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Wei Wang College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Xia Chen College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Xinxiu Li College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Li Wang College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Haiyan Zhang College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Yu He College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Jingjing Wang College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Yongyan Zhao College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Baole Zhang College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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Yinxue Xu College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing 210095, People's Republic of China

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FSH plays a critical role in granulosa cell (GC) proliferation and steroidogenesis through modulation by factors including bone morphogenetic proteins family, which belongs to transforming growth factor β (TGFB) superfamily. TGFBs are the key factors in maintaining cell growth and differentiation in ovaries. However, the interaction of FSH and TGFB on the GCs' proliferation and steroidogenesis remains to be elucidated. In this study, we have investigated the role of SMAD4, a core molecule mediating the intracellular TGFB/SMAD signal transduction pathway, in FSH-mediated proliferation and steroidogenesis of porcine GCs. In this study, SMAD4 was knocked down using interference RNA in porcine GCs. Our results showed that SMAD4-siRNA causes specific inhibition of SMAD4 mRNA and protein expression after transfection. Knockdown of SMAD4 significantly inhibited FSH-induced porcine GC proliferation and estradiol production and changed the expression of cyclin D2, CDK2, CDK4, CYP19a1, and CYP11a1. Thus, these observations establish an important role of SMAD4 in the regulation of the response of porcine GCs to FSH.

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

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Aalia Batool State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
University of Chinese Academy of Sciences, Beijing, China

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Su-Ren Chen State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

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Yi-Xun Liu State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

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Reduced contractility of the testicular peritubular myoid (PTM) cells may contribute to human male subfertility or infertility. Transcription factor GATA4 in Sertoli and Leydig cells is essential for murine spermatogenesis, but limited attention has been paid to the potential role of GATA4 in PTM cells. In primary cultures of mouse PTM cells, siRNA knockdown of GATA4 increased the contractile activity, while GATA4 overexpression significantly attenuated the contractility of PTM cells using a collagen gel contraction assay. Using RNA sequencing and qRT-PCR, we identified a set of genes that exhibited opposite expressional alternation between Gata4 siRNA vs nontargeting siRNA-treated PTM cells and Gata4 adenovirus vs control adenovirus-treated PTM cells. Notably, ion channels, smooth muscle function, cytokines and chemokines, cytoskeleton, adhesion and extracellular matrix were the top four enriched pathways, as revealed by cluster analysis. Natriuretic peptide type B (NPPB) content was significantly upregulated by GATA4 overexpression in both PTM cells and their culture supernatant. More importantly, the addition of 100 μM NPPB could abolish the promoting effect of Gata4 silencing on PTM cell contraction. Taken together, we suggest that the inhibitory action of GATA4 on PTM cell contraction is mediated at least partly by regulating genes belonging to smooth muscle contraction pathway (e.g. Nppb).

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Huijuan Zhang International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Reproductive Medicine Center, The People’s Hospital of Zhengzhou University, Henan Provincial People’s Hospital, Zhengzhou, Henan, China

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Guishuan Wang International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Lin Liu The Reproductive Medicine Center, The First Hospital of Lanzhou University, Lanzhou, China

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Xiaolin Liang International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Yu Lin International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Yi-Yu Lin Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA

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Chu-Fang Chou Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, Alabama, USA

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Mo-Fang Liu Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

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Hefeng Huang International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Fei Sun International Peace Maternity and Child Health Hospital, Shanghai Key laboratory for Reproductive Medicine, School of Medicine, Shanghai Jiaotong University, Shanghai, China

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The chromatoid body (CB) is a specific cloud-like structure in the cytoplasm of haploid spermatids. Recent findings indicate that CB is identified as a male germ cell-specific RNA storage and processing center, but its function has remained elusive for decades. In somatic cells, KH-type splicing regulatory protein (KSRP) is involved in regulating gene expression and maturation of select microRNAs (miRNAs). However, the function of KSRP in spermatogenesis remains unclear. In this study, we showed that KSRP partly localizes in CB, as a component of CB. KSRP interacts with proteins (mouse VASA homolog (MVH), polyadenylate-binding protein 1 (PABP1) and polyadenylate-binding protein 2 (PABP2)), mRNAs (Tnp2 and Odf1) and microRNAs (microRNA-182) in mouse CB. Moreover, KSRP may regulate the integrity of CB via DDX5-miRNA-182 pathway. In addition, we found abnormal expressions of CB component in testes of Ksrp-knockout mice and of patients with hypospermatogenesis. Thus, our results provide mechanistic insight into the role of KSRP in spermatogenesis.

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Qian Zhang State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China
State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Song Yu State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Xing Huang State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China
State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Yi Tan State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Cheng Zhu State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Yan-Ling Wang State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Haibin Wang State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Hai-Yan Lin State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Jiejun Fu State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Hongmei Wang State Key Laboratory of Reproductive Biology, Department of Obstetrics, Key Laboratory of Longevity and Ageing-related Diseases, Laboratory Animal Center, School of Life Sciences, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China

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Cullin 3 (CUL3), a scaffold protein, assembles a large number of ubiquitin ligase complexes, similar to Skp1-Cullin 1-F-box protein complex. Several genetic models have shown that CUL3 is crucial for early embryonic development. Nevertheless, the role of CUL3 in human trophoblast function remains unclear. In this study, immunostaining revealed that CUL3 was strongly expressed in the villous cytotrophoblasts, the trophoblast column, and the invasive extravillous trophoblasts. Silencing CUL3 significantly inhibited the outgrowth of villous explant ex vivo and decreased invasion and migration of trophoblast HTR8/SVneo cells. Furthermore, CUL3 siRNA decreased pro-MMP9 activity and increased the levels of TIMP1 and 2. We also found that the level of CUL3 in the placental villi from pre-eclamptic patients was significantly lower as compared to that from their gestational age-matched controls. Moreover, in the lentiviral-mediated placenta-specific CUL3 knockdown mice, lack of CUL3 resulted in less invasive trophoblast cells in the maternal decidua. Taken together, these results suggest an essential role for CUL3 in the invasion and migration of trophoblast cells, and dysregulation of its expression may be associated with the onset of pre-eclampsia.

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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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Hang Qi Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Guiling Liang Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Jin Yu Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Xiaofeng Wang Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Yan Liang Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Xiaoqing He Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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Tienan Feng Clinical Research Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China

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Jian Zhang Department of Obstetrics and Gynecology, International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiaotong University, Shanghai, China
Institute of Embryo-Fetal Original Adult Disease, Affiliated to School of Medicine, Shanghai Jiaotong University, Shanghai, China

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MicroRNA (miRNA) expression profiles in tubal endometriosis (EM) are still poorly understood. In this study, we analyzed the differential expression of miRNAs and the related gene networks and signaling pathways in tubal EM. Four tubal epithelium samples from tubal EM patients and five normal tubal epithelium samples from uterine leiomyoma patients were collected for miRNA microarray. Bioinformatics analyses, including Ingenuity Pathway Analysis (IPA), Gene Ontology (GO) analysis and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, were performed. Quantitative real-time polymerase chain reaction (qRT-PCR) validation of five miRNAs was performed in six tubal epithelium samples from tubal EM and six from control. A total of 17 significantly differentially expressed miRNAs and 4343 potential miRNA-target genes involved in tubal EM were identified (fold change >1.5 and FDR-adjusted P value <0.05). IPA indicated connections between miRNAs, target genes and other gynecological diseases like endometrial carcinoma. GO and KEGG analysis revealed that most of the identified genes were involved in the mTOR signaling pathway, SNARE interactions in vesicular transport and endocytosis. We constructed an miRNA-gene-disease network using target gene prediction. Functional analysis showed that the mTOR pathway was connected closely to tubal EM. Our results demonstrate for the first time the differentially expressed miRNAs and the related signal pathways involved in the pathogenesis of tubal EM which contribute to elucidating the pathogenic mechanism of tubal EM-related infertility.

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Chulin Yu
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Meiling Li
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Yue Wang State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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Ying Liu State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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Chengzhi Yan State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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Jirong Pan State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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Jiali Liu State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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Sheng Cui State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People’s Republic of China

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The corticotropin-releasing hormone (CRH) signaling system is involved in numbers of stress-related physiological and pathological responses, including its inhibiting effects on estradiol (E2) synthesis and follicular development in the ovary. In addition, there are reports that microRNAs (miRNAs) can control the function of animal reproductive system. The aim of present study was to investigate the functions of miR-375 and the relationship between miR-375 and CRH signaling molecules in the porcine ovary. First, our common PCR results show that miR-375 and the CRH receptor 1 (CRHR1) are expressed in porcine ovary, whereas CRH receptor 2 (CRHR2) is not detected. We further have located the cell types of miR-375 and CRHR1 by in situ hybridization (ISH), and the results show that miR-375 is located only in the granulosa cells, whereas CRHR1 is positive in all of granulosa cells and oocytes, inferring that miR-375 and CRHR1 are co-localized in granulosa cells. Second, we show that overexpression of miR-375 in cultured granulosa cells suppresses the E2 production, whereas miR-375 knockdown demonstrates the opposite result. Besides, our in vitro results demonstrate that miR-375 mediates the signaling pathway of CRH inhibiting E2 synthesis. Finally, our data show that the action of miR-375 is accomplished by directly binding to the 3′UTR of specificity protein1 (SP1) mRNA to decrease the SP1 protein level. Thus, we conclude that miR-375 is a key factor in regulating E2 synthesis by mediating the CRH signaling pathway.

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Tengteng Li Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei, China

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Jiajia Fei Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei, China

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Huihui Yu Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei, China

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Xingxing Wang Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei, China

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Dan Li Department of Scientific Research, The Second Affiliated Hospital of Anhui Medical University, Hefei, China

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Zongzhi Yin Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei, China
NHC Key Laboratory of the Study of Abnormal Gametes and the Reproductive Tract, Anhui Medical University, Hefei, China

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In brief

During pregnancy, uterine kept quiescence along with uterine overdistention before labor. Prolonged stretching induced uterus myometrial hypoxia, increased TREK1 expression, and relaxed the myometrium, which may contribute to uterine quiescence and atony during pregnancy.

Abstract

The mechanisms underlying pre-labor uterine quiescence and uterine atony during overdistention are unclear. TREK1 (a two-pore domain potassium channel) and hypoxia-inducible factor-1α (HIF-1α) are activated by mechanical stretch, and their expression is upregulated by decreased uterine contractility. HIF-1α is a nuclear factor which regulates numerous target proteins, but whether it regulates TREK1 during the uterine stretch to cause uterine quiescence and/or atony is unclear. We investigated uterine contractility at different gestational stages in rats, as well as in non-pregnant uteri, which were induced by prolonged stretching and hypoxia. We also assessed the effects of incubating the uteri with or without echinomycin or l-methionine. Moreover, we analyzed HIF-1α and TREK1 expression levels in each group, as well as at various gestational stages of pregnant human uteri. We found that contractility was significantly decreased in pregnant uteri when compared with non-pregnant uteri, and this decrease was associated with increases in HIF-1α and TREK1 expression levels. HIF-1α and TREK1 expression levels in human uteri increased with the gestational length. Decreased uterine contractility and increased HIF-1α and TREK1 expression levels were also observed in non-pregnant rat uteri under 8 g of stretching tension or hypoxia. Inhibition of hypoxia with echinomycin restored normal uterine contractility, while HIF-1α and TREK1 protein expression remained reduced. TREK1 inhibition with l-methionine also restored uterine contractility under tension or hypoxia. In conclusion, we demonstrated that prolonged stretching induces myometrial hypoxia, increases TREK1 expression, and relaxes the myometrium, which may contribute to uterine quiescence and atony.

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Zhengkai Wei College of Life Sciences and Engineering, Foshan University, Foshan, Guangdong Province, People’s Republic of China

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Tingting Yu Jilin Provincial Key Laboratory of Animal Embryo Engineering, Institute of Zoonosis, College of Animal Sciences, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Jingjing Wang Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Chaoqun Wang Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Xiao Liu Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Zhen Han Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Xu Zhang Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Yong Zhang Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Hongsheng Ouyang Jilin Provincial Key Laboratory of Animal Embryo Engineering, Institute of Zoonosis, College of Animal Sciences, Jilin University, Changchun, Jilin Province, People’s Republic of China

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Zhengtao Yang College of Life Sciences and Engineering, Foshan University, Foshan, Guangdong Province, People’s Republic of China

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Sperm motility, fertilization and embryo implantation are several important factors in reproduction. Except healthy state of sperm and embryo themselves, successful pregnancy is closely related to the status of female reproductive tract immune system. Increased immune cells in reproductive tract often leads to low sperm motility and low chance of embryo implantation, but the mechanisms remain not well clarified. The aim of this study is to investigate the direct effects of swine polymorphonuclear neutrophils (PMNs) on sperm or embryo in vitro and then try to clarify the molecular mechanisms undergoing the phenomenon. Swine sperm-triggered neutrophil extracellular traps (NETs) were observed by scanning electron microscopy (SEM). PMNs phagocytosis of sperms was examined by transmission electron microscopy (TEM). Sperm-triggered NETs were quantitated by Pico Green®. Vital staining of the interaction between PMNs and embryo were observed by using confocal microscope. It was showed that PMNs were directly activated by sperm in the form of phagocytosis or casting NETs and that sperm-triggered-NETs formation was made up with DNA co-located with citrullinated histone 3 (citH3) and myeloperoxidase (MPO). In addition, the potential mechanism of NETs release was relevant to NADPH oxidase, ERK1/2 or p38 MAPK signaling pathways. Of great interest was that swine embryo was first found entangled in NETs in vitro, but the function and mechanism of this action in vivo fertilization still needed further investigation. In conclusion, this is the first report about swine sperm-induced NETs that entangle sperm and embryo, which might provide an entirely understanding of swine reproductive physiology and immunology.

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Yue Li Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China
Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Ru Zheng Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China
Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Rui Wang Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China
Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Xiaoyin Lu Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China
Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Cheng Zhu Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Hai-Yan Lin Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Hongmei Wang Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Xiaoguang Yu Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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Jiejun Fu Department of Biochemistry and Molecular Biology, State Key Laboratory of Reproductive Biology, University of Chinese Academy of Sciences, Key Laboratory of Longevity and Ageing-related Diseases, College of Basic Medical Science, Harbin Medical University, Harbin 150081, People's Republic of China

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The placenta has numerous functions, such as transporting oxygen and nutrients and building the immune tolerance of the fetus. Cell fusion is an essential process for placental development and maturation. In human placental development, mononucleated cytotrophoblast (CTB) cells can fuse to form a multinucleated syncytiotrophoblast (STB), which is the outermost layer of the placenta. Nephrin is a transmembrane protein that belongs to the Ig superfamily. Previous studies have shown that nephrin contributes to the fusion of myoblasts into myotubes in zebrafish and mice, presenting a functional conservation with its Drosophila ortholog sticks and stones. However, whether nephrin is involved in trophoblast syncytialization remains unclear. In this study, we report that nephrin was localized predominantly in the CTB cells and STB of human placenta villi from first trimester to term pregnancy. Using a spontaneous fusion model of primary CTB cells, the expression of nephrin was found to be increased during trophoblast cell fusion. Moreover, the spontaneous syncytialization and the expression of syncytin 2, connexin 43, and human chorionic gonadotropin beta were significantly inhibited by nephrin-specific siRNAs. The above results demonstrate that nephrin plays an important role in trophoblast syncytialization.

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