受精卵在发育过程中的死亡和胚胎附植阶段的丢失,会引起母畜产仔数降低和繁殖能力低下,是妊娠失败的重要因素。胚胎附植是指囊胚后期的胚胎在子宫内游离一段时间后,经过发育、迁移、定位、黏附和侵入,逐步与子宫内膜建立结构和生理上联系的过程。附植是母畜妊娠过程的关键环节,通过提高胚胎着床率增加产仔数,可提高家畜的繁殖效率。其决定因素包括胚胎活力、子宫内膜容受性和胚胎与母体间的相互作用[1],其中子宫内膜容受性是胚胎植入成功的关键。为了提高子宫内膜容受性,子宫内膜基质细胞需要快速增殖分化为蜕膜细胞,这个过程被称为蜕膜化。通过高通量测序等技术发现,miRNAs、lncRNAs和circRNAs通过与其靶基因互作,参与调控母畜子宫的生理功能,最终影响胚胎附植和妊娠建立。
子宫内膜生理状态对妊娠的维持和成功至关重要,最终影响家畜的繁殖性能,因此有必要探讨影响子宫内膜容受性和蜕膜化的作用机制。本文总结了近年来miRNAs、lncRNAs和circRNAs对哺乳动物子宫内膜容受性建立和蜕膜化过程的调节作用,有助于详细地了解ncRNAs调控子宫生理功能的分子机制,确定其在家畜子宫发育过程中的作用,对提高哺乳动物的繁殖率具有重要意义。
1 子宫内膜容受性和蜕膜化子宫内膜容受性建立和蜕膜化过程是复杂且动态协调的生理过程,会受到基因和分子的时空调控,形成特殊的子宫腔微环境,促使子宫内膜达到最佳生理状态。
1.1 子宫内膜容受性子宫内膜容受性是指子宫内膜允许囊胚定位、黏附、侵入并最终着床的能力。在哺乳动物中,子宫内膜容受性对于胚胎的成功着床至关重要[2]。为了着床成功,子宫内膜会根据生理特征发生形态和结构的改变,包括子宫内膜基质细胞增殖和上皮细胞分化,最终会在雌激素和孕酮的协同作用下转变为可以接受胚胎黏附的状态,使胚胎黏附和成功着床成为可能[3]。如果子宫内膜不能“接受”,胚泡就不能着床。这种接受性会受到分子介质的影响,包括生长因子、细胞因子、趋化因子、脂质和黏附分子等[4],其表达主要受雌激素和孕酮的调节。许多基因也参与调控该过程,Labarta等[5]已经描述了140种子宫内膜相关基因,如GPX3、PAEP和LIF等,它们在孕酮水平升高时表达水平发生改变,这与细胞黏附、子宫内膜重塑以及容受性调节有关。
由于判断子宫内膜容受性的传统方法是简单地进行子宫内膜的形态学观察,不能充分判断容受性状况,需要更有效的方法来评估子宫内膜容受性的情况。鉴于子宫内膜容受性建立过程中ncRNAs动态表达,所以探究ncRNAs如何调控子宫内膜容受性,对于了解哺乳动物妊娠过程至关重要。
1.2 子宫内膜蜕膜化在侵入性着床的啮齿和灵长类动物胚胎附植过程中,胚胎可以附着在接受性子宫内膜腔上皮上,并侵入基质层,响应胚胎侵袭的基质细胞在蜕膜化过程中会增殖分化形成蜕膜细胞。虽然子宫内膜上皮细胞是胚泡启动着床的第一接触点,但异常的蜕膜化也会导致妊娠丢失,对于母体妊娠的建立和维持至关重要。蜕膜化可被视为排卵后子宫内膜为怀孕做准备的过程,有助于子宫止血、血管生成和胚胎着床,并能提高妊娠期间的免疫能力[6]。研究发现,在小鼠妊娠的第4天(第1天=阴道塞),卵巢孕酮和植入前雌二醇分泌使子宫接受胚泡,这是胚胎植入和蜕膜化的先决条件;大约在第5天下午,位于植入胚泡周围基质细胞会分化为蜕膜细胞并形成初级蜕膜区(PDZ);在怀孕的第6~7天,邻近PDZ的基质细胞继续增殖并分化为多倍体蜕膜细胞,形成次级蜕膜区(SDZ);在妊娠第7天,构成PDZ的细胞已经通过凋亡发生进行性退化,并且在第8天大部分已经消失;第8天之后,胎盘和胚胎生长缓慢取代SDZ[7]。对于人类来说,在蜕膜化过程中,子宫内膜成纤维细胞会转化为分泌细胞,同时产生蜕膜细胞的表型标记物,如催乳素(PRL)和胰岛素样生长因子结合蛋白-1(IGFBP-1)[8-9]。
月经周期中激素水平的变化会诱导人类子宫内膜基质细胞的自发蜕膜化[10],但小鼠子宫直到胚胎接触子宫上皮进行着床后才会经历蜕膜化[11]。总之,对于多数灵长类和啮齿类动物来说,必须发生蜕膜化,着床才能正常进行。因此,了解ncRNAs与蜕膜化之间的相关性,是研究调控蜕膜化机制的重要切入点,也为探究其在蜕膜化中的重要作用提供理论基础。
2 ncRNAs调控子宫内膜容受性和蜕膜化的作用机制母体子宫微环境对胚胎着床和胎儿出生后健康状况有长期影响,已在妊娠期检测到大量的ncRNAs,包括在子宫内膜和胚胎中。ncRNAs作为一种重要的表观遗传因子,通过影响哺乳动物子宫内膜容受性和蜕膜化过程相关基因和蛋白表达,直接或间接地调控子宫生理功能,最终影响胚胎附植[12] (图 1)。
2.1.1 miRNAs的特点和功能 miRNAs是大约19~25个核苷酸长的单链非编码小分子RNA,成熟的miRNAs通过互补配对方式与靶mRNA 3′-UTR或5′-UTR上的miRNA反应元件(MRE)结合,最终在转录后水平抑制靶基因表达,其中miRNA和mRNA之间的序列互补程度决定了调节的强度[13]。在典型的miRNA生物发生途径中[14],miRNA的基因组DNA依次通过RNA聚合酶II、RNase III酶Drosha和RNase III酶Dicer转录和切割最终生成miRNA双链体[15]。除了典型的miR生物合成途径外,还报道了独立于Drosha或Dicer的其他途径[16],如mirtron途径,即某些脱节的内含子模仿pre-miRNA的结构特征,在没有Drosha介导的裂解下进入miRNA加工途径。通过测序、敲除miRNA生成过程中的关键基因以及过表达或抑制miRNA表达量等方法,揭示了miRNA在雌性哺乳动物生殖过程的作用机制,包括胚胎发育、着床前子宫内膜的重塑和胎盘形成[17]。
2.1.2 lncRNAs的特点和功能 lncRNAs分布于细胞核或细胞质中,是长度超过200个核苷酸的转录产物[18],经常被加帽、聚腺苷酸化和剪接,在转录或转录后进行表观遗传修饰影响基因表达[19]。lncRNAs已被证明在多种生理功能中发挥作用,如蛋白质支架、染色质成环和mRNA稳定性的调节[20]。此外,lncRNAs可能潜在地与miRNAs相互作用。一方面,lncRNAs可能作为竞争性内源性RNA(ceRNAs),即miRNAs海绵或拮抗剂,通过降低miRNAs的表达和活性,在转录后水平调控miRNAs靶基因的表达;另一方面,miRNAs也可以抑制lncRNAs的表达[21]。lncRNAs与卵巢发育、胚胎发育和胎盘形成等发育过程有关,提示lncRNAs在雌性哺乳动物的生殖过程中发挥重要的作用[22-23]。
2.1.3 circRNAs的特点和功能 circRNAs是一类具有闭合环状结构的内源非编码RNA,没有游离的5′或3′端,富含MRE,可通过多种机制发挥生物学功能。既可竞争性地结合内源性miRNAs,解除miRNAs对靶基因的抑制作用,调节靶基因的表达水平,也可以通过翻译蛋白质或与蛋白质相互作用,参与调控多种生理过程。例如circRNAs在奶山羊的预接受和接受胚胎植入期间存在不同的表达水平[24],表明circRNAs可能在哺乳动物胚胎附植过程中起关键性的调控作用。
2.2 ncRNAs调控子宫内膜容受性的作用机制本小节归纳了与家畜子宫内膜容受性相关的ncRNAs及其与靶基因的互作关系(表 1),旨在确定其调控哺乳动物子宫生理功能的作用机制。
2.2.1 miRNAs调控子宫内膜容受性 近年来各种研究强调了miRNAs在子宫内膜容受性中的重要性[25-26]。白血病抑制因子(LIF)在子宫内膜容受性和着床中发挥重要作用,已得到充分证实[27],在评估靶向LIF的miRNAs的研究中,miR-181和miR-223影响小鼠子宫内膜中LIF的表达,并抑制胚胎植入过程[28-29]。环氧化酶-2基因(Cox-2)也被确定为小鼠胚胎植入的关键分子,研究发现miR-101a和miR-199a可靶向Cox-2基因降低子宫内膜容受性[30]。miR-199a也可以靶向黏蛋白-1(MUC1)提高子宫内膜容受性,MUC1被确立为维持鼠子宫内膜上皮细胞非接受状态的关键分子[31]。此外,let-7和miR-192[32]同样也可以调节MUC1的表达水平影响小鼠的子宫内膜容受性。许多研究还集中在miR-30 d上,认为其是子宫内膜容受性的有利标志[33]。Kuokkanen等[34]研究中发现,miR-30 d在人妊娠晚期子宫内膜中的表达低于中期子宫内膜。另外,多氯联苯可以通过抑制miR-30 d的表达影响上皮间质转化(EMT)调控因子Snai1的水平,降低子宫内膜容受性[35]。在哺乳动物妊娠过程中,EMT过程对于胚胎成功植入和发育至关重要,一些miRNAs可以通过调节EMT来影响子宫容受性[36-37]。例如,miR429通过靶向参与细胞黏附和细胞形态的原钙蛋白8(Pcdh8)抑制EMT过程[38];来源于滋养层细胞外泌体的miR-1290通过靶向LHX6促进子宫内膜上皮细胞的EMT过程,提高子宫容受性[39]。有趣的是,关于miR-23a在子宫内膜容受性调节中的作用,存在相互矛盾的结果。一项研究表明miR-23a下调cullin-3(CUL3)的表达以提高Ishikawa细胞的容受性[40],而其他研究表明CUL3的下调导致β-catenin的上调,最终损害而不是提高子宫内膜容受性和着床率[41-42]。另外,奶山羊胚胎植入过程中与子宫内膜容受性相关的miRNAs,如miR-182[43]、miR-26a[44]和miR-449a[45]被发现在奶山羊子宫正常的生理过程中起重要作用,能分别通过靶向PTN、PTEN和LGR,提高奶山羊的子宫内膜容受性。β-catenin/Wnt信号通路在子宫内膜容受性的调节中变得越来越重要[46],部分miRNAs可以通过影响该通路调控容受性。Li等[41]证明,let-7-a/g可以通过抑制β-catenin/Wnt通路改善子宫内膜容受性;Zheng等[47]表明,miR-200c通过靶向基因岩藻糖基转移酶4(FUT4)间接灭活β-catenin/Wnt信号,导致子宫内膜容受性和着床受损。此外,miRNAs在反复着床失败(RIF)的妇女子宫内膜容受性中也发挥重要作用[48],miR-183-5p的下调可提高catenin-2(CTNNA2)的表达显著降低RIF的妇女的子宫内膜容受性,从而导致着床失败[42];miR-135b在不孕妇女中表达升高,通过抑制同源盒A10(HOX A10)的表达降低子宫内膜容受性[49]。基于此,miRNAs可通过影响容受性因子和相关信号通路促进或抑制子宫内膜容受性的建立。
2.2.2 lncRNAs调节子宫内膜容受性 除了miRNAs,lncRNAs也被认为在调节子宫内膜容受性和着床中发挥关键作用,并认为其是子宫内膜容受性的生物标志物[50]。Lin等[51]的研究表明,lncRNA-miRNA-mRNA调控网络与子宫内膜容受性中涉及的生物学过程相关。研究表明,特定的mRNAs、miRNAs和lncRNAs在RIF妇女的分泌期子宫内膜中有差异表达,表明与子宫内膜容受性缺陷有关[52]。在猪等其他物种中,lncRNAs的表达在第9天至第15天的子宫内膜中有差异,这种差异与猪在第12天左右的植入准备过程中子宫内膜的功能状态变化有关,表明了lncRNAs可以在子宫内膜中发挥调节作用,并有助于子宫内膜-胚胎串扰[53];Su等[54]研究表明,在猪子宫内膜上皮细胞中lncRNAXLOC-2222497通过调节醛酮还原酶家族1成员C1(AKR1C1),参与孕酮代谢过程最终影响胚胎附植。Li等[55]第一次发现lnc01060和lnc01104是潜在的子宫内膜容受性相关标记,为lncRNAs作为判断子宫容受性的分子标志提供新的思路。lncRNAs也可通过多种途径影响子宫内膜容受性的建立。如lncRNA H19会通过lncRNA H19/let-7/IGF1R或lncRNA H19/let-7/ITGβ3途径影响子宫内膜容受性和胚胎植入过程[56-57];linc02349可以通过Wnt途径影响子宫内膜容受性[58-59];linc02190可以通过与启动子的150-250 BP区域结合来降低整合素AD(ITGAD)的表达,并抑制胚胎在子宫内膜上附着,导致RIF的发生[60];lncRNAENST00000433673可能通过促进ICAM1 mRNA的表达和子宫内膜上皮细胞的黏附,最终提高胚胎-子宫内膜附着效率[61]。Zhang等[62]还阐明了受雌激素和孕激素调节的lncRNA882可充当miR-15b的竞争性内源性RNA,间接调节山羊子宫内膜上皮细胞LIF的表达水平,有助于提高奶山羊子宫内膜的容受性。Liu和Gong[63]研究表明lncRNA-TCL6通过调节容受性因子表皮生长因子受体(EGFR)表达,促进早期流产并抑制胎盘植入。Cai等[64]通过研究子宫内膜异位症的大鼠在着床窗口期子宫中lncRNA和mRNA的表达谱,发现lncRNA和mRNA表达的变化可能影响大鼠的子宫内膜容受性,最终会导致胚胎着床失败。可见,lncRNAs在子宫内膜容受性的调节中发挥重要作用。
2.2.3 circRNAs调控子宫内膜容受性 circRNAs可作为miRNA分子海绵对子宫生理功能起到重要的调控作用。研究表明,circ-8073作为分子海绵介导miR-449a调控CEP55,通过PI3K/AKT/mTOR通路促进子宫内膜上皮细胞的增殖,其中CEP55可调控子宫内膜上皮细胞中血管内皮生长因子(VEGF)和叉头盒M1(FOXM1)的表达水平,提高子宫内膜容受性[65]。circRNA-9119通过靶向miR-26降低其表达水平,miR-26a又进一步影响体外奶山羊子宫内膜上皮细胞中预测的靶位点下调前列腺素内过氧化物合酶2(PTGS2)的表达,提高子宫内膜容受性[66]。此外,Shen等[67]证实,circBACH1可能作为miRNAs的ceRNA影响子宫内膜容受性。Ma等[68]发现Circ-9110可通过吸附miR-100-5p提高HOX A1的表达,又进一步调控PI3K/AKT/mTOR和ERK1/2通路来诱导山羊子宫基质细胞凋亡,提高子宫容受性,最终促进胚胎植入过程。另外,Zhang等[69]通过对梅山猪和约克夏猪子宫内膜样品中circRNA-miRNA-mRNA的表达分析得出,circ0001470可以促进子宫内膜上皮细胞的增殖和周期进程,并且通过降低miR-140-3p调节下游PTGFR表达,改善子宫内膜容受性调控胚胎着床过程。同时,通过体内试验表明,circGRN也通过影响PTGFR的表达,激活MAPK通路,提高子宫容受性[69]。Zhao等[70]发现,HSA-CIRC-0038383/miR-196b-5p/HOX A9轴可能是影响子宫容受性和胚胎着床的关键途径,即Circ-0038383作为miR-196b-5p的分子海绵,调节HOX A9的表达,提高子宫容受性。
总之,miRNAs、lncRNAs和circRNAs通过参与子宫内膜容受性的调节,影响胚胎附植过程,也为未来哺乳动物子宫内膜的转录组研究和妊娠的分子调控提供了有价值的信息。
2.3 ncRNAs调控子宫内膜蜕膜化的作用机制本小节总结了参与调控子宫内膜蜕膜化的ncRNAs及其作用(表 2),为多层次探究家畜子宫蜕膜化调控机制提供参考。
2.3.1 miRNAs调节子宫蜕膜化 已经证明miRNAs参与蜕膜化的调节。Estella等[71]发现,当人类子宫内膜基质细胞体外蜕膜化后,共有26种上调和17种下调的miRNAs。另外,Jimenez等[72]发现miR-200通过抑制锌指E盒结合同源盒1和2(ZEB1和ZEB2)的表达促进人类子宫内膜基质细胞的蜕膜化。Ma等[73]发现,RIF患者的miR-22水平升高,Tiam/Rac1水平降低,抑制蜕膜化过程,这是一种被认为在早期基质细胞蜕膜化中具有潜在重要性的信号通路。且在RIF患者体内,miR-148a的过度表达可以通过抑制同源盒C8(HOXC8)的水平影响其蜕膜化[74]。Yan等[75]和Zhang等[76]从人子宫内膜分离的原代基质细胞,将Kruppel样因子12(KLF12)鉴定为miR-21和miR-181a的靶基因,两种miRNAs都通过下调KLF12的表达促进体外蜕膜化过程。同时,Zhang等[76]也证明了miR-181a刺激人类子宫内膜基质细胞蜕膜化相关基因,如FOXO1A、PRL、IGFBP-1、DCN和TIMP3,从而促进其形态学转化。此外,Graham等[77]证实在人类子宫内膜基质细胞系中,miR-181b下调金属蛋白酶组织抑制因子3(TIMP-3)和膜联蛋白A2,但总体上不显著影响蜕膜化过程。Qian等[78]表明,miR-222可通过介导CDKN1C/p57kip2调节子宫内膜基质细胞分化,影响细胞周期进程,促进基质细胞向蜕膜细胞转化。另外,Tochigi等[79]证明了miR-542-3p转染后抑制了IGFBP-1的基因表达,导致人类子宫内膜基质细胞蜕膜化受到抑制,这表明miR-542-3p在子宫内膜蜕膜化的调节中起重要作用。Yu等[80]研究表明miR-375可以引起NADPH氧化酶4(NOX4)下调减少活性氧(ROS)的产生并抑制子宫内膜基质细胞的蜕膜化。另外miR-542-3p[81]和miR-194-3p[82]分别下调ILK途径和PR抑制蜕膜化过程。此外,miR-96在鼠子宫内膜基质细胞的蜕膜化中起重要作用。Yang等[83]的研究发现, 在鼠子宫内膜基质细胞中miR-96水平与抗凋亡蛋白B细胞淋巴瘤2(Bcl2)的表达呈负相关促进蜕膜化过程;Shen等[84]研究表明,miR-96靶向Kruppel样因子13(Klf13),可能调节小鼠中的孕酮受体影响蜕膜化过程。另外,miR-200a[84]和miR-141[85]靶向鼠子宫内膜基质细胞中的相同基因,通过负调节磷酸酶和张力蛋白同源物(PTEN)的表达,影响蜕膜化过程中细胞的增殖和凋亡,最终抑制蜕膜化过程。像Bcl2一样,PTEN也被认为参与控制基质细胞的增殖和凋亡,从而维持蜕膜化的所需环境[84]。通过对miRNAs在蜕膜化中的一系列研究,深入揭示了miRNAs调控蜕膜化的复杂性,同时也促进了其对子宫作用机制的探索。
2.3.2 lncRNAs影响子宫蜕膜化 除了miRNAs,lncRNAs也被认为在调节子宫蜕膜化过程中发挥作用,最终影响蜕膜化过程。谭丽萍等[86]发现,lincRNA ac027700参与了妊娠早期子宫内膜的蜕膜化过程。在人子宫蜕膜化过程中,lncRNA HK2P1通过调节HK2的表达加速糖酵解过程,最终促进蜕膜化过程,这是通过竞争miR-6887-3p结合位点实现的[87]。人子宫内膜基质细胞在体外通过被db-cAMP处理后,linC00473表达在蜕膜化过程中被高度诱导,并且linC00473的敲除减弱了几种关键蜕膜转录因子如PRL、IGFBP1、HOX A10、HOX A11和WNT4的表达,说明linC00473促进了蜕膜化过程的发生[88]。Hong等[89]通过对附着前阶段山羊子宫内膜的全基因组分析得出着床“窗口期”的lnc-010092,证实其可以促进胚胎着床过程,验证了差异表达的lncRNAs可以通过影响子宫内膜上部分基因的表达来调节子宫内膜的重塑。Jia等[90]证明lncRNA Hand2os1显著促进体外蜕膜过程,并增加蜕膜化标记物催乳素家族8、亚家族a、成员2(Prl8a2)和催乳素家族3、亚家族c和成员1(Prl3c1)的表达。因此,lncRNAs不仅通过竞争性结合miRNAs间接调控蜕膜化过程,还可以通过调控蜕膜相关基因的表达直接调控蜕膜化过程。
2.3.3 circRNAs调控子宫蜕膜化 相对于miRNAs和lncRNAs在子宫蜕膜化过程的广泛研究,circRNAs的研究起步较晚。研究表明,circFAM120A通过miR-29/ABHD5轴促进重复植入失败者的蜕膜化过程[91]。在人子宫内膜间质细胞中,circSTK40通过调节HSP90的活性,阻止HSP90的蛋白酶体降解,抑制蜕膜化过程,损害子宫内膜容受性[92]。Zhao等[93]发现,hsa-circ-001946可以促进细胞增殖和细胞周期过程,增加蜕膜化标记物的表达,并能通过抑制miR-135b和增加HOX A10的表达促进蜕膜化过程,最终提高子宫内膜容受性。此外,Zhang等[94]还推测circRNAs-21887可能通过调节蜕膜细胞的增殖和分化来影响胚胎着床。
鉴于miRNAs、lncRNAs和circRNAs在调控子宫蜕膜化过程中的深入研究,将为判断啮齿动物和灵长类动物子宫内膜生理状态的分子标志提供依据。这些ncRNAs并不是独立发挥作用的,而是相互协调共同调节子宫内膜蜕膜化过程。
3 总结与展望综上所述,子宫内膜容受性建立和蜕膜化是影响哺乳动物胚胎附植的两个关键过程,受到ncRNAs复杂且精密的调控。一方面,miRNAs、lncRNAs和circRNAs可以直接与调控子宫内膜容受性和蜕膜化过程的关键基因和蛋白发生作用。另一方面,lncRNAs和circRNAs可通过吸附miRNAs调控子宫生理功能,最终影响哺乳动物的胚胎附植过程。
但目前,ncRNAs对子宫调控作用的研究仍存在一定问题:1)尚未在多数哺乳动物中进行深入的功能研究,多通过对部分组织或体液进行检测,探究子宫内膜生理功能和表型变化,这在一定程度上并不能完全反映其在动物体内的正常生理状态;2)miRNAs、lncRNAs、circRNAs和mRNA之间存在的一对多和多对一的复杂互作调控关系,为ncRNAs的作用机理研究增加了一定难度。
随着多组学测序技术的对子宫ncRNAs的进一步挖掘,有以下3个方面值得探究:1)通过转录组测序鉴定新的ncRNAs,作为判断母畜繁殖能力的生物标记物,并应用到畜牧生产中;2)基于空间转录组分析技术,了解ncRNAs在雌性哺乳动物子宫中的时空特异性表达,明确其对子宫生理功能的精确调控,解析不同母畜胚胎附植的机制及其差异;3)外泌体作为细胞通讯的重要“媒介”,可通过分离卵巢颗粒细胞、卵母细胞、子宫内膜细胞、子宫腔液和血清中的外泌体,通过测序技术探究不同细胞和体液外泌体中的ncRNAs如何调控子宫生理功能,最终影响胚胎附植过程。因此,通过对这些研究方向的推进,必将更加深入地了解子宫容受性和蜕膜化过程,也为完善ncRNAs在哺乳动物子宫生理功能的调控网络提供科学依据。
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(编辑 郭云雁)