Insufficiency of melatonin in follicular fluid is a reversible cause for advanced maternal age-related aneuploidy in oocytes

Zhang, Mianqun; Lu, Yajuan; Chen, Ying; Zhang, Yu; Xiong, Bo

doi:10.1016/j.redox.2019.101327

Cited by 56 publications

(36 citation statements)

References 40 publications

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“…Regarding the influence of maternal age on antioxidants, we found that only melatonin levels were significantly affected during the first month of breastfeeding, also confirmed by the linear model. Maternal age is one of the main factors limiting antioxidant production in humans, as established by previous studies, and extensively demonstrated for melatonin [49,50]. Melatonin levels in plasma are known to decline with age [51] and plasma concentrations match those found in BM [38].…”

Section: Discussionmentioning

confidence: 61%

Influence of Maternal Age and Gestational Age on Breast Milk Antioxidants During the First Month of Lactation

et al. 2020

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Breast milk (BM) is beneficial due to its content in a wide range of different antioxidants, particularly relevant for preterm infants, who are at higher risk of oxidative stress. We hypothesize that BM antioxidants are adapted to gestational age and are negatively influenced by maternal age. Fifty breastfeeding women from two hospitals (Madrid, Spain) provided BM samples at days 7, 14 and 28 of lactation to assess total antioxidant capacity (ABTS), thiol groups, reduced glutathione (GSH), superoxide dismutase (SOD) and catalase activities, lipid peroxidation (malondialdehyde, MDA + 4-Hydroxy-Trans-2-Nonenal, HNE), protein oxidation (carbonyl groups) (spectrophotometry) and melatonin (ELISA). Mixed random-effects linear regression models were used to study the influence of maternal and gestational ages on BM antioxidants, adjusted by days of lactation. Regression models evidenced a negative association between maternal age and BM melatonin levels (β = −7.4 ± 2.5; p-value = 0.005); and a negative association between gestational age and BM total antioxidant capacity (β = −0.008 ± 0.003; p-value = 0.006), SOD activity (β = −0.002 ± 0.001; p-value = 0.043) and protein oxidation (β = −0.22 ± 0.07; p-value = 0.001). In conclusion, BM antioxidants are adapted to gestational age providing higher levels to infants with lower degree of maturation; maternal ageing has a negative influence on melatonin, a key antioxidant hormone.

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Section: Discussionmentioning

confidence: 61%

Influence of Maternal Age and Gestational Age on Breast Milk Antioxidants During the First Month of Lactation

et al. 2020

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“…Studies have found that preovulatory follicular fluid contains high levels of MLT 44 ; oocytes synthesize MLT through mitochondria to resist free radical 45 ; MT1…”

Section: This Study Indicated That the Ovary Is Another Organ That Sementioning

confidence: 99%

Melatonin as an endogenous hormone to slow down the exhaustion of ovarian follicle reserve in mice–a novel insight into its roles in early folliculogenesis and ovarian aging

Yang¹,

Liu²,

Chen³

et al. 2020

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Previous studies have shown that long-term intake of exogenous melatonin can effectively delay ovarian aging, but the mechanism has not been fully elucidated. We observed that SNAT, the rate-limiting enzyme in the melatonin synthetic pathway, is localized in primordial and early follicle, and that granulosa cells isolated from follicle can synthesize melatonin. In vitro cultured neonatal mice ovaries with melatonin inhibited primordial follicle activation and early follicle growth. In vivo experiments further indicated that daily injections of melatonin to neonatal mice during the primordial follicle activation phase can reduce the number of activated follicles by inhibiting the PI3K-AKT-FOXO3 pathway; during the early follicle growth phase, injections of melatonin significantly suppressed early follicle growth and atresia, and transcriptome data showed that multiple pathways involved in folliculogenesis, including PI3K-AKT, were suppressed. Further, SNAT knockout in mice resulted in a significant increase in follicle activation and atresia, and eventually accelerated ovarian aging. We also demonstrated that prolonged high-dose melatonin intake had no obvious adverse effect on the health condition of mice. This study confirms that endogenous melatonin is involved in the regulation of ovarian aging, and reveals that melatonin delays ovarian aging by inhibiting primordial follicle activation, early follicle growth and atresia.

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“…in vitro oocyte maturation (IVM) is one of the multiple steps of IVP that the oocytes are recovered directly from the follicles and are cultured in a specific condition. Despite its advancement, incomparable in vitro and in vivo environment is still a major problem contributing to the success of IVM performance [2,3]. During in vivo oocyte development, several delicate substances and hormones are locally secreted in follicular fluid by ovarian and granulosa cells to nourish oocytes.…”

mentioning

confidence: 99%

“…During in vivo oocyte development, several delicate substances and hormones are locally secreted in follicular fluid by ovarian and granulosa cells to nourish oocytes. This includes melatonin which was widely studied for its contribution to oocyte quality [2][3][4][5]. Melatonin was most recognized for its scavenging function on reactive oxygen species (ROS).…”

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confidence: 99%

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Novel classifier orthologs of bovine and human oocytes matured in different melatonin environments

et al. 2020

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It has been demonstrated that melatonin influences the developmental competence of both in vivo and in vitro matured oocytes. It modulates oocyte-specific gene expression patterns among mammalian species. Due to differences among study systems, the identification of the classifier orthologs-the homologous genes related among mammals that could universally categorize oocytes matured in environments with varied melatonin levels is still limitedly studied. To gain insight into such orthologs, cross-species transcription profiling meta-analysis of in vitro matured bovine oocytes and in vivo matured human oocytes in low and high melatonin environments was demonstrated in the current study. RNA-Seq data of bovine and human oocytes were retrieved from the Sequence Read Archive database and pre-processed. The used datasets of bovine oocytes obtained from culturing in the absence of melatonin and human oocytes from old patients were regarded as oocytes in the low melatonin environment (Low). Datasets from bovine oocytes cultured in 10-9 M melatonin and human oocytes from young patients were considered as oocytes in the high melatonin environment (High). Candidate orthologs differentially expressed between Low and High melatonin environments were selected by a linear model, and were further verified by Zero-inflated regression analysis. Support Vector Machine (SVM) was applied to determine the potentials of the verified orthologs as classifiers of melatonin environments. According to the acquired results, linear model analysis identified 284 candidate orthologs differentially expressed between Low and High melatonin environments. Among them, only 15 candidate orthologs were verified by Zero-inflated regression analysis (FDR ≤ 0.05). Utilization of the verified orthologs as classifiers in SVM resulted in the precise classification of oocyte learning datasets according to their melatonin environments (Misclassification rates < 0.18, area under curves > 0.9). In conclusion, the cross-species RNA-Seq meta-analysis to identify novel classifier orthologs of matured oocytes under different melatonin environments was successfully demonstrated in this study-delivering candidate orthologs for future studies at biological levels. Such verified orthologs might provide valuable evidence about melatonin sufficiency in target oocytes-by which, the decision on melatonin supplementation could be implied.

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Insufficiency of melatonin in follicular fluid is a reversible cause for advanced maternal age-related aneuploidy in oocytes

Cited by 56 publications

References 40 publications

Influence of Maternal Age and Gestational Age on Breast Milk Antioxidants During the First Month of Lactation

Influence of Maternal Age and Gestational Age on Breast Milk Antioxidants During the First Month of Lactation

Melatonin as an endogenous hormone to slow down the exhaustion of ovarian follicle reserve in mice–a novel insight into its roles in early folliculogenesis and ovarian aging

Novel classifier orthologs of bovine and human oocytes matured in different melatonin environments

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