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Yi Sun State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China
State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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Wen-Jia Zhang State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China
State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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Xin Zhao State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China
State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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Ren-Pei Yuan State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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Hui Jiang State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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Xiao-Ping Pu State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China
State Key Laboratory of Natural and Biomimetic Drugs, Department of Molecular and Cellular Pharmacology, Department of Andrology, School of Pharmaceutical Science, Peking University, Beijing, People's Republic of China

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PARK7 (DJ1) is a multifunctional oxidative stress response protein that protects cells against reactive oxygen species (ROS) and mitochondrial damage. PARK7 defects are known to cause various physiological dysfunctions, including infertility. Asthenozoospermia (AS), i.e. low-motile spermatozoa in the ejaculate, is a common cause of human male infertility. In this study, we found that downregulation of PARK7 resulted in increased levels of lipid peroxide and ROS, decreased mitochondrial membrane potential, and reduced mitochondrial complex I enzyme activity in the spermatozoa from AS patients. Furthermore, it was observed that PARK7 was translocated into the mitochondria of damaged spermatozoa in AS. Finally, we examined the oxidative state of PARK7 and the results demonstrated the enhancement of oxidation, expressed by increased sulfonic acid residues, the highest form of oxidation, as the sperm motility decreased. Taken together, these results revealed that PARK7 deficiency may increase the oxidative stress damage to spermatozoa. Our present findings open new avenues of therapeutic intervention targeting PARK7 for the treatment of AS.

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Pei-Li Wu Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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Jing-Wen Zhu Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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Cheng Zeng Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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Xin Li Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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Qing Xue Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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Hui-Xia Yang Department of Obstetrics and Gynecology, Peking University First Hospital, Beijing, China

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In brief

Insufficient trophoblast invasion at the maternal–fetal interface contributes to abortion-prone pregnancy. Our study shows that decreased levels of IGFBP7 in unexplained recurrent spontaneous abortion (URSA) trophoblast cells inhibit MMP2 and Slug expression as well as trophoblast invasion, suggesting that IGFBP7 should be considered a potential therapeutic protein target in URSA.

Abstract

Insufficient trophoblast invasion at the maternal–fetal interface contributes to abortion-prone pregnancy. Cyclosporine A (CsA) can exert therapeutic effects on URSA by promoting trophoblast invasion. A previous study showed decreased expression of insulin-like growth factor-binding protein 7 (IGFBP7) in the sera of recurrent spontaneous abortion patients. However, the role of IGFBP7 in URSA remains unknown. The aim of this study was to determine whether IGFBP7 modulates trophoblast invasion in URSA and the underlying molecular mechanisms. We found that IGFBP7 was expressed at lower levels in villous specimens from URSA patients. Manipulating IGFBP7 expression significantly affected the MMP2 and Slug expression in HTR-8/SVneo cells as well as trophoblast invasion in vitro. Inactivation of IGF-1R by IGFBP7 was observed, and IGF-1R inhibition increased the IGFBP7-induced MMP2 and Slug expression in HTR-8/SVneo cells. Moreover, the level of c-Jun was significantly upregulated in the URSA group. Silencing IGFBP7 increased the binding of downstream c-Jun to the MMP2 and Slug promoter regions in HTR-8/SVneo cells, thus suppressing transcription. In addition, increased expression of IGFBP7 in HTR-8/SVneo cells was observed upon CsA treatment. Knockdown of IGFBP7 inhibited the CsA-enhanced MMP2 and Slug expression in HTR-8/SVneo cells. Our results suggest that in normal pregnancy, IGFBP7 induces MMP2 and Slug expression via the IGF-1R-mediated c-Jun signaling pathway, thereby promoting trophoblast invasion. IGFBP7 depletion in URSA inhibits MMP2 and Slug expression as well as trophoblast invasion. Moreover, IGFBP7 participates in CsA-induced trophoblast invasion, suggesting that IGFBP7 is a potential therapeutic target for URSA.

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Xue-Yun Qin Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China
NHC Key Lab of Reproduction Regulation, Shanghai Institute for Biomedical and Pharmaceutical Technologies, Fudan University, Shanghai, People’s Republic of China

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Hui-Hui Shen Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China
NHC Key Lab of Reproduction Regulation, Shanghai Institute for Biomedical and Pharmaceutical Technologies, Fudan University, Shanghai, People’s Republic of China

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Xin-Yan Zhang Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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Xing Zhang Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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Feng Xie Center for Diagnosis and Treatment of Cervical and Uterine Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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Wen-Jun Wang Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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Yu Xiong Department of Obstetrics, Hospital of Obstetrics and Gynecology, Shanghai Medical School, Fudan University, Shanghai, People’s Republic of China
Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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Jie Mei Reproductive Medicine Center, Department of Obstetrics and Gynecology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medicine School, Nanjing, People’s Republic of China

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Ming-Qing Li Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China
NHC Key Lab of Reproduction Regulation, Shanghai Institute for Biomedical and Pharmaceutical Technologies, Fudan University, Shanghai, People’s Republic of China
Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, People’s Republic of China

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In brief

Hypoxia is vital for the establishment of the maternal–fetal interface during early pregnancy. This study shows that decidual macrophages (dMφ) could be recruited and reside in decidua under the regulation of hypoxia/VEGFA-CCL2 axis.

Abstract

Infiltration and residence of decidual macrophages (dMφ) are of great significance to pregnancy maintenance for their role in angiogenesis, placental development, and inducing immune tolerance. Besides, hypoxia has now been acknowledged as an important biological event at maternal–fetal interface in the first trimester. However, whether and how hypoxia regulates biofunctions of dMφ remain elusive. Herein, we observed increased expression of C–C motif chemokine ligand 2 (CCL2) and residence of macrophages in decidua compared to secretory-phase endometrium. Moreover, hypoxia treatment on stromal cells improved the migration and adhesion of dMφ. Mechanistically, these effects might be mediated by upregulated CCL2 and adhesion molecules (especially ICAM2 and ICAM5) on stromal cells in the presence of endogenous vascular endothelial growth factor-A (VEGFA) in hypoxia. These findings were also verified by recombinant VEGFA and indirect coculture, indicating that the interaction between stromal cells and dMφ in hypoxia condition may facilitate dMφ recruitment and residence. In conclusion, VEGFA derived from a hypoxic environment may manipulate CCL2/CCR2 and adhesion molecules to enhance the interactions between dMφ and stromal cells and thus contribute to the enrichment of macrophages in decidua early during normal pregnancy.

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Xin Wen Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China
Department of Pediatric Urology, Key Laboratory of Children Genitourinary Diseases of Wenzhou City, Key Laboratory of Structural Malformations in Children of Zhejiang Province, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Jiexia Wang Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China
Department of Pediatric Urology, Key Laboratory of Children Genitourinary Diseases of Wenzhou City, Key Laboratory of Structural Malformations in Children of Zhejiang Province, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Mengjie Qin Department of Pharmacology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Hu Wang Zhejiang Provincial Key Laboratory of Anesthesiology, Department of Anesthesiology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Jingfeng Xu Zhejiang Provincial Key Laboratory of Anesthesiology, Department of Anesthesiology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Xiaoju Guan Department of Pediatric Urology, Key Laboratory of Children Genitourinary Diseases of Wenzhou City, Key Laboratory of Structural Malformations in Children of Zhejiang Province, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Dan Shan Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Panpan Chen Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Jiajia Xie Department of Pharmacology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Jingjing Shao Department of Pharmacology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Ping Duan Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Congde Chen Department of Pediatric Urology, Key Laboratory of Children Genitourinary Diseases of Wenzhou City, Key Laboratory of Structural Malformations in Children of Zhejiang Province, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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Haolin Chen Department of Gynecology and Obstetrics, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China
Department of Pediatric Urology, Key Laboratory of Children Genitourinary Diseases of Wenzhou City, Key Laboratory of Structural Malformations in Children of Zhejiang Province, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China
Department of Pharmacology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China
Zhejiang Provincial Key Laboratory of Anesthesiology, Department of Anesthesiology, the Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, Zhejiang, China

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In brief

Progenitor cells with ovulation-related tissue repair activity were identified with defined markers (LGR5, EPCR, LY6A, and PDGFRA), but their potentials to form steroidogenic cells were not known. This study shows that the cells can generate progenies with different steroidogenic activities.

Abstract

Adult mammalian ovaries contain stem/progenitor cells necessary for folliculogenesis and ovulation-related tissue rupture repair. Theca cells are recruited and developed from progenitors during the folliculogenesis. Theca cell progenitors were not well defined. The aim of current study is to compare the potentials of four ovarian progenitors with defined markers (LY6A, EPCR, LGR5, and PDGFRA) to form steroidogenic theca cells in vitro. The location of the progenitors with defined makers was determined by immunohistochemistry and immunofluorescence staining of ovarian sections of adult mice. Different progenitor populations were purified by magnetic-activated cell sorting (MACS) and/or fluorescence-activated cell sorting (FACS) techniques from ovarian cell preparation and were tested for their abilities to generate steroidogenic theca cells in vitro. The cells were differentiated with a medium containing LH, ITS, and DHH agonist for 12 days. The results showed that EPCR+ and LGR5+ cells primarily distributed along the ovarian surface epithelium (OSE), while LY6A+ cells distributed in both the OSE and parenchyma. However, PDGFRA+ cells were exclusively located in interstitial compartment. When the progenitors were purified by these markers and differentiated in vitro, LY6A+ and PDGFRA+ cells formed steroidogenic cells expressing both CYP11A1 and CYP17A1 and primarily producing androgens, showing characteristics of theca-like cells, while LGR5+ cells generated steroidogenic cells devoid of CYP17A1 expression and androgen production, showing a characteristic of progesterone-producing cells (granulosa- or lutea-like cells). In conclusion, progenitors from both OSE and parenchyma of adult mice are capable of generating steroidogenic cells with different steroidogenic capacities, showing a possible lineage preference.

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Hai-Yan Hou Chinese Academy of Medical Sciences & Peking Union Medical College, Peking Union Medical College Hospital, Beijing, People’s Republic of China
Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Xi Wang Chinese Academy of Medical Sciences & Peking Union Medical College, Peking Union Medical College Hospital, Beijing, People’s Republic of China

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Qi Yu Chinese Academy of Medical Sciences & Peking Union Medical College, Peking Union Medical College Hospital, Beijing, People’s Republic of China

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Hong-Yi Li Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Shao-Jie Li Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Rui-Yi Tang Chinese Academy of Medical Sciences & Peking Union Medical College, Peking Union Medical College Hospital, Beijing, People’s Republic of China

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Zai-Xin Guo Chinese Academy of Medical Sciences & Peking Union Medical College, Peking Union Medical College Hospital, Beijing, People’s Republic of China

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Ya-Qiong Chen Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Chun-Xiu Hu Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Zhi-Juan Yang Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Wen-ke Zhang Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Yan Qin Department of Obstetrics and Gynecology, Characteristic Medical Center of PAP, Tianjin, People’s Republic of China

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Decline in successful conception decreases more rapidly after 38 years of age owing to follicular depletion and decreased oocyte quality. However, limited information is available regarding the underlying mechanism and the useful treatment. This study aimed to evaluate the effects of growth hormone supplementation on oocyte maturation in vivo in aged and young mice and to determine its effect on mitochondrial function. The influence of three different doses of recombinant human growth hormone (rhGH) (0.4, 0.8 and 1.6 mg/kg/day) for 8 weeks before ovarian stimulation was analyzed. Superovulated oocytes were released from the oviduct of 12-week-old and 40-week-old female C57BL/6J mice 14–16 h after administration of human chorionic gonadotropin. Ovarian follicle and morphological analysis and oocyte maturation parameters were then evaluated. This study is the first, to our knowledge, to report that medium- and high-dose rhGH significantly increases antral follicles in aged mice but anti-Müllerian hormone (AMH) levels. Furthermore, derived oocytes, MII-stage oocyte rate, ATP levels, mitochondrial membrane potential and frequencies of homogeneous mitochondrial distribution increased. In contrast, in both aged and young mice, the mtDNA copy numbers per oocyte were similar before rhGH administration, and upon saline administration, they did not differ significantly. We conclude that medium-dose rhGH supplementation before standard ovarian stimulation regimens improves oocyte quality in aged mice, probably by enhancing mitochondrial functionality.

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Ning-Xin Qin Department of Assisted Reproductive Medicine, Shanghai First Maternity and Infant Hospital, School of Medicine, Tongji University, Shanghai, China

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Yi-Ran Zhao The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Wei-Hui Shi The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Zhi-Yang Zhou The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Ke-Xin Zou The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Chuan-Jin Yu The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Xia Liu The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Ze-Han Dong The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Yi-Ting Mao The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Cheng-Liang Zhou The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Jia-Le Yu The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Xin-Mei Liu Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China

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Jian-Zhong Sheng Department of Pathology and Pathophysiology, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

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Guo-Lian Ding Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China

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Wen-Long Zhao The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China

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Yan-Ting Wu Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China

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He-Feng Huang The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
Shanghai Key Laboratory of Embryo Original Diseases, Shanghai, China
Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
The Key Laboratory of Reproductive Genetics (Zhejiang University), Ministry of Education, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

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The number of children born after assisted reproductive technology (ART) is accumulating rapidly, and the health problems of the children are extensively concerned. This study aims to evaluate whether ART procedures alter behaviours in male offspring. Mouse models were utilized to establish three groups of offspring conceived by natural conception (NC), in vitro fertilization and embryo transfer (IVF-ET), and frozen-thawed embryo transfer (IVF-FET), respectively. A battery of behaviour experiments for evaluating anxiety and depression levels, including the open field test (OFT), elevated plus maze (EPM) test, light/dark transition test (L/DTT), tail suspension test (TST), forced swimming test (FST), and sucrose preference test (SPT) was carried out. Aged (18 months old), but not young (3 months old), male offspring in the IVF-ET and IVF-FET groups, compared with those in the NC group, exhibited increased anxiety and depression-like behaviours. The protein expression levels of three neurotrophins in PFC or hippocampus in aged male offspring from the IVF-ET and IVF-FET groups reduced at different extent, in comparison to NC group. RNA sequencing (RNA-Seq) was performed in the hippocampus of 18 months old offspring to further explore the gene expression profile changes in the three groups. KEGG analyses revealed the coexisted pathways, such as PI3K-Akt signalling pathway, which potentially reflected the similarity and divergence in anxiety and depression between the offspring conceived by IVF-ET and IVF-FET. Our research suggested the adverse effects of advanced age on the psychological health of children born after ART should be highlighted in the future.

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