兔雌性胚胎干细胞X染色体活性状态的研究
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摘要
X染色体的活性状态与雌性胚胎干细胞(embryonic stem cells, ES cells)或诱导多能细胞(iuduced pluripotent stem cells, iPS cells)的多能状态有重要的相关性。双活性X染色体是雌性ES或iPS细胞具有生殖系嵌合能力的一种重要标志。兔是一种常用的实验室动物,虽然已经有较多的兔ES和iPS细胞系建立,但是一直未获得具有生殖系嵌合能力的细胞系,制约了转基因兔和兔胚胎发育等相关研究的进展。至今为止,在兔ES和iPS细胞的研究中,未见有关于X染色体活性状态的报道。
本课题以B28-6、NJ12、NJ10等3株兔雌性ES细胞为研究对象,对兔雌性ES细胞X染色体活性状态进行研究。在前期研究中发现,兔雌性ES细胞系与人ES细胞类似,X染色体活性状态存在不同类别。3株兔雌性ES细胞在早期传代的条件下(P<10)均已经启动X染色体失活(Xchromosome inactive, XCI)。其中B28-6、NJ12免疫荧光染色H3K27me3点状着色,Xist正常表达,表现为一条活性一条失活的X染色体(XiXistXa)。有趣的是,余下的一株NJ10细胞系,H3K27me3点状着色,表明已经启动XCI,但是未检测到Xist表达(Xiw/oXistXa)。随着传代次数的增加,P12以后,丢失了H3K27me3修饰,表现为XCI受损(XeXa)。SCID小鼠体内分化试验及qRT-PCR检测结果提示,NJ10细胞存在体内分化能力缺陷及癌基因高表达。参考人ES细胞X染色体活性状态的分类,把B28-6、NJ12归为Ⅱ类,NJ10归为Ⅲ类ES细胞。在进一步试验中,证明了慢病毒介导过表达Oct4、Sox2、Klf4、c-Myc等4个转录因子,联合应用N2B27+LIF+2i培养体系,可以重编程NJ10细胞系。获得类似于小鼠ES细胞一样凸起克隆样生长的细胞,称为mESC-like兔ES细胞(mouse ES cell-like rabbit ES cells)。mESC-like兔ES细胞克隆形态凸起,细胞倍增时间缩短,胰酶单细胞消化传代克隆形成率高,自我更新信号通路由bFGF转化为LIF,NJ10Ⅲ类兔ES细胞类似于人ES细胞,而mESC-like兔ES细胞类似于小鼠ES细胞。最重要的是,通过X染色体活性的相关检测,SCID小鼠皮下注射体内分化能力检测,及qRT-PCR癌基因表达检测,证明了重编程不仅可以重新激活失活的X染色体,而且mESC-like兔ES细胞体内分化能力提高,癌基因表达下降。
本研究不仅证明了兔ES细胞存在多种X染色体活性状态,且与人ES细胞在X染色体活性状态上存在着保守性。也证明通过慢病毒介导过表达Oct4等转录因子,可挽救兔ES细胞存在的体内分化缺陷。这些发现为以后优化兔ES细胞的培养体系,建立具有生殖系传递能力的兔ES细胞系提供了理论依据。
The deficiency of X-inactive specific transcript (Xist) on the inactive X chromosome affects the behavior of female ES cells (Embryonic stem cells) and iPS cells (iuduced pluripotent stem cells, iPS cells). However, X chromosome instability has not been identified in other species.The rabbit is a classical experimeatal animal. Previously established rabbit ES cells and rabbit iPS cells exhibited flat colony morphology and bFGF dependence and displayed many characteristics that were similar to those of human ES cells. Although rabbit ES cells have been previously derived in several laboratories, little is known about the X chromosome status of female rabbit ES cells and its correlation with pluripotency.
In the present study, we investigated the X chromosome status of three female rabbit ES cell lines and found variations in X chromosome inactivation in early passages. Two of the rabbit ES cell lines B28-6and NJ12can be defined as class Ⅱ because they display a heterochromatic Xi with Xist RNA coating and H3K27me3foci. In contrast, the third cell line NJ10lacked Xist expression and Xist RNA coating. However, unlike the XaXa state, this cell line displayed H3K27me3foci at early passage (P8), did not express Xist during differentiation, thus indicated as Xist-deficient XiXa. Moreover, the H3K27me3foci would further lose in passaging and yield an eroded Xi (P12). Therefore, this cell line is considered to be class Ⅲ. We further found that the class Ⅲ rabbit ES cells exhibited relatively high expression levels of some oncogenes, orthologous genes of which were reported to be highly expressed in class Ⅲ human iPS cells. The class Ⅲ rabbit ES cells also showed poor differentiation in vivo compared to class Ⅱ and male rabbit ES cells. Furthermore, we found that the class Ⅲ rabbit ES cells could be converted into a mESC-like pluripotent state by overexpressing the reprogramming factors: Oct4, Sox2, Klf4and c-Myc. We examined the colony morphology, colony formation ability, transcriptional changes and the activation of signaling pathways associated with pluripotency. We found that the induced rabbit ES cells are more like mouse ES cells, which therefore defined as mESC-like rabbit ES cells. We then confirmed that the mESC-like rabbit ES cells re-obtain two active X chromosomes, meanwhile, the oncogene expression is repressed and the impaired differentiation ability in vivo is rescued.
This experiments first indicated that the X chromosome instability and the impact of Xist-deficiency in Xi might be conserved between human and rabbit. These data also revealed that forced expression of reprogramming factors under optimized culture condition can reprogram the rabbit ES cells to mESC-like state which is XaXa state. Futher these data may be informative to other groups who will attempt to derive fully pluripotent rabbit ES cells or rabbit iPS cells.
本课题以B28-6、NJ12、NJ10等3株兔雌性ES细胞为研究对象,对兔雌性ES细胞X染色体活性状态进行研究。在前期研究中发现,兔雌性ES细胞系与人ES细胞类似,X染色体活性状态存在不同类别。3株兔雌性ES细胞在早期传代的条件下(P<10)均已经启动X染色体失活(Xchromosome inactive, XCI)。其中B28-6、NJ12免疫荧光染色H3K27me3点状着色,Xist正常表达,表现为一条活性一条失活的X染色体(XiXistXa)。有趣的是,余下的一株NJ10细胞系,H3K27me3点状着色,表明已经启动XCI,但是未检测到Xist表达(Xiw/oXistXa)。随着传代次数的增加,P12以后,丢失了H3K27me3修饰,表现为XCI受损(XeXa)。SCID小鼠体内分化试验及qRT-PCR检测结果提示,NJ10细胞存在体内分化能力缺陷及癌基因高表达。参考人ES细胞X染色体活性状态的分类,把B28-6、NJ12归为Ⅱ类,NJ10归为Ⅲ类ES细胞。在进一步试验中,证明了慢病毒介导过表达Oct4、Sox2、Klf4、c-Myc等4个转录因子,联合应用N2B27+LIF+2i培养体系,可以重编程NJ10细胞系。获得类似于小鼠ES细胞一样凸起克隆样生长的细胞,称为mESC-like兔ES细胞(mouse ES cell-like rabbit ES cells)。mESC-like兔ES细胞克隆形态凸起,细胞倍增时间缩短,胰酶单细胞消化传代克隆形成率高,自我更新信号通路由bFGF转化为LIF,NJ10Ⅲ类兔ES细胞类似于人ES细胞,而mESC-like兔ES细胞类似于小鼠ES细胞。最重要的是,通过X染色体活性的相关检测,SCID小鼠皮下注射体内分化能力检测,及qRT-PCR癌基因表达检测,证明了重编程不仅可以重新激活失活的X染色体,而且mESC-like兔ES细胞体内分化能力提高,癌基因表达下降。
本研究不仅证明了兔ES细胞存在多种X染色体活性状态,且与人ES细胞在X染色体活性状态上存在着保守性。也证明通过慢病毒介导过表达Oct4等转录因子,可挽救兔ES细胞存在的体内分化缺陷。这些发现为以后优化兔ES细胞的培养体系,建立具有生殖系传递能力的兔ES细胞系提供了理论依据。
The deficiency of X-inactive specific transcript (Xist) on the inactive X chromosome affects the behavior of female ES cells (Embryonic stem cells) and iPS cells (iuduced pluripotent stem cells, iPS cells). However, X chromosome instability has not been identified in other species.The rabbit is a classical experimeatal animal. Previously established rabbit ES cells and rabbit iPS cells exhibited flat colony morphology and bFGF dependence and displayed many characteristics that were similar to those of human ES cells. Although rabbit ES cells have been previously derived in several laboratories, little is known about the X chromosome status of female rabbit ES cells and its correlation with pluripotency.
In the present study, we investigated the X chromosome status of three female rabbit ES cell lines and found variations in X chromosome inactivation in early passages. Two of the rabbit ES cell lines B28-6and NJ12can be defined as class Ⅱ because they display a heterochromatic Xi with Xist RNA coating and H3K27me3foci. In contrast, the third cell line NJ10lacked Xist expression and Xist RNA coating. However, unlike the XaXa state, this cell line displayed H3K27me3foci at early passage (P8), did not express Xist during differentiation, thus indicated as Xist-deficient XiXa. Moreover, the H3K27me3foci would further lose in passaging and yield an eroded Xi (P12). Therefore, this cell line is considered to be class Ⅲ. We further found that the class Ⅲ rabbit ES cells exhibited relatively high expression levels of some oncogenes, orthologous genes of which were reported to be highly expressed in class Ⅲ human iPS cells. The class Ⅲ rabbit ES cells also showed poor differentiation in vivo compared to class Ⅱ and male rabbit ES cells. Furthermore, we found that the class Ⅲ rabbit ES cells could be converted into a mESC-like pluripotent state by overexpressing the reprogramming factors: Oct4, Sox2, Klf4and c-Myc. We examined the colony morphology, colony formation ability, transcriptional changes and the activation of signaling pathways associated with pluripotency. We found that the induced rabbit ES cells are more like mouse ES cells, which therefore defined as mESC-like rabbit ES cells. We then confirmed that the mESC-like rabbit ES cells re-obtain two active X chromosomes, meanwhile, the oncogene expression is repressed and the impaired differentiation ability in vivo is rescued.
This experiments first indicated that the X chromosome instability and the impact of Xist-deficiency in Xi might be conserved between human and rabbit. These data also revealed that forced expression of reprogramming factors under optimized culture condition can reprogram the rabbit ES cells to mESC-like state which is XaXa state. Futher these data may be informative to other groups who will attempt to derive fully pluripotent rabbit ES cells or rabbit iPS cells.
引文
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