猪皮肤来源前体细胞多能性的分子机制
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摘要
神经嵴细胞起源于背部神经管,然后迁移到不同的组织区域形成各种各样的细胞类型。神经嵴干细胞/前体细胞可以分离自胚胎发育期和成体期的不同组织:神经嵴外植体、坐骨神经、背根节、肠神经节、角膜、骨髓、触须垫、颈动脉体和心脏。皮肤来源前体细胞(skin-derived progenitors, SKP)来自于胚胎期神经嵴干细胞,并且存在于成体期。人、啮齿类和猪的SKP细胞具有多能性,能分化产生神经胚层和中胚层起源的子代细胞。但是,关于SKP多能性的分子机制尚不清楚。本研究首先从第40-50天猪胎儿皮肤组织分离表达绿色荧光蛋白(Enhanced green fluorescence protein, EGFP)的猪皮肤来源前体细胞,证明其多向分化潜能,同时鉴定出关于其多能性和神经嵴起源的多种分子标志。其次,通过高通量基因芯片技术比较了猪SKP细胞和神经干细胞(神经球)的转录表达谱,同时比较了猪SKP细胞和SKP来源的类成纤维细胞(SKP-derived fibroblast-like cells, SFC)的基因表达谱。最后,通过基因功能注解和KEGG通路分析,发现了几种相关的细胞内源调控机制和外源信号通路,它们对调控SKP细胞的多能性起重要作用。
一SKP细胞的多能性和特异性标志分子的表达
1本研究从第40~50天猪胎儿皮肤组织中分离了表达绿色荧光蛋白的SKP细胞,其在无血清和高浓度EGF和bFGF存在时可以形成悬浮的球形结构。
2通过RT-PCR证实了猪SKP细胞共表达多能性相关基因(POU5F1、SOX2、NANOG和STAT3)和神经嵴标志分子(p75NTR、TWIST1、PAX3、SNAI2、SOX9和SOX10),这与胚胎神经嵴干细胞的表达谱类似,说明猪SKP细胞的神经嵴源性。
3通过免疫荧光细胞化学染色发现猪SKP球中POU5F1、巢蛋白、纤连蛋白和波形蛋白阳性细胞的比例分别为12.3%、15.1%、67.9%和53.7%,这说明猪SKP球具有异质性。
4通过体外诱导分化和免疫荧光细胞化学染色发现,猪SKP细胞分化培养物中存在表达微管蛋白β-III、神经丝蛋白M、GFAP、p75NTR和平滑肌肌动蛋白的阳性细胞。这说明猪SKP细胞可以分化产生神经(神经元和胶质细胞)和中胚层细胞类型(平滑肌细胞和脂肪细胞),证明其具有多向分化能力。
5通过使用不同的培养体系和实时定量PCR检测,发现四种转录因子(POU5F1、SNAI2、SOX9和PAX3)的表达水平在生长因子(EGF和bFGF)和FBS存在时有显著性差异。POU5F1、SNAI2、SOX9和PAX3可能是维持SKP细胞体外多能性的关键因子。?二猪SKP细胞和神经干细胞的基因芯片分析
1本研究从第40~50天猪胎儿大脑组织中分离了表达绿色荧光蛋白的神经干细胞/神经球(neurospheres),同时从同一个胎儿中分离了皮肤来源的前体细胞。它们在同一种培养液(DMEM/F12+B27+N2+EGF+bFGF)中可形成悬浮的球形结构。
2通过体外诱导分化和免疫荧光细胞化学染色发现,猪神经干细胞可分化形成神经和胶质细胞后代,证明其具有多能性;而猪SKP在体外能分化成神经和中胚层来源的子代细胞。
3通过RT-PCR对猪神经干细胞和SKP细胞分析发现,它们都表达NANOG、STAT3、TWIST1、p75NTR、巢蛋白、纤连蛋白和波形蛋白。但是,猪神经干细胞表达较高水平的SOX2,而且也表达GFAP。然而,SNAI2只在SKP球中表达。这说明神经干细胞和SKP球有类似的表达谱,但是有各自特异的转录状态。
4通过高通量的基因芯片技术比较了猪SKP球和神经球的转录表达谱,发现SKP球高表达254个转录物,而神经干细胞有484个转录物高表达。进一步分析发现,SKP球和神经球共同高表达142个基因,他们分别涉及核糖体功能、紧密连接、间隙连接、细胞通讯、钙离子信号、ErbB信号、JAK-STAT信号以及MAPK信号等。
5在1336个筛选出的转录物中,发现在SKP球和神经球中72个转录物的表达水平在统计学上有显著性差异(P<0.05)。这些差异表达的基因主要涉及生理过程、细胞过程、信号刺激反应、发育过程、生物过程的条件和行为。
6功能注解聚类分析发现猪SKP球和神经球共同高表达基因主要涉及以下功能:RNA结合、蛋白质的生物合成以及核糖体等。对SKP球和神经球差异表达基因功能分析发现,胶原蛋白异构体和核心蛋白聚糖在细胞通讯、皮肤发育、信号转导以及胞外基质作用等方面发挥作用。
7 KEGG通路分析发现,猪SKP球和神经球共表达基因涉及淀粉和蔗糖代谢、糖酵解、紧密连接、间隙连接、嘌呤代谢、谷氨酸盐代谢、细胞通讯、MAPK信号、钙离子信号、ErbB信号和JAK-STAT信号等通路;而它们差异表达基因主要涉及ECM受体和TGF-β信号通路。细胞通讯信号整合ECM-受体相互作用和TGF-β信号通路,可能对于维持猪SKP球和神经球特异的干细胞性质起重要作用。
三猪SKP细胞中胚层潜能的基因芯片分析
1猪SKP细胞在悬浮培养中形成球状结构,但是在血清作用下贴壁生长形成类成纤维细胞。通过体外诱导分化和免疫荧光细胞化学染色发现,在SKP细胞分化为SFC过程中,其神经分化能力逐渐丧失而仍保留中胚层分化能力。
2通过RT-PCR比较猪SKP球和SFC标志基因的表达,发现它们都表达NANOG和STAT3,以及神经嵴细胞分子标志TWIST1、SNAI2和p75NTR。然而,SOX10只在SKP细胞中表达,可能与SKP的外周神经分化潜能有关。
3通过对猪SKP和SFC细胞的转录表达谱分析发现在SKP分化为SFC细胞过程中共有401个基因的表达在统计学上有显著性差异(P<0.05),其中,305个基因表达上调和96个基因表达下调。
4通过功能注解聚类分析发现,上调表达基因主要涉及结合功能、细胞过程以及代谢过程;下调表达基因比较重要的GO(gene ontology)功能是磷酸化蛋白和结合活性。
5通过KEGG和BIOCARTA通路分析发现,下调表达基因主要涉及突触蛋白、Rac1细胞运动信号通路、Ran对有丝分裂纺锤体的调控、Dicer通路以及蛋白转运到核内等内源性机制;而上调表达基因参与了一些外源性信号通路,例如ErbB通路、MAPK通路、ECM-受体相互作用、Wnt信号、细胞通讯和TGF-β信号通路。这些内源性机制和外源性的信号通路共同调节SKP到SFC的基因转录状态改变。
6为了验证基因芯片数据,本研究通过相对标准曲线法对14个差异表达基因进行实时定量qPCR分析。定量PCR使用在制作基因芯片时扩增的cDNA作为模板。实时定量qPCR数据与基因芯片数据的表达谱类似,证明了基因芯片数据的可靠性。
Neural crest is a group of cells that originate from the dorsal neural tube, and migrate along a number of routes to various tissues, where they stop moving and contribute to various local cell types. Neural crest/progenitor stem cells have been isolated from diverse tissues during embryonic development and adulthood: embryonic neural crest explant, sciatic nerve, dorsal root ganglion, skin, enteric ganglia, cornea, bone marrow, whisker pad, carotid body and heart. Skin-derived progenitors (SKPs) are considered as embryonic neural crest derived precursor cells that persist into adulthood. SKP cells have been demonstrated to be multipotent and can produce both neural and mesodermal progeny in human, rodent and pigs. However, the molecular mechanism of the multipotency of SKPs is still illusive. Here we isolated porcine GFP transgenic SKP cells from embryonic skin and demonstrated their multipotent potential. We identified several kinds of marker genes which may contribute to their multipotency and neural crest derived property. Furthermore, we compared the transcriptional profiles of SKPs and neural stem cells (neurospheres) to dissect the neurogenic potential of porcine SKP cells by microarray analysis. Concomitantly, we deciphered the mesodermal potential of SKPs by comparing the transcriptional profiling of SKPs with SKP-derived fibroblast like cells (termed SFCs). Finally we identified several key intrinsic programs and extrinsic signaling pathways that have significance in mediating the stem-cell identity of SKPs.
1) Tracing the stemness of porcine skin derived progenitors back to specific marker gene expression
Multipotent skin derived progenitors (SKP) can produce both neural and mesodermal progeny in vitro, sharing the characteristics of embryonic neural crest stem cells. However, the molecular basis for the property of multipotency and neural crest origin of SKPs is still elusive. Here we report the cooperative expression of pluripotency related genes (POU5F1, SOX2, NANOG, STAT3) and neural crest marker genes (p75NTR, TWIST1, PAX3, SNAI2, SOX9, SOX10) in GFP-transgenic porcine skin derived progenitors (pSKP). The proportion of cells positive for POU5F1, nestin, fibronectin and vimentin were 12.3%, 15.1%, 67.9% and 53.7%, showing the heterogeneity of pSKP spheres. Moreover, pSKP cells can generate both neural (neurons and glias) and mesodermal cell types (smooth muscle cells) in vitro, indicating the multiple lineage potency. Four transcription factors (POU5F1, SNAI2, SOX9 and PAX3) were identified which were sensitive to mitogen (FBS) and/or growth factors (EGF and bFGF). It is tempting to speculate that POU5F1, SNAI2, SOX9 and PAX3 may be the key players for regulating the neural crest derived multipotency of SKP cells in vitro.
2) Dissecting the“stemness”of porcine skin derived progenitor (SKP) spheres and neurospheres by microarray analysis
Skin derived progenitors (SKP) are neural crest derived and can generate neural and mesodermal progeny in vitro, corresponding to the multipotency of neural crest stem cells. Likewise, neural stem/progenitor cells, which are self-renewing and multipotent, can display as neurospheres. Both of them form spheres in response to epidermal growth factor (EGF) and basic fibroblast growth factor (bFGF) in vitro. Although the“stemness”of neural stem/progenitor cells has been extensively investigated, direct comparison of“stemness”between SKP spheres and neurospheres is unknown. Here we dissect the“stemness”of SKP spheres and neurospheres by microarray analysis. Totally 142 genes are commonly enriched in SKP spheres and neurospheres, which are involved in ribosome, tight junction, gap junction, cell communication, calcium signaling, ErbB signaling, JAK-STAT signaling, MAPK signaling et al. Functional annotation clustering indicates that SKP spheres and neurospheres employ similar protein biosynthesis process but differential cell communication pathways. In addition, the differentially expressed genes between SKP spheres and neurospheres are most commonly involved in ECM-receptor interaction and TGF-βsignaling pathway. It is suggested that cell-communication pathways which integrate ECM-receptor interaction and TGF-βsignaling may contribute to the differential stem-cell identity of SKP spheres and neurospheres. Thus it is inferred that the ground state of stem cells could be maintained in a cell-intrinsic manner within local microenvironment mediated by cell-cell communication pathways.
3) Deciphering the mesodermal potency of porcine skin derived progenitors by microarray analysis
Skin stem cells have an essential role in maintaining tissue homeostasis by dynamically replenishing those constantly lost during tissue turnover or following injury. Multipotent skin derived progenitors (SKP) can generate both neural and mesodermal progeny, representing neural crest-derived progenitors during embryogenesis through adulthood. SKP cells develop into spheres in suspension and can differentiate into fibroblast-like cells (SFC) in adhesive culture with serum. However, little is known about the molecular mechanism of the transition of SKP spheres into SFC in vitro. Here we characterized the transcriptional profiles of porcine SKP spheres and SFC by microarray analysis. The 305 up-regulated and 96 down-regulated genes were found during transition, respectively. The down-regulated genes are mainly involved in intrinsic programs like the Dicer pathway and asymmetric cell division; whereas up-regulated genes are likely to participate in extrinsic signaling pathways such as ErbB signaling, MAPK signaling, ECM-receptor reaction, Wnt signaling, cell communication and TGF-βsignaling pathways. These intrinsic programs and extrinsic signaling pathways collaborate to mediate the transcription-state transition between SKP spheres and SFC. These potential signaling pathways may regulate self-renewal and cell fate determination of skin-derived stem cells in vivo, thus orchestrating the molecular programs of skin stem cells and morphogenesis in skin development.
一SKP细胞的多能性和特异性标志分子的表达
1本研究从第40~50天猪胎儿皮肤组织中分离了表达绿色荧光蛋白的SKP细胞,其在无血清和高浓度EGF和bFGF存在时可以形成悬浮的球形结构。
2通过RT-PCR证实了猪SKP细胞共表达多能性相关基因(POU5F1、SOX2、NANOG和STAT3)和神经嵴标志分子(p75NTR、TWIST1、PAX3、SNAI2、SOX9和SOX10),这与胚胎神经嵴干细胞的表达谱类似,说明猪SKP细胞的神经嵴源性。
3通过免疫荧光细胞化学染色发现猪SKP球中POU5F1、巢蛋白、纤连蛋白和波形蛋白阳性细胞的比例分别为12.3%、15.1%、67.9%和53.7%,这说明猪SKP球具有异质性。
4通过体外诱导分化和免疫荧光细胞化学染色发现,猪SKP细胞分化培养物中存在表达微管蛋白β-III、神经丝蛋白M、GFAP、p75NTR和平滑肌肌动蛋白的阳性细胞。这说明猪SKP细胞可以分化产生神经(神经元和胶质细胞)和中胚层细胞类型(平滑肌细胞和脂肪细胞),证明其具有多向分化能力。
5通过使用不同的培养体系和实时定量PCR检测,发现四种转录因子(POU5F1、SNAI2、SOX9和PAX3)的表达水平在生长因子(EGF和bFGF)和FBS存在时有显著性差异。POU5F1、SNAI2、SOX9和PAX3可能是维持SKP细胞体外多能性的关键因子。?二猪SKP细胞和神经干细胞的基因芯片分析
1本研究从第40~50天猪胎儿大脑组织中分离了表达绿色荧光蛋白的神经干细胞/神经球(neurospheres),同时从同一个胎儿中分离了皮肤来源的前体细胞。它们在同一种培养液(DMEM/F12+B27+N2+EGF+bFGF)中可形成悬浮的球形结构。
2通过体外诱导分化和免疫荧光细胞化学染色发现,猪神经干细胞可分化形成神经和胶质细胞后代,证明其具有多能性;而猪SKP在体外能分化成神经和中胚层来源的子代细胞。
3通过RT-PCR对猪神经干细胞和SKP细胞分析发现,它们都表达NANOG、STAT3、TWIST1、p75NTR、巢蛋白、纤连蛋白和波形蛋白。但是,猪神经干细胞表达较高水平的SOX2,而且也表达GFAP。然而,SNAI2只在SKP球中表达。这说明神经干细胞和SKP球有类似的表达谱,但是有各自特异的转录状态。
4通过高通量的基因芯片技术比较了猪SKP球和神经球的转录表达谱,发现SKP球高表达254个转录物,而神经干细胞有484个转录物高表达。进一步分析发现,SKP球和神经球共同高表达142个基因,他们分别涉及核糖体功能、紧密连接、间隙连接、细胞通讯、钙离子信号、ErbB信号、JAK-STAT信号以及MAPK信号等。
5在1336个筛选出的转录物中,发现在SKP球和神经球中72个转录物的表达水平在统计学上有显著性差异(P<0.05)。这些差异表达的基因主要涉及生理过程、细胞过程、信号刺激反应、发育过程、生物过程的条件和行为。
6功能注解聚类分析发现猪SKP球和神经球共同高表达基因主要涉及以下功能:RNA结合、蛋白质的生物合成以及核糖体等。对SKP球和神经球差异表达基因功能分析发现,胶原蛋白异构体和核心蛋白聚糖在细胞通讯、皮肤发育、信号转导以及胞外基质作用等方面发挥作用。
7 KEGG通路分析发现,猪SKP球和神经球共表达基因涉及淀粉和蔗糖代谢、糖酵解、紧密连接、间隙连接、嘌呤代谢、谷氨酸盐代谢、细胞通讯、MAPK信号、钙离子信号、ErbB信号和JAK-STAT信号等通路;而它们差异表达基因主要涉及ECM受体和TGF-β信号通路。细胞通讯信号整合ECM-受体相互作用和TGF-β信号通路,可能对于维持猪SKP球和神经球特异的干细胞性质起重要作用。
三猪SKP细胞中胚层潜能的基因芯片分析
1猪SKP细胞在悬浮培养中形成球状结构,但是在血清作用下贴壁生长形成类成纤维细胞。通过体外诱导分化和免疫荧光细胞化学染色发现,在SKP细胞分化为SFC过程中,其神经分化能力逐渐丧失而仍保留中胚层分化能力。
2通过RT-PCR比较猪SKP球和SFC标志基因的表达,发现它们都表达NANOG和STAT3,以及神经嵴细胞分子标志TWIST1、SNAI2和p75NTR。然而,SOX10只在SKP细胞中表达,可能与SKP的外周神经分化潜能有关。
3通过对猪SKP和SFC细胞的转录表达谱分析发现在SKP分化为SFC细胞过程中共有401个基因的表达在统计学上有显著性差异(P<0.05),其中,305个基因表达上调和96个基因表达下调。
4通过功能注解聚类分析发现,上调表达基因主要涉及结合功能、细胞过程以及代谢过程;下调表达基因比较重要的GO(gene ontology)功能是磷酸化蛋白和结合活性。
5通过KEGG和BIOCARTA通路分析发现,下调表达基因主要涉及突触蛋白、Rac1细胞运动信号通路、Ran对有丝分裂纺锤体的调控、Dicer通路以及蛋白转运到核内等内源性机制;而上调表达基因参与了一些外源性信号通路,例如ErbB通路、MAPK通路、ECM-受体相互作用、Wnt信号、细胞通讯和TGF-β信号通路。这些内源性机制和外源性的信号通路共同调节SKP到SFC的基因转录状态改变。
6为了验证基因芯片数据,本研究通过相对标准曲线法对14个差异表达基因进行实时定量qPCR分析。定量PCR使用在制作基因芯片时扩增的cDNA作为模板。实时定量qPCR数据与基因芯片数据的表达谱类似,证明了基因芯片数据的可靠性。
Neural crest is a group of cells that originate from the dorsal neural tube, and migrate along a number of routes to various tissues, where they stop moving and contribute to various local cell types. Neural crest/progenitor stem cells have been isolated from diverse tissues during embryonic development and adulthood: embryonic neural crest explant, sciatic nerve, dorsal root ganglion, skin, enteric ganglia, cornea, bone marrow, whisker pad, carotid body and heart. Skin-derived progenitors (SKPs) are considered as embryonic neural crest derived precursor cells that persist into adulthood. SKP cells have been demonstrated to be multipotent and can produce both neural and mesodermal progeny in human, rodent and pigs. However, the molecular mechanism of the multipotency of SKPs is still illusive. Here we isolated porcine GFP transgenic SKP cells from embryonic skin and demonstrated their multipotent potential. We identified several kinds of marker genes which may contribute to their multipotency and neural crest derived property. Furthermore, we compared the transcriptional profiles of SKPs and neural stem cells (neurospheres) to dissect the neurogenic potential of porcine SKP cells by microarray analysis. Concomitantly, we deciphered the mesodermal potential of SKPs by comparing the transcriptional profiling of SKPs with SKP-derived fibroblast like cells (termed SFCs). Finally we identified several key intrinsic programs and extrinsic signaling pathways that have significance in mediating the stem-cell identity of SKPs.
1) Tracing the stemness of porcine skin derived progenitors back to specific marker gene expression
Multipotent skin derived progenitors (SKP) can produce both neural and mesodermal progeny in vitro, sharing the characteristics of embryonic neural crest stem cells. However, the molecular basis for the property of multipotency and neural crest origin of SKPs is still elusive. Here we report the cooperative expression of pluripotency related genes (POU5F1, SOX2, NANOG, STAT3) and neural crest marker genes (p75NTR, TWIST1, PAX3, SNAI2, SOX9, SOX10) in GFP-transgenic porcine skin derived progenitors (pSKP). The proportion of cells positive for POU5F1, nestin, fibronectin and vimentin were 12.3%, 15.1%, 67.9% and 53.7%, showing the heterogeneity of pSKP spheres. Moreover, pSKP cells can generate both neural (neurons and glias) and mesodermal cell types (smooth muscle cells) in vitro, indicating the multiple lineage potency. Four transcription factors (POU5F1, SNAI2, SOX9 and PAX3) were identified which were sensitive to mitogen (FBS) and/or growth factors (EGF and bFGF). It is tempting to speculate that POU5F1, SNAI2, SOX9 and PAX3 may be the key players for regulating the neural crest derived multipotency of SKP cells in vitro.
2) Dissecting the“stemness”of porcine skin derived progenitor (SKP) spheres and neurospheres by microarray analysis
Skin derived progenitors (SKP) are neural crest derived and can generate neural and mesodermal progeny in vitro, corresponding to the multipotency of neural crest stem cells. Likewise, neural stem/progenitor cells, which are self-renewing and multipotent, can display as neurospheres. Both of them form spheres in response to epidermal growth factor (EGF) and basic fibroblast growth factor (bFGF) in vitro. Although the“stemness”of neural stem/progenitor cells has been extensively investigated, direct comparison of“stemness”between SKP spheres and neurospheres is unknown. Here we dissect the“stemness”of SKP spheres and neurospheres by microarray analysis. Totally 142 genes are commonly enriched in SKP spheres and neurospheres, which are involved in ribosome, tight junction, gap junction, cell communication, calcium signaling, ErbB signaling, JAK-STAT signaling, MAPK signaling et al. Functional annotation clustering indicates that SKP spheres and neurospheres employ similar protein biosynthesis process but differential cell communication pathways. In addition, the differentially expressed genes between SKP spheres and neurospheres are most commonly involved in ECM-receptor interaction and TGF-βsignaling pathway. It is suggested that cell-communication pathways which integrate ECM-receptor interaction and TGF-βsignaling may contribute to the differential stem-cell identity of SKP spheres and neurospheres. Thus it is inferred that the ground state of stem cells could be maintained in a cell-intrinsic manner within local microenvironment mediated by cell-cell communication pathways.
3) Deciphering the mesodermal potency of porcine skin derived progenitors by microarray analysis
Skin stem cells have an essential role in maintaining tissue homeostasis by dynamically replenishing those constantly lost during tissue turnover or following injury. Multipotent skin derived progenitors (SKP) can generate both neural and mesodermal progeny, representing neural crest-derived progenitors during embryogenesis through adulthood. SKP cells develop into spheres in suspension and can differentiate into fibroblast-like cells (SFC) in adhesive culture with serum. However, little is known about the molecular mechanism of the transition of SKP spheres into SFC in vitro. Here we characterized the transcriptional profiles of porcine SKP spheres and SFC by microarray analysis. The 305 up-regulated and 96 down-regulated genes were found during transition, respectively. The down-regulated genes are mainly involved in intrinsic programs like the Dicer pathway and asymmetric cell division; whereas up-regulated genes are likely to participate in extrinsic signaling pathways such as ErbB signaling, MAPK signaling, ECM-receptor reaction, Wnt signaling, cell communication and TGF-βsignaling pathways. These intrinsic programs and extrinsic signaling pathways collaborate to mediate the transcription-state transition between SKP spheres and SFC. These potential signaling pathways may regulate self-renewal and cell fate determination of skin-derived stem cells in vivo, thus orchestrating the molecular programs of skin stem cells and morphogenesis in skin development.
引文
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