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Chuwei Li C Li, Medical School, Nanjing University, Nanjing, China

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Zhang Qian Z Qian, Medical School, Nanjing University, Nanjing, China

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Hong Zhang H Zhang, Medical School, Nanjing University, Nanjing, China

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Xie Ge X Ge, Medical School, Nanjing University, Nanjing, China

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Li Chen L Chen, Department of Reproductive Medicine, Nanjing Jinling Hospital, Nanjing, China

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Ting Tang T Tang, Medical School, Nanjing University, Nanjing, China

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Mengqi Xue M Xue, Medical School, Nanjing University, Nanjing, China

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Zhaowanyue He Z He, Medical School, Nanjing University, Nanjing, China

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Lu Zheng L Zheng, Medical School, Nanjing University, Nanjing, China

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Chun Cao C Cao, Department of Reproductive Medicine, Southern Medical University, Guangzhou, China

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Kemei Zhang K Zhang, Department of Reproductive Medicine, Nanjing Medical University, Nanjing, China

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Rujun Ma R Ma, Medical School, Nanjing University, Nanjing, China

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Bing Yao B Yao, Medical School, Nanjing University, Nanjing, China

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With an increase in the mean age at parturition worldwide, female reproductive aging has become a key health problem. Advanced maternal age is reflected by decreased oocyte quality; however, the molecular mechanisms of oocyte aging are uncharacterized. O-linked N-acetylglucosamine (O-GlcNAc), a dynamic posttranslational modification, plays a critical role in the development of many age-related diseases, yet it remains unclear whether and how O-GlcNAc participates in oocyte aging. Here, we found that global O-GlcNAc was elevated in normal biological aging mice oocytes (32-34 weeks) which were characterized by meiotic maturation failure and impaired mitochondrial function. Specifically, O-GlcNAc targeted the mitochondrial fission protein dynamic-related protein 1 (DRP1) to meditate mitochondrial distribution in the process of aging. Using the O-GlcNAcase (OGA) pharmacological inhibitor Thiamet-G and OGA knockdown (OGA-KD) to mimic the age-related high O-GlcNAc in young oocytes from 6-8 week-old mice mimicked the phenotype of oocyte aging. Moreover, reducing O-GlcNAc levels in aging oocytes restored spindle organization to improve oocyte quality. Our results demonstrate that O-GlcNAc is a key regulator of meiotic maturation that participates in the progression of oocyte aging.

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