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Shou-Bin Tang College of Animal Science and Technology, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Lei-Lei Yang College of Animal Science and Technology, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Ting-Ting Zhang Reproductive Medicine Center of People’s Hospital of Zhengzhou University, Zhengzhou, Henan Province, People’s Republic of China

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Qian Wang Reproductive Medicine Center of People’s Hospital of Zhengzhou University, Zhengzhou, Henan Province, People’s Republic of China

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Shen Yin College of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Shi-Ming Luo College of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Wei Shen College of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Zhao-Jia Ge College of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Qing-Yuan Sun College of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, People’s Republic of China

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It is demonstrated that repeated superovulation has deleterious effects on mouse ovaries and cumulus cells. However, little is known about the effects of repeated superovulation on early embryos. Epigenetic reprogramming is an important event in early embryonic development and could be easily disrupted by the environment. Thus, we speculated that multiple superovulations may have adverse effects on histone modifications in the early embryos. Female CD1 mice were randomly divided into four groups: (a) spontaneous estrus cycle (R0); (b) with once superovulation (R1); (c) with three times superovulation at a 7-day interval (R3) and (d) with five times superovulation at a 7-day interval (R5). We found that repeated superovulation remarkably decreased the fertilization rate. With the increase of superovulation times, the rate of early embryo development was decreased. The expression of Oct4, Sox2 and Nanog was also affected by superovulation in blastocysts. The immunofluorescence results showed that the acetylation level of histone 4 at lysine 12 (H4K12ac) was significantly reduced by repeated superovulation in mouse early embryos (P < 0.01). Acetylation level of histone 4 at lysine 16 (H4K16ac) was also significantly reduced in pronuclei and blastocyst along with the increase of superovulation times (P < 0.01). H3K9me2 and H3K27me3 were significantly increased in four-cell embryos and blastocysts. We further found that repeated superovulation treatment increased the mRNA level of histone deacetylases Hdac1, Hdac2 and histone methyltransferase G9a, but decreased the expression level of histone demethylase-encoding genes Kdm6a and Kdm6b in early embryos. In a word, multiple superovulations alter histone modifications in early embryos.

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Xiao Han State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Cong Zhang State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Xiangping Ma State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Xiaowei Yan State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Bohui Xiong State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Wei Shen College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Shen Yin College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Hongfu Zhang State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China

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Qingyuan Sun College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China
Fertility Preservation Lab, Reproductive Medicine Center, Guangdong Second Provincial General Hospital, Guangzhou, People’s Republic of China

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Yong Zhao State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China
College of Life Sciences, Qingdao Agricultural University, Qingdao, People’s Republic of China

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Muscarinic acetylcholine receptor (mAChR) antagonists have been reported to decrease male fertility; however, the roles of mAChRs in spermatogenesis and the underlying mechanisms are not understood yet. During spermatogenesis, extensive remodeling between Sertoli cells and/or germ cells interfaces takes place to accommodate the transport of developing germ cells across the blood-testis barrier (BTB) and adluminal compartment. The cell–cell junctions play a vital role in the spermatogenesis process. This study used ICR male mice and spermatogonial cells (C18-4) and Sertoli cells (TM-4). shRNA of control or M5 gene was injected into 5-week-old ICR mice testes. Ten days post-viral grafting, mice were deeply anesthetized with pentobarbital and the testes were collected. One testicle was fresh frozen for RNA-seq analysis or Western blotting (WB). The second testicle was fixed for immunofluorescence staining (IHF). C18-4 or TM-4 cells were treated with shRNA of control or M5 gene. Then, the cells were collected for RNA-seq analysis, WB, or IHF. Knockdown of mAChR M5 disrupted mouse spermatogenesis and damaged the actin-based cytoskeleton and many types of junction proteins in both Sertoli cells and germ cells. M5 knockdown decreased Phldb2 expression in both germ cells and Sertoli cells which suggested that Phldb2 may be involved in cytoskeleton and cell–cell junction formation to regulate spermatogenesis. Our investigation has elucidated a novel role for mAChR M5 in the regulation of spermatogenesis through the interactions of Phldb2 and cell–cell junctions. M5 may be an attractive future therapeutic target in the treatment of male reproductive disorders.

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Dong Zhang State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Shen Yin State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Man-Xi Jiang State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Wei Ma State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Yi Hou State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Cheng-Guang Liang State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Ling-Zhu Yu State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Wei-Hua Wang State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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Qing-Yuan Sun State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China

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The present study was designed to investigate the localization and function of cytoplasmic dynein (dynein) during mouse oocyte meiosis and its relationship with two major spindle checkpoint proteins, mitotic arrest-deficient (Mad) 1 and Mad2. Oocytes at various stages during the first meiosis were fixed and immunostained for dynein, Mad1, Mad2, kinetochores, microtubules, and chromosomes. Some oocytes were treated with nocodazole before examination. Anti-dynein antibody was injected into the oocytes at germinal vesicle (GV) stage before the examination of its effects on meiotic progression or Mad1 and Mad2 localization. Results showed that dynein was present in the oocytes at various stages from GV to metaphase II and the locations of Mad1 and Mad2 were associated with dynein’s movement. Both Mad1 and Mad2 had two existing states: one existed in the cytoplasm (cytoplasmic Mad1 or cytoplasmic Mad2), which did not bind to kinetochores, while the other bound to kinetochores (kinetochore Mad1 or kinetochore Mad2). The equilibrium between the two states varied during meiosis and/or in response to the changes of the connection between microtubules and kinetochores. Cytoplasmic Mad1 and Mad2 recruited to chromosomes when the connection between microtubules and chromosomes was destroyed. Inhibition of dynein interferes with cytoplasmic Mad1 and Mad2 transportation from chromosomes to spindle poles, thus inhibits checkpoint silence and delays anaphase onset. These results indicate that dynein may play a role in spindle checkpoint inactivation.

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