Nakamura Keigo, Kusama Kazuya, Bai Rulan, Sakurai Toshihiro, Isuzugawa Kazuto, Godkin James D, Suda Yoshihito, Imakawa Kazuhiko
Animal Resource Science Center, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Ibaraki, Japan.
Department of Food, Agriculture and Environment, Miyagi University, Miyagi, Japan.
PLoS One. 2016 Jun 28;11(6):e0158278. doi: 10.1371/journal.pone.0158278. eCollection 2016.
Biochemical and/or physical communication between the conceptus and the uterine endometrium is required for conceptus implantation to the maternal endometrium, leading to placentation and the establishment of pregnancy. We previously reported that in vitro co-culture system with bovine trophoblast CT-1 cells, primary uterine endometrial epithelial cells (EECs), and uterine flushings (UFs) mimics in vivo conceptus attachment process. To identify molecules in UFs responsible for this change, we first characterized protein contents of UFs from day 17 cyclic (C17) and pregnant (P17) ewes through the use of two dimensional-Polyacrylamide Gel Electrophoresis (2D-PAGE), followed by Liquid Chromatography-tandem Mass Spectrometry (LC-MS/MS) analysis. These analyses identified 266 proteins specific for P17 UFs, from which 172 proteins were identified as exosomal proteins. Among 172 exosomal proteins, 8 proteins that had been identified as exosomal proteins were chosen for further analysis, including macrophage-capping protein (CAPG), aldo-keto reductase family 1, member B1 protein (AKR1B1), bcl-2-like protein 15 (BCL2L15), carbonic anhydrase 2 (CA2), isocitrate dehydrogenase 2 (IDH2), eukaryotic translation elongation factor 2 (EEF2), moesin (MSN), and ezrin (EZR). CAPG and AKR1B1 were again confirmed in P15 and P17 UFs, and more importantly CAPG and AKR1B1, mRNA and protein, were found only in P15 and P17 conceptuses. Moreover, exosomes were isolated from C15, C17, P15, or P17 UFs. Only P15 and P17 exosomes, originated from the conceptus, contained interferon tau (IFNT) as well as CAPG and AKR1B1, and up-regulated STAT1, STAT2, MX1, MX2, BST2, and ISG15 transcripts in EECs. These observations indicate that in addition to endometrial derived exosomes previously described, conceptus-derived exosomes are present in UFs and could function to modify endometrial response. These results suggest that exosomes secreted from conceptuses as well as endometria are involved in cell to cell interactions for conceptus implantation to the maternal endometrium.
胚胎植入母体子宫内膜以实现胎盘形成和妊娠建立,需要胚胎与子宫内膜之间进行生化和/或物理通讯。我们之前报道过,牛滋养层CT-1细胞、原代子宫内膜上皮细胞(EECs)和子宫冲洗液(UFs)的体外共培养系统可模拟体内胚胎附着过程。为了鉴定UFs中负责这一变化的分子,我们首先通过二维聚丙烯酰胺凝胶电泳(2D-PAGE),然后进行液相色谱-串联质谱(LC-MS/MS)分析,对来自第17天周期(C17)和妊娠(P17)母羊的UFs的蛋白质含量进行了表征。这些分析鉴定出了266种P17 UFs特有的蛋白质,其中172种蛋白质被鉴定为外泌体蛋白。在172种外泌体蛋白中,选择了8种已被鉴定为外泌体蛋白的蛋白质进行进一步分析,包括巨噬细胞帽蛋白(CAPG)、醛酮还原酶家族1成员B1蛋白(AKR1B1)、bcl-2样蛋白15(BCL2L15)、碳酸酐酶2(CA2)、异柠檬酸脱氢酶2(IDH2)、真核翻译延伸因子2(EEF2)、埃兹蛋白(MSN)和ezrin(EZR)。CAPG和AKR1B1在P15和P17 UFs中再次得到证实,更重要的是,仅在P15和P17胚胎中发现了CAPG和AKR1B1的mRNA和蛋白质。此外,从C15、C17、P15或P17 UFs中分离出了外泌体。仅源自胚胎的P15和P17外泌体含有干扰素τ(IFNT)以及CAPG和AKR1B1,并上调了EECs中的STAT1、STAT2、MX1、MX2、BST2和ISG15转录本。这些观察结果表明,除了先前描述的子宫内膜来源的外泌体之外,胚胎来源的外泌体也存在于UFs中,并可能起到改变子宫内膜反应的作用。这些结果表明,胚胎和子宫内膜分泌的外泌体参与了胚胎植入母体子宫内膜的细胞间相互作用。