, dietary fish oil can influence the expression of genes related to steroid hormone, glucose and lipid metabolism. This study will clarify the mechanism of dietary fish oil in promoting ovary development in teleost fish.

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Section: Growth Performance and Ovarian Development In Spotted Scatmentioning

confidence: 60%

Ovary transcriptomic analysis reveals regulation effects of dietary fish oil on hormone, lipid, and glucose metabolism in female adult spotted scat (Scatophagus argus)

Wang

Liu

et al. 2022

Front. Mar. Sci.

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“…Follicles with a diameter greater than 8 mm were used to collect follicular uid for E2 and progesterone (P4) assays. Using previously de ned criteria for assessing follicle health, a practical classi cation system was established based on the relative levels of E2 and P4 found in the follicular uid [34,35]. Follicles with an E2/P4 ratio < 1 were classi ed as atretic follicles, while follicles with E2/P4 > 5 were considered healthy follicles.…”

Section: Materials Supplies and Chemicalsmentioning

confidence: 99%

Follicular atresia in buffalo: Cocaine- and Amphetamine-Regulated Transcript (CART) the underlying mechanisms

Chunyan,

Haiying,

Amin

et al. 2024

Preprint

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Background: Atresia, a prevailing phenomenon within the majority of ovarian follicles, is a process regulated by hormone-induced apoptosis and influenced by changes in both endocrine and paracrine factors. Amongthese alterations, granulosa cell (GC) apoptosis is a key mechanism orchestrated through diverse signaling pathways. Cocaine- and amphetamine-regulated transcript (CART) signaling within ovarian GCs has been demonstrated to play a key role in the regulation of follicular atresia in cattle, pigs and sheep. In the present study, we aimed to investigate the potential local regulatory role of CART in the process of GCapoptosis-induced follicular atresia in buffalo, focusing on the modulation of the AKT/GSK3β/β-catenin pathways, the intracellular signaling pathways involved in cell viability. To address our objective, we firstinvestigated the association between CART gene (CARTPT) expression levels and follicular atresia by conducting gene expression analyses for CARTPT and related genes in both healthy and atretic follicles. Next, we investigated the influence of CART supplementation, with or without FSH, on GCestradiol production and apoptosis, exploring its potential regulatory role in the AKT/GSK3β/β-catenin pathways. Results: Our findings revealed increased expression of the CARTPT and BAX genes in atretic follicles, accompanied by decreased levels of AKT, β-catenin, and CYP19A1, compared to those in healthy follicles. Subsequently, CART treatment in the presence of FSH potently inhibited the FSH-induced rise in GC viability by reducing estradiol production and increasing apoptosis. This change was accompanied by an increase in the gene expression levels of both CARTPT and BAX, while the expression levels of AKT and CYP19A1 weresignificantly decreased. Moreover, at the protein level, treatment with CART in the presence of FSH negatively affects the activity of AKT, β-catenin and LEF1, while the activity of GSK3β was enhanced. Conclusion: In conclusion, our study illuminates how CART negatively influences buffalo GC viability by affecting estradiol production and promoting apoptosis—a key factor in follicular atresia. This regulatory mechanism involves modulation of the AKT/GSK3β/β-catenin pathway, providing valuable insights into the intricate mechanisms governing ovarian follicle development and granulosa cell function. These findings have implications for reproductive biology not only for buffalo but also for different species.

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“…As follicular survival and development are energy-dependent processes, intracytoplasmic energy sources are reduced in atretic follicles, resulting in proapoptotic gene expression and biosynthesis. Recently, a metabolomics study of follicular atresia in Chinese buffaloes provided a new understanding of the carbohydrate metabolism underlying follicular atresia [57] . In this study, the researchers reported that follicular atresia results from reduced glycolysis, the TCA cycle, and OXPHOS.…”

Section: Glucose Metabolism At Different Stages Of Folliculogenesismentioning

confidence: 99%

Role of glucose metabolism and signaling pathways at different stages of ovarian folliculogenesis

Zeng

Sui

et al. 2023

Reproductive and Developmental Medicine

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The female ovaries are critical for follicle growth and development in the process known as “folliculogenesis”. This complex process is regulated by various factors, among which the microenvironment around follicles appears to be crucial. According to previous studies, folliculogenesis is an energy-demanding process. In fact, well-balanced follicular energy metabolism is associated with ovarian function and female fertility. Consequently, glucose metabolism has been widely described as the main source of energy during folliculogenesis. Generally, the follicular glucose metabolism profiles change dynamically during follicular development. Metabolic abnormalities during folliculogenesis are associated with aging, primary ovarian insufficiency, and polycystic ovary syndrome, thereby leading to subfertility and infertility in females. The signaling pathways in follicles appear to form a link between glucose metabolism and folliculogenesis. Therefore, a better understanding of glucose metabolism dynamics at different stages of folliculogenesis and the associated signaling pathways will provide potential implications for follicle developmental competence. This review aimed to describe variations in glucose metabolism at different stages of folliculogenesis, provide new insights into glucose metabolic disorder-related diseases, and specifically discuss two major signaling pathways that regulate glucose metabolism during folliculogenesis: phosphatidylinositol 3-kinase, protein kinase B (PI3K-PKB/AKT) and AMP-activated protein kinase (AMPK) signaling pathways.

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Integration of transcriptomics and non-targeted metabolomics reveals the underlying mechanism of follicular atresia in Chinese buffalo

Cited by 9 publications

References 58 publications

Ovary transcriptomic analysis reveals regulation effects of dietary fish oil on hormone, lipid, and glucose metabolism in female adult spotted scat (Scatophagus argus)

Ovary transcriptomic analysis reveals regulation effects of dietary fish oil on hormone, lipid, and glucose metabolism in female adult spotted scat (Scatophagus argus)

Follicular atresia in buffalo: Cocaine- and Amphetamine-Regulated Transcript (CART) the underlying mechanisms

Role of glucose metabolism and signaling pathways at different stages of ovarian folliculogenesis

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