基于超顺磁性纳米颗粒的肿瘤干细胞生物学特性研究
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摘要
肿瘤干细胞（Cancer stem cells, CSCs）被广泛认为是肿瘤形成的“种子”细胞，在肿瘤发生、维持、转移与复发过程中均发挥着关键性作用。针对肿瘤干细胞进行靶向治疗是未来肿瘤治疗最有效的策略之一，为肿瘤治疗指出了新方向。然而，肿瘤干细胞数量稀少，分离及纯化较难，成为肿瘤干细胞研究的关键性技术瓶颈问题。因此，建立一套有效分离并鉴定肿瘤干细胞的技术体系，对肿瘤研究和治疗具有十分重要的价值。鉴于此，本研究以人源性多形性胶质母细胞瘤U251细胞系为主要研究对象，成功建立一套有效富集、分离肿瘤干细胞的超顺磁性纳米颗粒分离体系；并进一步分析超顺磁性纳米颗粒对肿瘤干细胞生物学特性的影响，为超顺磁性纳米颗粒在肿瘤干细胞分离纯化、肿瘤诊断与靶向治疗等方面的应用提供理论基础。通过上述研究工作，我们取得了以下重要结论：
1.采用无血清悬浮培养联合细胞周期特异性药物长春新碱（vincristine, VCR）富集分离多形性胶质母细胞瘤U251细胞系中的肿瘤干细胞，结果表明该方法能够有效富集肿瘤干细胞。富集分离的肿瘤干细胞能够连续传代，具有良好的自我更新能力。MTT分析及FDA/PI荧光双染结果显示VCR诱导富集得到的肿瘤干细胞增殖能力旺盛、细胞活性好；RT-PCR以及免疫细胞化学染色结果显示肿瘤干细胞表面标志物CD133和神经巢蛋白（nestin）呈强阳性表达；胶质瘤球具有多向分化能力，能够分化为以胶质纤维酸性蛋白（GFAP）为标志物的星形细胞、髓鞘脂碱性蛋白（MBP）为标志物的少突胶质细胞以及微管相关蛋白（MAP2和tau）为标志物的神经元；RT-PCR分析表明富集分离的肿瘤干细胞高表达多药耐药蛋白1（MRP1）基因和凋亡抑制基因survivin。因此，此种方法富集分离的肿瘤干细胞可以用于开展后续试验。
2.研究超顺磁性纳米颗粒标记对肿瘤干细胞生物学特性的影响。研究了多聚赖氨酸（Poly-L-lysine, PLL）修饰的γ-Fe_2O_3纳米颗粒标记肿瘤干细胞对其细胞活性和增殖能力、自我更新能力、多向分化潜能、细胞周期分布与细胞凋亡等生物学性能的潜在影响。我们首先利用部分还原共沉淀法制备出超顺磁性γ-Fe_2O_3纳米颗粒，并将阳离子转染剂PLL修饰于γ-Fe_2O_3纳米颗粒表面以加强细胞对纳米颗粒的吸收；然后利用PLL修饰γ-Fe_2O_3纳米颗粒标记来源于胶质瘤细胞系U251的肿瘤干细胞。普鲁士蓝染色及原子吸收分光光度计分析结果表明PLL修饰γ-Fe_2O_3纳米颗粒成功标记肿瘤干细胞；FDA/PI荧光双染及MTT分析结果表明磁标记不影响肿瘤干细胞及其分化细胞的活性和增殖能力；免疫细胞化学染色及半定量RT-PCR分析结果表明磁标记不影响肿瘤干细胞标志物表达及其多向分化潜能；并且磁标记后形成的胶质瘤球能传代形成新的胶质瘤球，表明磁标记肿瘤干细胞具有自我更新能力。此外，流式细胞仪分析结果表明与未标记对照相比磁标记对肿瘤干细胞及其分化细胞的细胞周期分布（S期细胞为15.93%vs15.44%&11.35%vs11.31%）基本没有影响；流式细胞仪分析磁标记细胞及其分化细胞的早期凋亡率分别为4.4%和1.4%，与对照相比（4.9%和1.1%）基本没有影响。以上这些研究结果为超顺磁性纳米颗粒在肿瘤干细胞分离、细胞基的治疗以及利用磁共振成像技术非侵袭性的捕获肿瘤干细胞体内行为等方面的应用提供了理论基础。
3.利用超顺磁性Fe_3O_4纳米颗粒的类酶活性特征调控肿瘤干细胞的增殖。通过Fe_3O_4纳米颗粒的类辣根过氧化物酶（HRP）活性可以调控肿瘤干细胞自身活性氧（ROS）的产生水平，从而能够调控肿瘤干细胞的增殖。研究结果表明，PLL修饰不影响Fe_3O_4纳米颗粒的类过氧化物酶活性。PLL-Fe3O4纳米颗粒复合物通过降低肿瘤干细胞内源性ROS水平，从而促进了其增殖及细胞周期进程；PLL-Fe_3O_4纳米颗粒复合物处理的肿瘤干细胞过氧化氢酶活性显著升高。此外，PLL-Fe3O4纳米颗粒复合物不影响肿瘤干细胞标志物表达、多向分化能力以及actin细胞骨架结构与形态。与前人研究不同，本研究报道的是Fe_3O_4纳米颗粒对细胞生长的有利影响，从而为Fe3O4纳米颗粒在生物医药领域潜在的广泛应用提供有力证据。
4.利用改进的高温乳化法制备出超顺磁性HSA/γ-Fe_2O_3微珠，然后以蛋白微珠HSA/γ-Fe_2O_3为载体材料，通过亲和素-生物素的桥联作用将蛋白微珠与特异性捕获抗体（抗-CD133单克隆抗体）偶联制得免疫磁珠（immunomagnetic beads, IMBs），利用制得的IMBs进一步分离纯化肿瘤干细胞。结果表明我们成功制备了活性较高的IMBs，并且利用制得的IMBs成功实现了靶细胞即CD133~+细胞的分离纯化。该分离体系在40min内就能实现CD133+细胞的分离。所分选的CD133~+细胞具有良好的细胞活性、能够增殖形成胶质瘤球，免疫染色结果表明增殖形成的肿瘤球高表达肿瘤干细胞标志物CD133和nestin，且增殖形成的胶质瘤球具有多向分化能力。
综上所述，我们成功建立了一种无血清悬浮培养联合细胞周期特异性药物VCR有效富集分离肿瘤干细胞的方法；并深入研究了超顺磁性纳米颗粒标记对肿瘤干细胞生物学特性的影响，进而为磁性纳米颗粒在肿瘤干细胞研究领域中的应用奠定了理论基础。此外，我们深入分析了Fe_3O_4纳米颗粒的过氧化物酶类酶活性对肿瘤干细胞增殖的调控作用；并建立了一种基于超顺磁性蛋白微珠的肿瘤干细胞高效分离与纯化技术体系，该体系不仅可以用于U251细胞系中肿瘤干细胞的分离与纯化，还可以用于其它肿瘤组织或细胞系中靶细胞的分离与纯化。
Cancer stem cells (CSCs) are widely thought as the "seeds" of tumor formation, and playa crucial role in the process of tumor initiation, retention, transfer and recurrence, and areamong central points for cancer research and targeted therapy. However, the scarcity of CSCsand their difficulty for isolation and purification have become the key technical bottleneckproblem in the research of cancer stem cells. Thus to establish an effective system foridentification and isolation of CSCs is definitely of great importance in cancer research andtherapy. Therefore, in the present study, human glioblastoma multiforme U251cell line wasused to establish an efficient magnetic nanoparticles-based separation system for enrichmentand isolation of CSCs. The biological properties of CSCs potentially affected by magneticnanoparticles were further analyzed to provide a theoretical basis for potential utilization ofmagnetic nanoparticles in the isolation and purification of CSCs and cancer diagnosis andtherapy in future. According to our present results (data), the conclusions were made asfollows.
1. The serum-free suspension culture in combination with the cell cycle specific drugvincristine (VCR) was applied to enrich and separate CSCs derived from human glioblastomamultiforme U251cell line. The results showed that this method could effectively enrichcancer stem cells, and the enriched CSCs exhibited a good capability of continuous culturingand self-renewal. The MTT method and the FDA/PI fluorescent double staining proved thatthe enriched CSCs induced by VCR had an excellent proliferation potential and cellularviability. The RT-PCR analysis and immunocytochemistry staining results showed that thespecific markers CD133and nestin were positively expressed in CSCs, and the glioblastomaspheres had a potential of multi-differentiation, and could differentiate into astrocytes markedwith glial fiber acid protein (GFAP), oligodendrocytes with myelin basic protein (MBP), andneurons with microtubules related proteins (MAP2and tau). The RT-PCR analysis resultsshowed multi-drug resistance-associated protein1(MRP1) and anti-apoptotic protein survivingene strongly expressed in CSCs. Therefore, the VCR induced enrichment and separation ofCSCs could be used to carry out the follow-up experimental work.
2. The effects of magnetic nanoparticles on biological properties of cancer stem cells (CSCs) were analysed by revealing the performance of tumor stem cells after treatment withpoly-L-lysine (PLL) modified γ-Fe_2O_3nanoparticles including proliferation, cellular viability,self-renewal, multi-differentiation potential, cell cycle distribution and apoptosis, and so on.The partial reduction co-precipitation method was used to prepare superparamagnetic γ-Fe_2O_3nanoparticles, and the positively charged PLL was applied to modify γ-Fe_2O_3nanoparticles to improve surface absorption of target cells, and the PLL-modified γ-Fe_2O_3nanoparticles were used to surface label cancer stem cells derived from human U251cell line.The Prussian blue staining and atomic absorption spectrometry analysis showed that the PLLmodified γ-Fe_2O_3nanoparticles successfully labeled CSCs. The FDA/PI fluorescent doublestaining and MTT analysis showed that the magnetic labeling did not affect cellular viabilityand proliferation capacity of CSCs and their differentiated progeny. The immunocyto-chemistry staining and semi-quantitative RT-PCR analysis showed that the magnetic labelingdid not affect specific marker expression of cancer stem cells and their multi-differentiationpotential. Besides, the magnetically labeled glioblastoma spheres could reproduce andpropagate indicating that the magnetically labeled CSCs had an intact capability forself-renewal. In addition, flow cytometric analysis showed that the magnetic labeling andunlabeling in CSCs and differentiated progeny did not affect cell cycle distribution (cells in Sphase accounting for15.93%vs15.44%and11.35%vs11.31%), and the early apoptosisrates of magnetically labeled CSCs and their differentiated progeny were4.4%and1.4%, incontrast with the unlabeled counterparts (4.9%and1.1%). Taken together, these findingsprovided solid foundations for utilization of magnetic nanoparticles in the isolation of CSCs,cancer treatment and therapy, and noninvasive capture of CSCs by magnetic resonanceimaging in vivo etc.
3. The identified peroxidase-like activity of superparamagnetic Fe_3O_4nanoparticlespotentially regulating the proliferation of cancer stem cells was analyzed by examining thelevels of reactive oxygen species (ROS). The results showed that the PLL modification ofFe_3O_4nanoparticles did not affect the peroxidase-like activity, and the PLL modified Fe_3O_4nanoparticles could lower endogenous ROS levels produced within cancer stem cells and thusto promote proliferation and accelerate cell cycles of cancer stem cells. The peroxidaseactivity of cancer stem cells treated with the PLL modified Fe_3O_4nanoparticles wassignificantly increased. In addition, the PLL modified Fe_3O_4nanoparticles did not affect thespecific marker expression of cancer stem cells, multi-differentiation potential and actinstructure within cells. Different from the previous reports, our results definitely indicated thatFe_3O_4nanoparticles could beneficially enhance cell growth, which provides powerfulevidence for possible use of Fe_3O_4nanoparticles in biological medicine field in future.
4. The high temperature-aided emulsification method was applied to prepare superpara-magnetic HSA/γ-Fe_2O_3microbeads as a carrier, and then further used specifically to captureantibody (anti-CD133monoclonal antibody) by specific affinity interaction between avidinand biotin to form as immunomagnetic beads (IMBs), which was further used to purify cancerstem cells. The results showed that the active IMBs were successfully prepared and could beeffectively used for isolation and purification of target CD133~+cells, and the successfulseparation of CD133~+cells could be achieved within40min. Besides, the sorted CD133~+cellsdisplayed an intact cellular viability, and could proliferate as glioblastoma spheres. Theimmunocytostainings showed that the formed tumor spheres had a multi-differentiationpotential and could highly express their specific markers nestin and CD133.
In conclusion, in the present study we have developed an effective method using aserum-free suspension culture combined with the cell cycle specific drug VCR to efficientlyenrich and isolation of cancer stem cells, and the effects of magnetic labeling bysuperparamagnetic nanoparticles on biological properties of cancer stem cells were fullyanalyzed, which definitely provided solid foundations for future utilization of magneticnanoparticles in the research of cancer stem cells. Furthermore, the peroxidase-like activity ofmagnetic Fe_3O_4nanoparticles was analyzed in regulating proliferation of cancer stem cells,and a cost-effective immunomagnetic beads-based system for isolation and purification ofcancer stem cells was successfully developed, which could be also potentially applied forisolation and purification of target cells derived from other tumor cell lines, except for humanU251cell line used here.
1.采用无血清悬浮培养联合细胞周期特异性药物长春新碱（vincristine, VCR）富集分离多形性胶质母细胞瘤U251细胞系中的肿瘤干细胞，结果表明该方法能够有效富集肿瘤干细胞。富集分离的肿瘤干细胞能够连续传代，具有良好的自我更新能力。MTT分析及FDA/PI荧光双染结果显示VCR诱导富集得到的肿瘤干细胞增殖能力旺盛、细胞活性好；RT-PCR以及免疫细胞化学染色结果显示肿瘤干细胞表面标志物CD133和神经巢蛋白（nestin）呈强阳性表达；胶质瘤球具有多向分化能力，能够分化为以胶质纤维酸性蛋白（GFAP）为标志物的星形细胞、髓鞘脂碱性蛋白（MBP）为标志物的少突胶质细胞以及微管相关蛋白（MAP2和tau）为标志物的神经元；RT-PCR分析表明富集分离的肿瘤干细胞高表达多药耐药蛋白1（MRP1）基因和凋亡抑制基因survivin。因此，此种方法富集分离的肿瘤干细胞可以用于开展后续试验。
2.研究超顺磁性纳米颗粒标记对肿瘤干细胞生物学特性的影响。研究了多聚赖氨酸（Poly-L-lysine, PLL）修饰的γ-Fe_2O_3纳米颗粒标记肿瘤干细胞对其细胞活性和增殖能力、自我更新能力、多向分化潜能、细胞周期分布与细胞凋亡等生物学性能的潜在影响。我们首先利用部分还原共沉淀法制备出超顺磁性γ-Fe_2O_3纳米颗粒，并将阳离子转染剂PLL修饰于γ-Fe_2O_3纳米颗粒表面以加强细胞对纳米颗粒的吸收；然后利用PLL修饰γ-Fe_2O_3纳米颗粒标记来源于胶质瘤细胞系U251的肿瘤干细胞。普鲁士蓝染色及原子吸收分光光度计分析结果表明PLL修饰γ-Fe_2O_3纳米颗粒成功标记肿瘤干细胞；FDA/PI荧光双染及MTT分析结果表明磁标记不影响肿瘤干细胞及其分化细胞的活性和增殖能力；免疫细胞化学染色及半定量RT-PCR分析结果表明磁标记不影响肿瘤干细胞标志物表达及其多向分化潜能；并且磁标记后形成的胶质瘤球能传代形成新的胶质瘤球，表明磁标记肿瘤干细胞具有自我更新能力。此外，流式细胞仪分析结果表明与未标记对照相比磁标记对肿瘤干细胞及其分化细胞的细胞周期分布（S期细胞为15.93%vs15.44%&11.35%vs11.31%）基本没有影响；流式细胞仪分析磁标记细胞及其分化细胞的早期凋亡率分别为4.4%和1.4%，与对照相比（4.9%和1.1%）基本没有影响。以上这些研究结果为超顺磁性纳米颗粒在肿瘤干细胞分离、细胞基的治疗以及利用磁共振成像技术非侵袭性的捕获肿瘤干细胞体内行为等方面的应用提供了理论基础。
3.利用超顺磁性Fe_3O_4纳米颗粒的类酶活性特征调控肿瘤干细胞的增殖。通过Fe_3O_4纳米颗粒的类辣根过氧化物酶（HRP）活性可以调控肿瘤干细胞自身活性氧（ROS）的产生水平，从而能够调控肿瘤干细胞的增殖。研究结果表明，PLL修饰不影响Fe_3O_4纳米颗粒的类过氧化物酶活性。PLL-Fe3O4纳米颗粒复合物通过降低肿瘤干细胞内源性ROS水平，从而促进了其增殖及细胞周期进程；PLL-Fe_3O_4纳米颗粒复合物处理的肿瘤干细胞过氧化氢酶活性显著升高。此外，PLL-Fe3O4纳米颗粒复合物不影响肿瘤干细胞标志物表达、多向分化能力以及actin细胞骨架结构与形态。与前人研究不同，本研究报道的是Fe_3O_4纳米颗粒对细胞生长的有利影响，从而为Fe3O4纳米颗粒在生物医药领域潜在的广泛应用提供有力证据。
4.利用改进的高温乳化法制备出超顺磁性HSA/γ-Fe_2O_3微珠，然后以蛋白微珠HSA/γ-Fe_2O_3为载体材料，通过亲和素-生物素的桥联作用将蛋白微珠与特异性捕获抗体（抗-CD133单克隆抗体）偶联制得免疫磁珠（immunomagnetic beads, IMBs），利用制得的IMBs进一步分离纯化肿瘤干细胞。结果表明我们成功制备了活性较高的IMBs，并且利用制得的IMBs成功实现了靶细胞即CD133~+细胞的分离纯化。该分离体系在40min内就能实现CD133+细胞的分离。所分选的CD133~+细胞具有良好的细胞活性、能够增殖形成胶质瘤球，免疫染色结果表明增殖形成的肿瘤球高表达肿瘤干细胞标志物CD133和nestin，且增殖形成的胶质瘤球具有多向分化能力。
综上所述，我们成功建立了一种无血清悬浮培养联合细胞周期特异性药物VCR有效富集分离肿瘤干细胞的方法；并深入研究了超顺磁性纳米颗粒标记对肿瘤干细胞生物学特性的影响，进而为磁性纳米颗粒在肿瘤干细胞研究领域中的应用奠定了理论基础。此外，我们深入分析了Fe_3O_4纳米颗粒的过氧化物酶类酶活性对肿瘤干细胞增殖的调控作用；并建立了一种基于超顺磁性蛋白微珠的肿瘤干细胞高效分离与纯化技术体系，该体系不仅可以用于U251细胞系中肿瘤干细胞的分离与纯化，还可以用于其它肿瘤组织或细胞系中靶细胞的分离与纯化。
Cancer stem cells (CSCs) are widely thought as the "seeds" of tumor formation, and playa crucial role in the process of tumor initiation, retention, transfer and recurrence, and areamong central points for cancer research and targeted therapy. However, the scarcity of CSCsand their difficulty for isolation and purification have become the key technical bottleneckproblem in the research of cancer stem cells. Thus to establish an effective system foridentification and isolation of CSCs is definitely of great importance in cancer research andtherapy. Therefore, in the present study, human glioblastoma multiforme U251cell line wasused to establish an efficient magnetic nanoparticles-based separation system for enrichmentand isolation of CSCs. The biological properties of CSCs potentially affected by magneticnanoparticles were further analyzed to provide a theoretical basis for potential utilization ofmagnetic nanoparticles in the isolation and purification of CSCs and cancer diagnosis andtherapy in future. According to our present results (data), the conclusions were made asfollows.
1. The serum-free suspension culture in combination with the cell cycle specific drugvincristine (VCR) was applied to enrich and separate CSCs derived from human glioblastomamultiforme U251cell line. The results showed that this method could effectively enrichcancer stem cells, and the enriched CSCs exhibited a good capability of continuous culturingand self-renewal. The MTT method and the FDA/PI fluorescent double staining proved thatthe enriched CSCs induced by VCR had an excellent proliferation potential and cellularviability. The RT-PCR analysis and immunocytochemistry staining results showed that thespecific markers CD133and nestin were positively expressed in CSCs, and the glioblastomaspheres had a potential of multi-differentiation, and could differentiate into astrocytes markedwith glial fiber acid protein (GFAP), oligodendrocytes with myelin basic protein (MBP), andneurons with microtubules related proteins (MAP2and tau). The RT-PCR analysis resultsshowed multi-drug resistance-associated protein1(MRP1) and anti-apoptotic protein survivingene strongly expressed in CSCs. Therefore, the VCR induced enrichment and separation ofCSCs could be used to carry out the follow-up experimental work.
2. The effects of magnetic nanoparticles on biological properties of cancer stem cells (CSCs) were analysed by revealing the performance of tumor stem cells after treatment withpoly-L-lysine (PLL) modified γ-Fe_2O_3nanoparticles including proliferation, cellular viability,self-renewal, multi-differentiation potential, cell cycle distribution and apoptosis, and so on.The partial reduction co-precipitation method was used to prepare superparamagnetic γ-Fe_2O_3nanoparticles, and the positively charged PLL was applied to modify γ-Fe_2O_3nanoparticles to improve surface absorption of target cells, and the PLL-modified γ-Fe_2O_3nanoparticles were used to surface label cancer stem cells derived from human U251cell line.The Prussian blue staining and atomic absorption spectrometry analysis showed that the PLLmodified γ-Fe_2O_3nanoparticles successfully labeled CSCs. The FDA/PI fluorescent doublestaining and MTT analysis showed that the magnetic labeling did not affect cellular viabilityand proliferation capacity of CSCs and their differentiated progeny. The immunocyto-chemistry staining and semi-quantitative RT-PCR analysis showed that the magnetic labelingdid not affect specific marker expression of cancer stem cells and their multi-differentiationpotential. Besides, the magnetically labeled glioblastoma spheres could reproduce andpropagate indicating that the magnetically labeled CSCs had an intact capability forself-renewal. In addition, flow cytometric analysis showed that the magnetic labeling andunlabeling in CSCs and differentiated progeny did not affect cell cycle distribution (cells in Sphase accounting for15.93%vs15.44%and11.35%vs11.31%), and the early apoptosisrates of magnetically labeled CSCs and their differentiated progeny were4.4%and1.4%, incontrast with the unlabeled counterparts (4.9%and1.1%). Taken together, these findingsprovided solid foundations for utilization of magnetic nanoparticles in the isolation of CSCs,cancer treatment and therapy, and noninvasive capture of CSCs by magnetic resonanceimaging in vivo etc.
3. The identified peroxidase-like activity of superparamagnetic Fe_3O_4nanoparticlespotentially regulating the proliferation of cancer stem cells was analyzed by examining thelevels of reactive oxygen species (ROS). The results showed that the PLL modification ofFe_3O_4nanoparticles did not affect the peroxidase-like activity, and the PLL modified Fe_3O_4nanoparticles could lower endogenous ROS levels produced within cancer stem cells and thusto promote proliferation and accelerate cell cycles of cancer stem cells. The peroxidaseactivity of cancer stem cells treated with the PLL modified Fe_3O_4nanoparticles wassignificantly increased. In addition, the PLL modified Fe_3O_4nanoparticles did not affect thespecific marker expression of cancer stem cells, multi-differentiation potential and actinstructure within cells. Different from the previous reports, our results definitely indicated thatFe_3O_4nanoparticles could beneficially enhance cell growth, which provides powerfulevidence for possible use of Fe_3O_4nanoparticles in biological medicine field in future.
4. The high temperature-aided emulsification method was applied to prepare superpara-magnetic HSA/γ-Fe_2O_3microbeads as a carrier, and then further used specifically to captureantibody (anti-CD133monoclonal antibody) by specific affinity interaction between avidinand biotin to form as immunomagnetic beads (IMBs), which was further used to purify cancerstem cells. The results showed that the active IMBs were successfully prepared and could beeffectively used for isolation and purification of target CD133~+cells, and the successfulseparation of CD133~+cells could be achieved within40min. Besides, the sorted CD133~+cellsdisplayed an intact cellular viability, and could proliferate as glioblastoma spheres. Theimmunocytostainings showed that the formed tumor spheres had a multi-differentiationpotential and could highly express their specific markers nestin and CD133.
In conclusion, in the present study we have developed an effective method using aserum-free suspension culture combined with the cell cycle specific drug VCR to efficientlyenrich and isolation of cancer stem cells, and the effects of magnetic labeling bysuperparamagnetic nanoparticles on biological properties of cancer stem cells were fullyanalyzed, which definitely provided solid foundations for future utilization of magneticnanoparticles in the research of cancer stem cells. Furthermore, the peroxidase-like activity ofmagnetic Fe_3O_4nanoparticles was analyzed in regulating proliferation of cancer stem cells,and a cost-effective immunomagnetic beads-based system for isolation and purification ofcancer stem cells was successfully developed, which could be also potentially applied forisolation and purification of target cells derived from other tumor cell lines, except for humanU251cell line used here.
引文
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