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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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Xiaoyang Wen Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Jingyang Zhang Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Zihan Xu Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Muzi Li Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Xiaotong Dong Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Yanbo Du Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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Zhen Xu Center for Medical Genetics and Prenatal Diagnosis, Shandong Provincial Maternal and Child Health Care Hospital, Jinan, Shandong, China
Shandong Medicine and Health Key Laboratory of Birth Defect Prevention and Genetic Medicine, Jinan, Shandong, China
Key Laboratory of Birth Regulation and Control Technology of National Health Commission of China, Jinan, Shandong, China

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Lei Yan Institute of Women, Children and Reproductive Health, Shandong University, Jinan, Shandong, China
State Key Laboratory of Reproductive Medicine and Offspring Health, Shandong University, Jinan, Shandong, China
Medical Integration and Practice Center, Shandong University, Jinan, Shandong, People’s Republic of China
Shandong Key Laboratory of Reproductive Medicine, Jinan, Shandong, People’s Republic of China
Reproductive Hospital Affiliated to Shandong University, Jinan, Shandong, People’s Republic of China

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In brief

Abnormal glucose metabolism may be involved in the pathogenesis of endometriosis. The present study identifies that highly expressed H19 leads to increased aerobic glycolysis and histone lactylation levels in endometriosis.

Abstract

Previous studies from our group and others have shown increased IncRNA H19 expression in both the eutopic endometrium and the ectopic endometriosis tissue during endometriosis. In this study, we use immunofluorescence, immunohistochemistry, and protein quantification to determine that levels of aerobic glycolysis and histone lactylation are increased in endometriosis tissues. In human endometrial stromal cells, we found that high H19 expression resulted in abnormal glucose metabolism by examining the levels of glucose, lactate, and ATP and measuring protein levels of enzymes that participate in glycolysis. At the same time, immunofluorescence and western blotting demonstrated increased histone lactylation in H19 overexpressing cells. Altering aerobic glycolysis and histone lactylation levels through the addition of sodium lactate and 2-deoxy-d-glucose demonstrated that increased aerobic glycolysis and histone lactylation levels resulted in enhanced cell proliferation and cell migration, contributing to endometriosis. To validate these findings in vivo, we constructed an endometriosis mouse model, demonstrating similar changes in endometriosis tissues in vivo. Both aerobic glycolysis and histone lactylation levels were elevated in endometriotic lesions. Taken together, these data demonstrate elevated expression levels of H19 in endometriosis patients promote abnormal glucose metabolism and elevated histone lactylation levels in vivo, enhancing cell proliferation and migration and promoting the progression of endometriosis. Our study provides a functional link between H19 expression and histone lactylation and glucose metabolism in endometriosis, providing new insights into disease mechanisms that could result in novel therapeutic approaches.

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Wenjie Dai Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Hong Yang Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Bo Xu Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Tiantian He Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Ling Liu Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Zhen Zhang Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Liyang Ding Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Xiuying Pei Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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Xufeng Fu Key Laboratory of Fertility Preservation and Maintenance of Ministry of Education, School of Basic Medical Sciences, Ningxia Medical University, Yinchuan, China

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In brief

This study reveals that orthotopic transplantation of 3D hUC-MSC spheroids is more effective than monolayer-cultured hUC-MSCs in improving POF and distinctly reducing oxidative stress through the paracrine effect, thereby preventing apoptosis and autophagy of GCs.

Abstract

Premature ovarian failure (POF) is a common reproductive disease in women younger than 40 years old, and studies have demonstrated that the application of human umbilical cord mesenchymal stem cells (hUC-MSCs) is a promising therapy strategy for POF. Given the previously established therapeutic advantages of 3D MSC spheroids, and to evaluate their effectiveness, both 3D hUC-MSC spheroids and monolayer-cultured hUC-MSCs were employed to treat a cyclophosphamide-induced POF rat model through orthotopic transplantation. The effects of these two forms on POF were subsequently assessed by examining apoptosis, autophagy, and oxidative damage in ovarian granulosa cells (GCs). The results indicated that hUC-MSC spheroids exhibited superior treatment effects on resisting autophagy, apoptosis, and oxidative damage in GCs compared to monolayer-cultured hUC-MSCs. To further elucidate the impact of hUC-MSC spheroids in vitro, a H2O2-induced KGN cells model was established and co-cultured with both forms of hUC-MSCs. As expected, the hUC-MSC spheroids also exhibited superior effects in resisting apoptosis and autophagy caused by oxidative damage. Therefore, this study demonstrates that 3D hUC-MSC spheroids have potential advantages in POF therapy; however, the detailed mechanisms need to be further investigated. Furthermore, this study will provide a reference for the clinical treatment strategy of POF.

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Wen-Wen Gu NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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Long Yang NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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Xing-Xing Zhen NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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Yan Gu The Second Hospital of Tianjin Medical University, Tianjin, China

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Hua Xu Shanghai Ji Ai Genetics and IVF Institute, Obstetrics and Gynecology Hospital, Fudan University, Shanghai, China

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Miao Liu Zhong Shan Hospital, Shanghai, China

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Qian Yang NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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Xuan Zhang NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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Jian Wang NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Shanghai, China

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The invasion of maternal decidua by extravillous trophoblast (EVT) is essential for the establishment and maintenance of pregnancy, and abnormal trophoblast invasion could lead to placenta-associated pathologies including early pregnancy loss and preeclampsia. SEC5, a component of the exocyst complex, plays important roles in cell survival and migration, but its role in early pregnancy has not been reported. Thus, the present study was performed to explore the functions of SEC5 in trophoblast cells. The results showed that SEC5 expression in human placental villi at first trimester was significantly higher than it was at the third trimester, and it was abundantly localized in the cytotrophoblast (CTB) and the trophoblastic column. SEC5 knockdown was accompanied by reduced migration and invasion in HTR-8/SVneo cells. In addition, the expression and plasma membrane distribution of integrin β1 was also decreased. Furthermore, shRNA-mediated knockdown of SEC5 inhibited the outgrowth of first trimester placental explants. SEC5 and InsP3R were colocalized in the cytoplasm of HTR-8/SVneo cells, and the cell-permeant calcium chelator BAPTA-AM could significantly inhibit HTR-8/SVneo cell invasion. The Ca2+ imaging results showed that the 10% fetal bovine serum-stimulated cytosolic calcium concentration ([Ca2+]c) was not only reduced by downregulated SEC5 but also was blocked by the InsP3R inhibitor. Furthermore, either the [Ca2+]c was buffered by BAPTA-AM or the knockdown of SEC5 disrupted HTR-8/SVneo cell F-actin stress fibers and caused cytoskeleton derangement. Taken together, our results suggest that SEC5 might be involved in regulating trophoblast cell migration and invasion through the integrin/Ca2+ signal pathway to induce cytoskeletal rearrangement.

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Yan Xu Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Miao Liu Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Yi-hua Gu Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Xiao-feng Jia Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Yong-Mei Chen Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Michelle Santos Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Ai-Zhen Wu Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Xiao-dong Zhang Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Hui-Juan Shi Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China
Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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Ching-Ling C Chen Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China
Medical School of Fudan University, Center for Biomedical Research, The Rockefeller University, National Population and Family Planning Key Laboratory of Contraceptive Drugs and Devices, Department of Anatomy, Shanghai, China

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With tetraspanning topology, members of the membrane-spanning four-domain subfamily A (MS4A) may facilitate signaling or ion channel functions in many tissues. In this study, we report the cloning of a full-length cDNA from rat testis, designated Ms4a14 (Sp3111), which encodes the MS4A protein with 1139 amino acid residues. In situ hybridization and immunohistochemical analyses indicate that Ms4a14 is predominantly expressed from round spermatids to spermatozoa at specific stages in the rat testis at both the mRNA and protein level. Immunofluorescence analysis revealed that MS4A14 (SP3111) is located in the acrosome and the midpiece of the flagellum in mature sperm. Previously, we explored and reported the involvement of MS4A14 in reproductive functions, using antibody blockage during IVF and a transgenic RNA interference method in a mouse model. Our results suggested that MS4A14 is involved in fertilization and zygote division. As MS4A14 protein exists in mammals, such as humans, cows, dogs, and rodents, MS4A14 may play a ubiquitous role in mammalian reproduction.

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