摘要
体细胞克隆技术(也称为体细胞核移植技术)具有重要的理论研究价值和生产实践价值,可应用于治疗性克隆、高价值药用蛋白的生产、抗病转基因家畜的生产、频临灭绝品种的保护、优良品种家畜的扩增繁殖、人类器官移植和疾病模型的构建等研究。但至今体细胞克隆的效率仍然不高,大量体细胞克隆胎儿在附植期或围产期死亡,出生存活的克隆动物也表现各种发育异常。目前认为,体细胞克隆效率低下的主要原因是供体细胞核不能被卵胞质完全的重编程。本文研究了体细胞克隆动物发育异常和死亡的重编程机理,以及探索通过促进重编程来提高体细胞克隆效率的方法,主要研究的内容和结果如下:
1.在发育异常体细胞克隆牛各组织上分析多个印迹基因的表达和DNA甲基化水平。巨胎症死亡组体细胞克隆牛的体重、胎盘重和单个胎盘子叶重都显著性高于对照组,但胎盘子叶数显著少于对照组。印迹基因XIST、PEG3和IGF2在巨胎症死亡组克隆牛的胎盘等多个组织上表达水平显著高于对照组;而印迹基因H19和IGF2R在巨胎症死亡组克隆牛的胎盘等多个组织上的表达水平显著低于对照组。H19甲基化差异区(DMR)的DNA甲基化水平在巨胎症死亡组牛胎盘等多个组织上显著高于对照组,呈现异常的超甲基化修饰;而XIST DMR和IGF2R DMR的DNA甲基化水平在巨胎症死亡组牛的胎盘等多个组织上显著低于对照组。体细胞克隆中这些异常的重编程(印迹基因的表达和DNA甲基化水平异常)可能和体细胞克隆牛发育异常以及死亡相关。
2.用深度测序技术高通量分析死亡体细胞克隆牛胎盘(克隆组)和正常繁殖生产牛胎盘(对照组)的差异基因表达谱、microRNA信息和全基因组甲基化信息,研究体细胞克隆牛死亡的分子机理。
(1)用RNA-seq (Q)深度测序技术高通量分析克隆组与对照组胎盘的基因表达谱,结果发现相比对照组,克隆组胎盘上有664个基因上调,有1948个基因下调。对这些差异基因进行GO显著性富集分析,发现分子功能上的催化活性、细胞位置上的组织相容性复合体及细胞表面是差异基因显著富集的项。在参与的生物过程上,差异基因有13个显著富集的项,其中大部分项都和免疫相关。差异表达基因显著富集的通路一共有25条,其中14条通路和免疫相关。
(2)用small RNA-seq深度测序技术高通量分析克隆组与对照组胎盘的microRNA信息。在克隆组和对照组胎盘上分别鉴定出了328种和344种已知的成熟microRNA,并发现169种牛的候选新microRNA。对照组和克隆组间共有135个表达显著差异的已知microRNA,其中克隆组有18个已知microRNA的表达上调,117个已知microRNA下调。两样品间有49个表达显著性差异的候选新microRNA,其中克隆组有35个microRNA的表达上调,有14个microRNA下调。
(3)用MeDIP-seq深度测序技术高通量分析克隆组与对照组胎盘上全基因组水平的DNA甲基化信息。本研究首次绘制出反刍动物(牛)的全基因组水平的DNA甲基化图谱。总体上,牛的全基因甲基化模式和其他物种动物和植物的相似。DNA甲基化主要富集在基因内(特别是内含子)和重复序列,而转录起始位点和转录终止位点的DNA甲基化水平较低。牛上大部分CpG岛为非甲基化状态。两样品间有大量差异甲基化水平的基因。共发现37191个CpG岛,甲基化的CpG岛在对照组和克隆租上分别有7482个和5461个。基因表达水平和甲基化水平反相关,转录起始位点附近更为显著,说明启动子甲基化修饰调控基因转录。
3.牛体细胞克隆胚胎上存在异常的重编程。多个基因位点在牛克隆胚胎上存在异常的甲基化修饰,XIST、OCT4、SOX2、NANOG、Rex1和Fgf4基因5’端区域的DMR的甲基化水平在牛体细胞克隆囊胚上都显著低于对照组体外受精囊胚。XIST在体细胞克隆囊胚上的表达水平显著高于对照组体外受精囊胚。H3K27me3在牛体细胞克隆囊胚上的表达异常。
4.用基因芯片高通量分析克隆效率高的细胞系获得的克隆囊胚(高效克隆组组)、克隆效率低下的细胞系获得的克隆囊胚(低效克隆组)以及孤雌囊胚三种类型的囊胚和体外受精囊胚之间的差异基因表达谱。相比体外受精组囊胚,TCF7、DGCR8、SENP7、DNMT3B、Vimentin、IFI6、EFNA2、F5、IRAK1、PRICKLE1、TNFRSF1A、ARG2和NEK6等基因在低效克隆组囊胚上表达异常,但在高效克隆组囊胚上表达正常。这些基因的异常表达可能与低效克隆组细胞系克隆效率低下有关。孤雌囊胚和体外受精囊胚间有240个显著性差异基因。PEG3和SNRPN等多个父源表达的印迹基因在孤雌囊胚上异常下调。
5.分析亮甲酚蓝(BCB)筛选不同核重编程能力的卵母细胞。结果显示用BCB筛选出的不同生长期卵母细胞具有不同的核重编程能力。来自生长完全的卵母细胞(finished growth phase)的牛体细胞克隆胚胎(BCB+)的卵裂率、囊胚发育率、以及移植后胚胎妊娠率和出生率都显著高于来自生长中的卵母细胞(growing oocytes)的克隆胚胎(BCB),说明生长完全的卵母细胞能更好地支持牛克隆胚胎体外和体内发育。BCB+组克隆胚胎上组蛋白乙酰化水平(AcH3K9和AcH3K18)以及H3K4位点的组蛋白甲基化水平高于BCB克隆胚胎,BCB+组克隆胚胎的胚胎质量(胚胎细胞数和胚胎凋亡率)也显著高于BCB克隆胚胎。BCB筛选的不同生长期的卵母细胞也影响克隆胚胎的基因表达。通过BCB筛选出的生长完全的卵母细胞具有更高的体细胞核的重编程能力,将其用于牛体细胞核移植,可提高牛体细胞克隆效率。
6.分析表观修饰药物组蛋白去乙酰化酶抑制剂Oxamflatin对体细胞克隆胚胎的重编程的影响。结果发现1μM Oxamflatin处理牛重构胚12h可提高牛克隆胚胎的AcH3K9和AcH3K18组蛋白乙酰化水平和H3K4me2组蛋白甲基化水平,下调H3K9me3组蛋白甲基化水平,降低体细胞克隆囊胚期胚胎上satellite I的DNA甲基化水平,提高克隆胚胎的质量(胚胎细胞数和胚胎凋亡率),改变克隆胚胎上基因的表达,促进牛体细胞克隆胚胎的体外发育。说明组蛋白去乙酰化酶抑制剂Oxamflatin可促进体细胞核的重编程和克隆胚胎的质量,对牛体细胞克隆胚胎的发育有显著的促进作用。
7.相比体外受精囊胚,TCF7、DGCR8、SENP7、DNMT3B、Vimentin、IFI6、EFNA2、F5、IRAK1、PRICKLE1、TNFRSF1A、ARG2、NEK6、OCT4、NANOG、SOX2、CDX2、XIST和IGF2R这些基因在克隆囊胚上表达正常的细胞系作为核供体获得的克隆胚胎比两个异常表达组的细胞系(异常表达组1是上述4.中的低效克隆组中三株已知遗传背景差的细胞系,用于供体细胞后,在克隆囊胚上TCF7、DGCR8、SENP7、DNMT3B、Vimentin、IFI6、EFNA2、F5、IRAK1、PRICKLE1、TNFRSF1A、ARG2和NEK6等大部分基因表达异常;异常表达组2是三株细胞系,用于供体细胞后,在克隆囊胚上OCT4、NANOG、SOX2、CDX2、XIST和IGF2R等几个多能性基因和印迹基因大部分表达异常)获得的克隆胚胎具有更高的体外和体内发育能力,其克隆效率显著高于两个异常表达组。依据这些基因在克隆囊胚上的表达是否正常可以作为筛选供体细胞系的依据。
本研究发现牛体细胞克隆中存在异常的重编程,表现为早期胚胎上有大量异常表达的基因、异常的DNA甲基化修饰和组蛋白修饰以及新生克隆牛上有大量异常表达的基因、microRNAs和异常的DNA甲基化修饰等。通过筛选易于重编程的供体细胞系、筛选核重编程能力较强的卵母细胞以及通过表观遗传修饰药物处理克隆胚胎,可提高体细胞克隆中的重编程效率,进而提高体细胞克隆效率。
Somatic cloning, also known as somatic cell nuclear transfer (SCNT), is apromising technology with potential applications in therapeutic cloning, producingvaluable recombinant proteins, breeding disease-resistant transgenic livestock, speciespreservation, livestock propagation, man xenotransplantation, and disease models.The cloning efficiency, however, remains low, which is a significant barrier to thewidespread use of such a promising technology. It is generally believed that the lowcloning efficiency is mostly attributed to aberrant nuclear reprogramming of the donorcell by oocytes. In the present study, the pathogenic mechanisms of developmentalabnormity in SCNT cattle were analyzed, and then how to improve the somaticcloning efficiency through enhancing nuclear reprogramming was analyzed.
1. The expression and DNA methylation status of imprinted genes in various tissuesfrom deceased cloned calves were analyzed using Quantitative RT-PCR (qRT-PCR),Bisulfite Sequencing PCR (BSP) and Combined Bisulfite Restriction Analysis(COBRA). The results showed that fetal weigh, placental weight and meanplacentome weight were larger, but the number of placentomes was smaller in thedeceased calves with Large Offspring Syndrome (LOS group) compared with thecontrol group. The XIST, PEG3and IGF2were significantly over-expressed inmultiple tissues (e.g. placenta) from the LOS group, whereas expression of H19andIGF2R was significantly reduced in multiple tissues (e.g. placenta) from the LOSgroup compared with controls. In multiple tissues (e.g. placenta) from the LOS group,H19DMR was significantly hypermethylated, but XIST DMR and IGF2R ICR weresignificantly hypomethylated compared with controls. We inferred that abnormalexpression of the imprinted genes in deceased calves could be associated with alteredDNA methylation levels at the DMRs of these imprinted genes. These alterationscould result from aberrant epigenetic nuclear reprogramming during SCNT and maydisrupt normal developmental regulation of placenta and fetus, which may result indevelopmental insufficiencies and ultimately fetal or perinatal death in cloned transgenic calves.
2. The pathogenic mechanism of developmental abnormity and death in SCNTcattle was analyzed in placenta from deceased cloned calves (SCNT group) andnormally produced female calves (control group) using Solexa sequencing.
(1) Gene expression difference analysis between SCNT and control sample usingRNA-seq (Q) HiSeq high-throughput sequencing revealed664up-regulated and1948down-regulated genes in SCNT group compared with control group. To investigatethe function distribution of differentially expressed genes (DEGs), we performed theGene Ontology (GO) enrichment analysis for the DEGs. DEGs were enriched in thefunctions of catalytic activity. DEGs were enriched in the cellular component of MHCprotein complex and cell surface. DEGs were enriched in the biological process of13GO term, most of them were related with immune system, for instance, immunesystem process, antigen processing and presentation of peptide antigen, immuneresponse, positive regulation of immune system process, and activation of immuneresponse, etc. Pathway enrichment analysis of DEGs showed that25Pathway weresignificantly enriched pathway, and most of them were related with immune system,for instance, Graft-versus-host disease, Allograft rejection, Antigen processing andpresentation, NOD and Toll-like receptor signaling pathway, Leukocytetransendothelial migration, and Autoimmune thyroid disease, etc.
(2) The microRNA information was analyzed by small RNA-seq in SCNT andcontrol placentas.328and344unique known bovine microRNAs were identified inSCNT and control placentas, respectively.169unique predicted novel bovinemicroRNAs were found in bovine placentas.135unique known microRNAs weredifferentially expressed between two samples,18microRNAs were up-regulated and117microRNAs were down-regulated in SCNT placentas compared with controls.49unique novel microRNAs were differentially expressed between two samples,35microRNAs were up-regulated and14microRNAs were down-regulated in SCNTplacentas compared with controls.
(3) The genome-wide patterns of DNA methylation were analyzed by MeDIP-seqin SCNT and control placentas. The genome-wide map of DNA methylation inruminants (cattle in this study) was, for the fist time, reported in the present study.Generally, cattle display analogous methylation pattern with that of other animals andplants. DNA methylation is enriched in the gene body regions (especially introns) andthe repetitive sequences, and depleted in the transcription start site (TSS) and the transcription termination site (TTS). Most of the CpG islands in the cattle genomewere kept in unmethylated state. There were many differentially methylated genesbetween SCNT and control placentas.37,191CpG islands were found in bovineplacentas.7,482and5,461methylated CpG islands were found in control and SCNTplacentas, respectively. The DNA methylation level of promoters was negativelycorrelated with the gene expression level, indicating its suppressive role in regulatinggene transcription.
3. Aberrant reprogramming was found in bovine cloned embryos. The XIST, OCT4,SOX2, NANOG, Rex1, and Fgf4were significantly hypomethylated in SCNTblastocysts compared with IVF blastocysts. The XIST was significantlyover-expressed in SCNT blastocysts compared with IVF blastocysts. The expressionof H3K27me3was aberrant in SCNT blastocysts compared with IVF blastocysts.
4. Global gene expression profilings were analyzed in SCNT blastocysts from celllines with high cloning efficiency (high efficiency group), SCNT blastocysts from celllines with low cloning efficiency (low efficiency group), parthenogenetic blastocysts(parthenogenesis group), and IVF blastocysts (IVF grpoup). TCF7, DGCR8, SENP7,DNMT3B, Vimentin, IFI6, EFNA2, F5, IRAK1, PRICKLE1, TNFRSF1A, ARG2,NEK6, and other genes were abnormally expressed in low efficiency group, whichnormally expressed in high efficiency group, compared with the IVF grpoup. Therewere240differentially expressed genes between parthenogenesis group and IVFgrpoup. Expression of PEG3and SNRPN, the paternally expressed imprinted genes,were significantly reduced in parthenogenetic blastocysts compared with the IVFblastocysts.
5. The differential bovine oocytes with different nuclear reprogramming capacitywere selected by Brilliant cresyl blue (BCB) staining. The results showed that oocytesof various growth stage selected by BCB staining yield different nuclearreprogramming capacity. The cloned embryos developed from oocytes of finishedgrowth phase (BCB+) showed higher cleavage rate, blastocyst rate, pregnancy rateand full term development rate than these developed from growing oocytes (BCB).Oocytes of finished growth phase support higher developmental competence ofbovine cloned embryos in vitro and in vivo. The global acetylation levels of H3K9and H3K18and the global methylation levels of H3K4in BCB+embryos at thetwo-cell stage were higher than in BCB embryos. BCB+embryos generated moretotal cells, trophectoderm (TE) cells, and inner cell mass (ICM) cells, and fewer apoptotic cells than BCB embryos. The gene expressions in BCB+and BCB blastocysts were also different. These results strongly suggest that BCB+oocytes(finished growth phase) have a higher nuclear reprogramming capacity, and that BCBstaining can be used to select developmentally competent oocytes for nuclear transfer.
6. The effects of Oxamflatin, a novel HDACi, on the nuclear reprogramming anddevelopment of bovine SCNT embryos in vitro were analyzed. The results showedthat Oxamflatin treatment (the SCNT embryos treated with1μM Oxamflatinpost-ionomycin for12h) increased the global acetylation levels of H3K9and H3K18and the global methylation levels of H3K4, but decreased the the global methylationlevels of H3K9, reduced the DNA methylation level of satellite I in SCNT blastocysts,increased total and inner cell mass (ICM) cell numbers and the ratio ofICM:trophectoderm (TE) cells, reduced the rate of apoptosis in SCNT blastocysts,modified gene expression and significantly enhanced the development of bovineSCNT embryos in vitro. The study showed that Oxamflatin modifies epigenetic statusand gene expression, increases blastocyst quality, and subsequently enhances thenuclear reprogramming and developmental potential of SCNT embryos.
7. The SCNT embryos derived from cell lines of normal expression group (TCF7,DGCR8, SENP7, DNMT3B, Vimentin, IFI6, EFNA2, F5, IRAK1, PRICKLE1,TNFRSF1A, ARG2, NEK6, OCT4, NANOG, SOX2, CDX2, XIST, and IGF2R werenormally expressed in SCNT blastocysts derived from these cell lines compare withIVF blastocysts) showed higher blastocyst rate, pregnancy rate and full termdevelopment rate than SCNT embryos derived from cell lines of two abnormalexpression groups (abnormal expression group1: low efficiency group in4.above-mentioned, TCF7, DGCR8, SENP7, DNMT3B, Vimentin, IFI6, EFNA2, F5,IRAK1, PRICKLE1, TNFRSF1A, ARG2, NEK6, and other genes were abnormallyexpressed in SCNT blastocysts derived from these cell lines compare with IVFblastocysts; abnormal expression group2: OCT4, NANOG, SOX2, CDX2, XIST andIGF2R were abnormally expressed in SCNT blastocysts derived from these cell linescompare with IVF blastocysts). Expression profiling analysis of TCF7, DGCR8,SENP7, DNMT3B, Vimentin, IFI6, EFNA2, F5, IRAK1, PRICKLE1, TNFRSF1A,ARG2, NEK6, OCT4, NANOG, SOX2, CDX2, XIST, and IGF2R in cloned embryoscould be as a method to select good donor cell lines.
Aberrant reprogramming, including alterations in gene expressions, DNAmethylation status of genes, histone modifications, and microRNAs in cloned embryos or cloned calves, was found during bovine somatic cloning, which maysubsequently result in developmental insufficiencies and ultimately fetal or perinataldeath in cloned calves. The reprogramming efficiency and even somatic cloningefficiency could be enhanced by selecting good donor cells, selecting oocytes withhigher nuclear reprogramming capacity and the treatments of cloned embryos withepigenetic drugs.
引文
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