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Qiao-Qiao Kong Postdoctoral workstation, Department of Reproduction and Genetics, Tai’an City Central Hospital, Tai’an, Shandong,China

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Guo-Liang Wang Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an, Shandong, China

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Jin-Song An Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an, Shandong, China

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Jia Wang Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an, Shandong, China

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Hao Cheng Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an, Shandong, China

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Tao Liu Postdoctoral workstation, Department of Reproduction and Genetics, Tai’an City Central Hospital, Tai’an, Shandong,China

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Jing-He Tan Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an, Shandong, China

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Postovulatory oocyte aging is one of the major causes for human early pregnancy loss and for a decline in the population of some mammalian species. Thus, the mechanisms for oocyte aging are worth exploring. While it is known that ovulated oocytes age within the oviduct and that female stresses impair embryo development by inducing apoptosis of oviductal cells, it is unknown whether the oviduct and/or female stress would affect postovulatory oocyte aging. By comparing aging characteristics, including activation susceptibility, maturation-promoting factor activity, developmental potential, cytoplasmic fragmentation, spindle/chromosome morphology, gene expression, and cumulus cell apoptosis, this study showed that oocytes aged faster in vivo in restraint-stressed mice than in unstressed mice than in vitro. Our further analysis demonstrated that oviductal cells underwent apoptosis with decreased production of growth factors with increasing time after ovulation, and female restraint facilitated apoptosis of oviductal cells. Furthermore, mating prevented apoptosis of oviductal cells and alleviated oocyte aging after ovulation. In conclusion, the results demonstrated that mouse oviducts underwent apoptosis and facilitated oocyte aging after ovulation; female restraint facilitated oocyte aging while enhancing apoptosis of oviductal cells; and copulation ameliorated oviductal apoptosis and oocyte aging.

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Wen-Min Cheng Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China
Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Lei An Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Zhong-Hong Wu Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Yu-Bo Zhu Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Jing-Hao Liu Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Hong-Mei Gao Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Xi-He Li Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Shi-Jun Zheng Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Dong-Bao Chen Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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Jian-Hui Tian Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Sciences and Technology, College of Veterinary Medicine, Department of Obstetrics and Gynecology, College of Animal Sciences and Technology, China Agricultural University, Beijing 100094, People's Republic of China

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We recently reported that electrical activation followed by secondary chemical activation greatly enhanced the developmental competence of in vitro matured porcine oocytes fertilized by intracytoplasmic sperm injection (ICSI). We hypothesized that sperm treatment with disulfide bond reducing agents will enhance the development competence of porcine embryos produced by this ICSI procedure. We examined the effects of glutathione (GSH), dithiothreitol (DTT), GSH or DTT in combination with heparin on sperm DNA structure, paternal chromosomal integrity, pronuclear formation, and developmental competence of in vitro matured porcine oocytes after ICSI. Acridine orange staining and flow cytometry based sperm chromatin structure assay were used to determine sperm DNA integrity by calculating the cells outside the main population (COMP αT). No differences were observed in COMP αT values among GSH-treated and control groups. COMP αT values in GSH-treated groups were significantly lower than that in DTT-treated groups. Following ICSI, GSH treatments did not significantly alter paternal chromosomal integrity. Paternal chromosomal integrity in sperm treated with DTT plus or minus heparin was also the lowest among all groups. GSH-treated sperm yielded the highest rates of normal fertilization and blastocyst formation, which were significantly higher than that of control and DTT-treated groups. The majority of blastocysts derived from control and GSH-treated spermatozoa were diploid, whereas blastocysts derived from DTT-treated spermatozoa were haploid. In conclusion, sperm treatment with GSH enhanced the developmental capacity of porcine embryos produced by our optimized ICSI procedure.

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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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Hung-Fu Liao Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Chu-Fan Mo Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Shinn-Chih Wu Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Dai-Han Cheng Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Chih-Yun Yu Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Kai-Wei Chang Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Tzu-Hao Kao Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Chia-Wei Lu Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Marina Pinskaya Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Antonin Morillon Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Shih-Shun Lin Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Winston T K Cheng Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Déborah Bourc'his Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Timothy Bestor Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Li-Ying Sung Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Shau-Ping Lin Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan
Institute of Biotechnology, Department of Animal Science and Technology, Genome and Systems Biology Degree Program, Genome and Systems Biology Degree Program, Institut Curie, Department of Animal Science and Biotechnology, INSERM U934/CNRS UMR3215, Department of Genetics and Development, Agricultural Biotechnology Research Center, Center for Systems Biology, Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei 106, Taiwan

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Nuclear transfer (NT) is a technique used to investigate the development and reprogramming potential of a single cell. DNA methyltransferase-3-like, which has been characterized as a repressive transcriptional regulator, is expressed in naturally fertilized egg and morula/blastocyst at pre-implantation stages. In this study, we demonstrate that the use of Dnmt3l-knockout (Dnmt3l-KO) donor cells in combination with Trichostatin A treatment improved the developmental efficiency and quality of the cloned embryos. Compared with the WT group, Dnmt3l-KO donor cell-derived cloned embryos exhibited increased cell numbers as well as restricted OCT4 expression in the inner cell mass (ICM) and silencing of transposable elements at the blastocyst stage. In addition, our results indicate that zygotic Dnmt3l is dispensable for cloned embryo development at pre-implantation stages. In Dnmt3l-KO mouse embryonic fibroblasts, we observed reduced nuclear localization of HDAC1, increased levels of the active histone mark H3K27ac and decreased accumulation of the repressive histone marks H3K27me3 and H3K9me3, suggesting that Dnmt3l-KO donor cells may offer a more permissive epigenetic state that is beneficial for NT reprogramming.

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