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Qingling Yang Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Shanjun Dai Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Xiaoyan Luo Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Jing Zhu Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Fangyuan Li Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Jinhao Liu Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Guidong Yao Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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Yingpu Sun Reproductive Medical Center, First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Henan Province Key Laboratory for Reproduction and Genetics, Zhengzhou, China

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The quality of postovulatory metaphase II oocytes undergoes a time-dependent deterioration as a result of the aging process. Melatonin is considered to be an anti-aging agent. However, the underlying mechanisms of how melatonin improves the quality of postovulatory aged oocytes remain largely unclear. In this study, by using mouse model, we found that there were elevated reactive oxygen species levels and impaired mitochondrial function demonstrated by reduced mitochondrial membrane potential and increased mitochondrial aggregation in oocytes aged 24 h, accompanied by an increased number of meiotic errors, unregulated autophagy-related proteins and early apoptosis, which led to decreased oocyte quality and disrupted developmental competence. However, all of these events can be largely prevented by supplementing the oocyte culture medium with 10−3 M melatonin. Additionally, we found that the expression of sirtuin family members (SIRT1, 2 and 3) was dramatically reduced in aged oocytes. In addition, in vitro supplementation with melatonin significantly upregulated the expression of SIRT1 and antioxidant enzyme MnSOD, but this action was not observed for SIRT2 and SIRT3. Furthermore, the protective effect of melatonin on the delay of oocyte aging vanished when the SIRT1 inhibitor EX527 was used to simultaneously treat the oocytes with melatonin. Consistent with this finding, we found that the postovulatory oocyte aging process was markedly attenuated when the oocytes were treated with the SIRT1 activator SRT1720. In conclusion, our data strongly indicate that melatonin delays postovulatory mouse oocyte aging via a SIRT1–MnSOD-dependent pathway, which may provide a molecular mechanism support for the further application of melatonin in the assisted reproductive technology field.

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Dengfeng Bi School of Life Sciences, University of Science and Technology of China, Hefei, China
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, China

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Jing Yao State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, China
Beijing Institute for Stem Cell and Regenerative Medicine, Beijing, China
University of Chinese Academy of Sciences, Beijing, China

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Yu Wang State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, China
University of Chinese Academy of Sciences, Beijing, China

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Guosong Qin State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, China

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Yunting Zhang State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

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Yanfang Wang Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China

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Jianguo Zhao School of Life Sciences, University of Science and Technology of China, Hefei, China
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, China
Beijing Institute for Stem Cell and Regenerative Medicine, Beijing, China
University of Chinese Academy of Sciences, Beijing, China

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An efficient mRNA knockdown strategy is needed to explore gene function in cells and embryos, especially to understand the process of maternal mRNA decay during early embryo development. Cas13, a novel RNA-targeting CRISPR effector protein, could bind and cleave complementary single-strand RNA, which has been employed for mRNA knockdown in mouse and human cells and RNA-virus interference in plants. Cas13 has not yet been reported to be used in pigs. In the current study, we explored the feasibility of CRISPR/Cas13d-mediated endogenous RNA knockdown in pigs. KDM5B, a histone demethylase of H3K4me3, was downregulated at the transcriptional level by 50% with CRISPR/Cas13d in porcine fibroblast cells. Knockdown of KDM5B-induced H3K4me3 expression and decreased the abundance of H3K27me3, H3K9me3, H3K4ac, H4K8ac, and H4K12ac. These changes affected cell proliferation and cell cycle. Furthermore, stable integration of the CRISPR/Cas13d system into the porcine genome resulted in the continuous expression of Cas13d and persistent knockdown of KDM5B. Finally, the RNA-targeting potential of Cas13d was further validated in porcine parthenogenetic embryos. By microinjection of Cas13d mRNA and gRNA targeting KDM5B into porcine oocytes, the expression of KDM5B was downregulated, the abundance of H3K4me3 increased as expected, and the expression of embryonic development-related genes was changed accordingly. These results indicate that CRISPR/Cas13d provides an easily programmable platform for spatiotemporal transcriptional manipulation in pigs.

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Jiaojiao Huang State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China
State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Hongyong Zhang State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China
State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Jing Yao State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Guosong Qin State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Feng Wang State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Xianlong Wang State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Ailing Luo State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Qiantao Zheng State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China
State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Chunwei Cao State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China
State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Jianguo Zhao State Key Laboratory of Stem Cell and Reproductive Biology, University of Chinese Academy of Sciences, College of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China

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Accumulating evidence suggests that faulty epigenetic reprogramming leads to the abnormal development of cloned embryos and results in the low success rates observed in all mammals produced through somatic cell nuclear transfer (SCNT). The aberrant methylation status of H3K9me and H3K9me2 has been reported in cloned mouse embryos. To explore the role of H3K9me2 and H3K9me in the porcine somatic cell nuclear reprogramming, BIX-01294, known as a specific inhibitor of G9A (histone-lysine methyltransferase of H3K9), was used to treat the nuclear-transferred (NT) oocytes for 14–16 h after activation. The results showed that the developmental competence of porcine SCNT embryos was significantly enhanced both in vitro (blastocyst rate 16.4% vs 23.2%, P<0.05) and in vivo (cloning rate 1.59% vs 2.96%) after 50 nm BIX-01294 treatment. BIX-01294 treatment significantly decreased the levels of H3K9me2 and H3K9me at the 2- and 4-cell stages, which are associated with embryo genetic activation, and increased the transcriptional expression of the pluripotency genes SOX2, NANOG and OCT4 in cloned blastocysts. Furthermore, the histone acetylation levels of H3K9, H4K8 and H4K12 in cloned embryos were decreased after BIX-01294 treatment. However, co-treatment of activated NT oocytes with BIX-01294 and Scriptaid rescued donor nuclear chromatin from decreased histone acetylation of H4K8 that resulted from exposure to BIX-01294 only and consequently improved the preimplantation development of SCNT embryos (blastocyst formation rates of 23.7% vs 21.5%). These results indicated that treatment with BIX-01294 enhanced the developmental competence of porcine SCNT embryos through improvements in epigenetic reprogramming and gene expression.

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Guangyin Xi Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Wenjing Wang Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Sarfaraz A Fazlani Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China
Lasbela University of Agriculture, Water and Marine Science, Lasbela, Balochistan, Pakistan

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Fusheng Yao Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Mingyao Yang Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Jing Hao Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Lei An Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Jianhui Tian Ministry of Agriculture Key Laboratory of Animal Genetics, Breeding and Reproduction, National Engineering Laboratory for Animal Breeding, College of Animal Sciences and Technology, China Agricultural University, Beijing, China

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Compared to ovarian antral follicle development, the mechanism underlying preantral follicle growth has not been well documented. Although C-type natriuretic peptide (CNP) involvement in preantral folliculogenesis has been explored, its detailed role has not been fully defined. Here, we used mouse preantral follicles and granulosa cells (GCs) as a model for investigating the dynamic expression of CNP and natriuretic peptide receptor 2 (NPR2) during preantral folliculogenesis, the regulatory role of oocyte-derived growth factors (ODGFs) in natriuretic peptide type C (Nppc) and Npr2 expression, and the effect of CNP on preantral GC viability. Both mRNA and protein levels of Nppc and Npr2 were gradually activated during preantral folliculogenesis. CNP supplementation in culture medium significantly promoted the growth of in vitro-cultured preantral follicles and enhanced the viability of cultured GCs in a follicle-stimulating hormone (FSH)-independent manner. Using adult and prepubertal mice as an in vivo model, CNP pre-treatment via intraperitoneal injection before conventional superovulation also had a beneficial effect on promoting the ovulation rate. Furthermore, ODGFs enhanced Nppc and Npr2 expression in the in vitro-cultured preantral follicles and GCs. Mechanistic study demonstrated that the regulation of WNT signaling and estrogen synthesis may be implicated in the promoting role of CNP in preantral folliculogenesis. This study not only proves that CNP is a critical regulator of preantral follicle growth, but also provides new insight in understanding the crosstalk between oocytes and somatic cells during early folliculogenesis.

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