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Canxin Wen Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Center for Reproductive Medicine, Institute of Women, Children and Reproductive Health,Shandong University, Jinan, Shandong, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Linlin Jiang Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Ping Pan Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Jia Huang Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Yanxin Xie Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Songbang Ou Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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Yu Li Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Guangdong Provincial Clinical Research Center for Obstetrical and Gynecological Diseases, Guangzhou, China

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In brief

Ovarian aging results in reactive oxygen species accumulation and mitochondrial deterioration. During the aging process, GRSF1 deficiency attenuates mitochondrial function in aging granulosa cells.

Abstract

Ovarian aging critically influences reproductive potential, with a marked decrease in oocyte quality and quantity and an increase in oxidative stress and mitochondrial dysfunction. This study elucidates the role of guanine-rich RNA sequence binding factor 1 (GRSF1) in the aging of ovarian granulosa cells (GCs). We observed a significant reduction in GRSF1 within GCs correlating with patient age, utilizing clinical samples from IVF patients. Using an siRNA-mediated knockdown technique, we established that diminished GRSF1 expression exacerbates mitochondrial dysfunction, elevates reactive oxygen species, and impairs ATP production. Furthermore, RNA immunoprecipitation revealed GRSF1’s interaction with superoxide dismutase 2 (SOD2) mRNA, a key antioxidant enzyme, suggesting a mechanism whereby GRSF1 modulates oxidative stress. Downregulation of SOD2 reversed the protective effects of GRSF1 overexpression on mitochondrial function. These insights into the role of GRSF1 in ovarian aging may guide the development of interventions to improve fertility outcomes in advanced age.

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Jian Zhang College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
Department of Biology, Southern University of Science and Technology, Shenzhen, Guangdong, China

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Linlin Hao Department of Radiotherapy, Second Hospital, Jilin University, Changchun, Jilin, China

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Qian Wei Department of Heat Disease, Affiliated Hospital to Changchun University of Chinese Medicine, Changchun, Jilin, China

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Sheng Zhang Academy of Translational Medicine, First Hospital, Jilin University, Changchun, Jilin, China

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Hui Cheng College of Veterinary Medicine, Jilin University, Changchun, Jilin, China

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Yanhui Zhai College of Veterinary Medicine, Jilin University, Changchun, Jilin, China

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Yu Jiang College of Veterinary Medicine, Jilin University, Changchun, Jilin, China

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Xinglan An Academy of Translational Medicine, First Hospital, Jilin University, Changchun, Jilin, China

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Ziyi Li Academy of Translational Medicine, First Hospital, Jilin University, Changchun, Jilin, China

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Xueming Zhang College of Veterinary Medicine, Jilin University, Changchun, Jilin, China

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Bo Tang College of Veterinary Medicine, Jilin University, Changchun, Jilin, China

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Somatic cell nuclear transfer (SCNT) has been successfully used for cloning in a variety of mammalian species. However, SCNT reprogramming efficiency is relatively low, in part, due to incomplete DNA methylation reprogramming of donor cell nuclei. We previously showed that ten-eleven translocation 3 (TET3) is responsible for active DNA demethylation during preimplantation embryonic development in bovines. In this study, we constructed TET3-overexpressing cell lines in vitro and observed that the use of these fibroblasts as donor cells increased the blastocyst rate by approximately 18 percentage points compared to SCNT. The overexpression of TET3 in bovine SCNT embryos caused a decrease in the global DNA methylation level of the pluripotency genes Nanog and Oct-4, ultimately resulting in an increase in the transcriptional activity of these pluripotency genes. Moreover, the quality of bovine TET3-NT embryos at the blastocyst stage was significantly improved, and bovine TET3-NT blastocysts possessed more total number of cells and fewer apoptotic cells than the SCNT blastocysts, similar to in vitro fertilization (IVF) embryos. Nevertheless, DNA methylation of the imprinting control region (ICR) for the imprinted genes H19-IGF2 in SCNT embryos remained unaffected by TET3 overexpression, maintaining parent-specific activity for further development. Thus, the results of our study provide a promising approach to rectify incomplete epigenetic reprogramming and achieve higher cloning efficiency.

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