The protective role of melatonin in porcine oocyte meiotic failure caused by the exposure to benzo(a)pyrene

Miao, Yun; Zhou, Changyin; Bai, Qingyun; Cui, Zhaokang; ShiYang, Xiayan; Lu, Yajuan; Zhang, Mianqun; Dai, Xinbin; Xiong, Bo

doi:10.1093/humrep/dex331

Cited by 65 publications

(53 citation statements)

References 35 publications

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“…Melatonin has important physiological functions, such as the control of circadian rhythms, decrease in oral temperature, regulation of follicular development and reproductive activity, and activation of the immune system . Previous research reports found that melatonin exerts a protective function in mouse oocytes and porcine oocytes . Our results agree with previous studies which suggest that melatonin plays an important role in steroid hormone synthesis of GCs, however, the mechanism underlying how melatonin affects steroid hormone synthesis in GCs is unclear.…”

Section: Discussionsupporting

confidence: 90%

Effects of melatonin on the synthesis of estradiol and gene expression in pig granulosa cells

Liu

Yang

et al. 2019

Journal of Pineal Research

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The interaction of granulosa cells (GCs) with oocytes is important to regulate follicle development. The exogenous melatonin promoting the maturation of oocytes by GCs has been approved in pig, however, the transcriptome profile and the functions of the genes regulated by melatonin in GCs have not yet to be fully characterized. In this study, we found melatonin could stimulate the synthesis of estradiol in pig GCs. The RNA‐seq was used to explore the effects of melatonin on gene expression, a total of 89 differentially expressed genes (DEGs) were identified. Gene ontology analysis showed DEGs which associated with regulation of cell proliferation, cell cycle, and anti‐apoptosis were significantly enriched. The functions of two DEGs, NOTCH2 and FILIP1L, were studied in pig GCs. The results showed that NOTCH2 inhibited the synthesis of estradiol, but FILIP1L promoted the synthesis of estradiol. Furthermore, inhibiting NOTCH2 in granulosa cells cocultured with cumulus‐oocyte‐complexes had no obvious effect on the maturation of pig oocyte, but could upregulate the cleavage rate of oocyte. We proved that FILIP1L had no effect on the maturation and cleavage of pig oocytes. Our work deepens the understanding of melatonin's effects on GCs and oocyte. The DEGs we found will be beneficial to reveal mechanisms of melatonin acting on GCs and oocytes and design the pharmacological interventions.

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Section: Discussionsupporting

confidence: 90%

Effects of melatonin on the synthesis of estradiol and gene expression in pig granulosa cells

Liu

Yang

et al. 2019

Journal of Pineal Research

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“…Paraquat exposure causes abnormal distribution patterns of mitochondria in in vitro bovine oocytes, and melatonin treatment improves mitochondrial functionality of the oocytes exposed to paraquat during IVM in the bovine [42]. IVM medium supplemented with melatonin can alter mitochondrial distribution patterns of oocytes, but do not affect mitochondrial activity of bovine oocytes [43], and defective mitochondrion integrity induced by benzo(a)pyrene can be recovered by melatonin treatment via inhibiting ROS level in the porcine oocytes [34]. Therefore, melatonin can enhance mitochondrial distribution of oocytes during IVM, which is helpful for functions and development competence of in vitro oocytes.…”

Section: Discussionmentioning

confidence: 99%

“…Melatonin achieves its detoxification of reactive oxygen through inducing antioxidant enzymes [33]. Benzo(a)pyrene leads to oocyte meiotic failure, which can be recovered by melatonin supplementation through repressing ROS level in the porcine [34]. Melatonin combined with prolonged IVM enhances development of poor-quality oocytes through decreasing ROS generation in pigs [35].…”

Section: Discussionmentioning

confidence: 99%

Effect of Melatonin on the In Vitro Maturation of Porcine Oocytes, Development of Parthenogenetically Activated Embryos, and Expression of Genes Related to the Oocyte Developmental Capability

Yang

Wang

Cui

et al. 2020

Animals

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Melatonin treatment can improve quality and in vitro development of porcine oocytes, but the mechanism of improving quality and developmental competence is not fully understood. In this study, porcine cumulus–oocyte complexes were cultured in TCM199 medium with non-treated (control), 10−5 M luzindole (melatonin receptor antagonist), 10−5 M melatonin, and melatonin + luzindole during in vitro maturation, and parthenogenetically activated (PA) embryos were treated with nothing (control), or 10−5 M melatonin. Cumulus oophorus expansion, oocyte survival rate, first polar body extrusion rate, mitochondrial distribution, and intracellular levels of reactive oxygen species (ROS) and glutathione of oocytes, and cleavage rate and blastocyst rate of the PA embryos were assessed. In addition, expression of growth differentiation factor 9 (GDF9), tumor protein p53 (P53), BCL2 associated X protein (BAX), catalase (CAT), and bone morphogenetic protein 15 (BMP15) were analyzed by real-time quantitative PCR. The results revealed that melatonin treatment not only improved the first polar body extrusion rate and cumulus expansion of oocytes via melatonin receptors, but also enhanced the rates of cleavage and blastocyst formation of PA embryos. Additionally, melatonin treatment significantly increased intraooplasmic level of glutathione independently of melatonin receptors. Furthermore, melatonin supplementation not only significantly enhanced mitochondrial distribution and relative abundances of BMP15 and CAT mRNA, but also decreased intracellular level of ROS and relative abundances of P53 and BAX mRNA of the oocytes. In conclusion, melatonin enhanced the quality and in vitro development of porcine oocytes, which may be related to antioxidant and anti-apoptotic mechanisms.

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“…This study also provides a warning for women who are frequently exposed to IBP at high concentrations by using in vitro culture model of porcine cumulus oocyte complexes as can be seen in Figure . The reason we chose porcine oocytes as a model because oocyte size and maturation time are more like human than mouse (Santos et al ), and several articles have used porcine cumulus oocyte complexes to evaluate oocyte (Liu et al ; Han et al ; Wang et al ; Miao et al ; Liang et al ).…”

Section: Discussionmentioning

confidence: 99%

Isobutylparaben Negatively Affects Porcine Oocyte Maturation Through Increasing Oxidative Stress and Cytoskeletal Abnormalities

Meng

Jiao

Chen

et al. 2020

Environ and Mol Mutagen

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As a member of parabens (PBs), Isobutylparaben (IBP) has a broad-spectrum antimicrobial activity and widely used in personal care products and cosmetics. Recent studies have indicated that usage of IBP poses a potential threat to reproductive health. In this study, we aimed to reveal the effects of acute exposure to IBP on the meiotic maturation of porcine cumulus oocyte complexes. Initial study showed that 200 μM of IBP significantly reduced the rate of the first polar body extrusion with no significant effect on cumulus cell expansion; however, 400 μM of IBP could significantly affect both. Further research revealed that abnormal spindles, misalignment chromosomes, and aberrant distributed actin filaments were detected in IBP-treated oocytes, which indicates that the cytoskeleton architecture of oocyte could be the target of IBP. At the same time, ROS level and apoptosis rate of oocyte were significantly increased by IBP exposure. Moreover, the levels of H3K9me3 and H3K27me3 were significantly induced in oocytes by IBP. Collectively, these results demonstrate that acute exposure to IBP could disrupt porcine oocyte maturation through affecting cytoskeleton, oxidative stress, viability and epigenetic modification. Environ. Mol. Mutagen. 61:433-444, 2020. Fig. 7. Schematic representation of negative effects of IBP on porcine oocytes. Oocyte exposure to IBP during meiotic maturation leads to inhibition of cumulus cell expansion, disruption of cytoskeleton, generation of oxidative stress and apoptosis, and alteration of epigenetic modifications. Environmental and Molecular Mutagenesis.

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The protective role of melatonin in porcine oocyte meiotic failure caused by the exposure to benzo(a)pyrene

Abstract: This study was supported by the National Natural Science Foundation of China (31571545) and the Natural Science Foundation of Jiangsu Province (BK20150677). The authors have no conflict of interest to disclose.

Cited by 65 publications

References 35 publications

Effects of melatonin on the synthesis of estradiol and gene expression in pig granulosa cells

Effects of melatonin on the synthesis of estradiol and gene expression in pig granulosa cells

Effect of Melatonin on the In Vitro Maturation of Porcine Oocytes, Development of Parthenogenetically Activated Embryos, and Expression of Genes Related to the Oocyte Developmental Capability

Isobutylparaben Negatively Affects Porcine Oocyte Maturation Through Increasing Oxidative Stress and Cytoskeletal Abnormalities

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