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Cancer-Initiating Enriched Cell Lines from Human Glioblastoma: Preparing for Drug Discovery Assays

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Abstract

Glioblastoma multiforme (GBM) is the most lethal type of brain tumour in the adult humans. The cancer-Initiatingcell (CIC) hypothesis supports the notion that failures in current approaches to GBM treatment might be attributed to the survival of the CIC subpopulation. Recent evidence shows the idea that using CIC-enriched cell lines derived from human GBM as new targets for drug discovery programs, may improve the chance of successfully translating the basic research findingsinto clinical trials. Although this approach appears promising, many important biological and technical issues (characterization of functional CIC markers, inter- and intra-tumoral CIC heterogeneity, and isolation and maintenance inconsistency) need to be resolved.

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References

  1. Louis, D. N., Ohgaki, H., Wiestler, O. D., et al. (2007). The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathologica (Berl), 114, 97–109.

    Article  Google Scholar 

  2. Palanichamy, K., & Chakravarti, A. (2009). Combining drugs and radiotherapy: from the bench to the bedside. Current Opinion in Neurology, 22, 625–632.

    Article  PubMed  CAS  Google Scholar 

  3. Hou, L. C., Veeravagu, A., Hsu, A. R., & Tse, V. C. (2006). Recurrent glioblastoma multiforme: a review of natural history and management options. Neurosurgical Focus, 20, E5.

    Article  PubMed  Google Scholar 

  4. Palanichamy, K., Erkkinen, M., Saia, G., & Chakravarti, A. (2007). Molecular and genetic profiling in human gliomas. Discovery Medicine, 7, 75–81.

    PubMed  Google Scholar 

  5. Nagarajan, R. P., & Costello, J. F. (2009). Epigenetic mechanisms in glioblastoma multiforme. Seminars in Cancer Biology, 19, 188–197.

    Article  PubMed  CAS  Google Scholar 

  6. Sathornsumetee, S., & Rich, J. N. (2008). Designer therapies for glioblastoma multiforme. Annals of the New York Academy of Sciences, 1142, 108–132.

    Article  PubMed  CAS  Google Scholar 

  7. Visvader, J. E., & Lindeman, G. J. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nature Reviews. Cancer, 8, 755–768.

    Article  PubMed  CAS  Google Scholar 

  8. Yuan, X., Curtin, J., Xiong, Y., et al. (2004). Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene, 23, 9392–9400.

    Article  PubMed  CAS  Google Scholar 

  9. Singh, S. K., Clarke, I. D., Terasaki, M., et al. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63, 5821–5828.

    PubMed  CAS  Google Scholar 

  10. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 3983–3988.

    Article  PubMed  CAS  Google Scholar 

  11. Dick, J. E., & Lapidot, T. (2005). Biology of normal and acute myeloid leukemia stem cells. International Journal of Hematology, 82, 389–396.

    Article  PubMed  CAS  Google Scholar 

  12. Galli, R., Binda, E., Orfanelli, U., et al. (2004). Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Research, 64, 7011–7021.

    Article  PubMed  CAS  Google Scholar 

  13. Singh, S. K., Hawkins, C., Clarke, I. D., et al. (2004). Identification of human brain tumour initiating cells. Nature, 432, 396–401.

    Article  PubMed  CAS  Google Scholar 

  14. Alvarez-Buylla, A., Seri, B., & Doetsch, F. (2002). Identification of neural stem cells in the adult vertebrate brain. Brain Research Bulletin, 57, 751–758.

    Article  PubMed  Google Scholar 

  15. Seri, B., Garcia-Verdugo, J. M., Collado-Morente, L., McEwen, B. S., & Alvarez-Buylla, A. (2004). Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. The Journal of Comparative Neurology, 478, 359–378.

    Article  PubMed  Google Scholar 

  16. Aimone, J. B., Deng, W., & Gage, F. H. (2010). Adult neurogenesis: integrating theories and separating functions. Trends in Cognitive Sciences, 14, 325–337.

    Article  PubMed  Google Scholar 

  17. Seaberg, R. M., & van der Kooy, D. (2002). Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. Journal of Neuroscience, 22, 1784–1793.

    PubMed  CAS  Google Scholar 

  18. Nunes, M. C., Roy, N. S., Keyoung, H. M., et al. (2003). Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nature Medicine, 9, 439–447.

    Article  PubMed  CAS  Google Scholar 

  19. Bao, S., Wu, Q., McLendon, R. E., et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 444, 756–760.

    Article  PubMed  CAS  Google Scholar 

  20. Liu, G., Yuan, X., Zeng, Z., et al. (2006). Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Molecular Cancer, 5, 67.

    Article  PubMed  Google Scholar 

  21. Beier, D., Rohrl, S., Pillai, D. R., et al. (2008). Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Research, 68, 5706–5715.

    Article  PubMed  CAS  Google Scholar 

  22. Sakariassen, P. O., Immervoll, H., & Chekenya, M. (2007). Cancer stem cells as mediators of treatment resistance in brain tumors: status and controversies. Neoplasia, 9, 882–892.

    Article  PubMed  CAS  Google Scholar 

  23. Vescovi, A. L., Galli, R., & Reynolds, B. A. (2006). Brain tumour stem cells. Nature Reviews. Cancer, 6, 425–436.

    Article  PubMed  CAS  Google Scholar 

  24. Diamandis, P., Sacher, A. G., Tyers, M., & Dirks, P. B. (2009). New drugs for brain tumors? Insights from chemical probing of neural stem cells. Medical Hypotheses, 72, 683–687.

    Article  PubMed  CAS  Google Scholar 

  25. Zhou, B. B., Zhang, H., Damelin, M., Geles, K. G., Grindley, J. C., & Dirks, P. B. (2009). Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nature Reviews. Drug Discovery, 8, 806–823.

    Article  PubMed  CAS  Google Scholar 

  26. Shapiro, J. R., & Shapiro, W. R. (1985). The subpopulations and isolated cell types of freshly resected high grade human gliomas: their influence on the tumor’s evolution in vivo and behavior and therapy in vitro. Cancer Metastasis Reviews, 4, 107–124.

    Article  PubMed  CAS  Google Scholar 

  27. Shapiro, J. R., Yung, W. K., & Shapiro, W. R. (1981). Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Research, 41, 2349–2359.

    PubMed  CAS  Google Scholar 

  28. Shapiro, J. R., & Shapiro, W. R. (1984). Clonal tumor cell heterogeneity. Progress in Experimental Tumor Research, 27, 49–66.

    PubMed  CAS  Google Scholar 

  29. Bao, S., Wu, Q., Li, Z., et al. (2008). Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Research, 68, 6043–6048.

    Article  PubMed  CAS  Google Scholar 

  30. Son, M. J., Woolard, K., Nam, D. H., Lee, J., & Fine, H. A. (2009). SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell, 4, 440–452.

    Article  PubMed  CAS  Google Scholar 

  31. Anido, J., Saez-Borderias, A., Gonzalez-Junca, A., et al. (2010). TGF-beta Receptor Inhibitors Target the CD44(high)/Id1(high) Glioma-Initiating Cell Population in Human Glioblastoma. Cancer Cell, 18, 655–668.

    Article  PubMed  CAS  Google Scholar 

  32. Mazzoleni, S., Politi, L. S., Pala, M., et al. (2010). Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Research, 70, 7500–7513.

    Article  PubMed  CAS  Google Scholar 

  33. Ogden, A. T., Waziri, A. E., Lochhead, R. A., et al. (2008). Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas. Neurosurgery, 62, 505–14. discussion 14–5.

    Article  PubMed  Google Scholar 

  34. Beier F, Beier CP, Aschenbrenner I, Hildebrandt GC, Brummendorf TH, Beier D.(2010). Identification of CD133(−)/Telomerase (low) Progenitor Cells in Glioblastoma-Derived Cancer Stem Cell Lines. Cell Mol Neurobiol.

  35. Ricci-Vitiani, L., Pallini, R., Biffoni, M., et al. (2010). Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature, 468, 824–828.

    Article  PubMed  CAS  Google Scholar 

  36. Wang, R., Chadalavada, K., Wilshire, J., et al. (2010). Glioblastoma stem-like cells give rise to tumour endothelium. Nature, 468, 829–833.

    Article  PubMed  CAS  Google Scholar 

  37. Klink, B., Schlingelhof, B., Klink, M., Stout-Weider, K., Patt, S., & Schrock, E. (2010). Glioblastomas with oligodendroglial component—common origin of the different histological parts and genetic subclassification. Analytical Cellular Pathology (Amsterdam), 33, 37–54.

    CAS  Google Scholar 

  38. Achanta, P., Sedora Roman, N. I., & Quinones-Hinojosa, A. (2010). Gliomagenesis and the use of neural stem cells in brain tumor treatment. Anti-Cancer Agents in Medicinal Chemistry, 10, 121–130.

    PubMed  CAS  Google Scholar 

  39. Verhaak, R. G., Hoadley, K. A., Purdom, E., et al. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell, 17, 98–110.

    Article  PubMed  CAS  Google Scholar 

  40. Noushmehr, H., Weisenberger, D. J., Diefes, K., et al. (2010). Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell, 17, 510–522.

    Article  PubMed  CAS  Google Scholar 

  41. Phillips, H. S., Kharbanda, S., Chen, R., et al. (2006). Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell, 9, 157–173.

    Article  PubMed  CAS  Google Scholar 

  42. Gunther, H. S., Schmidt, N. O., Phillips, H. S., et al. (2008). Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene, 27, 2897–2909.

    Article  PubMed  CAS  Google Scholar 

  43. Lottaz, C., Beier, D., Meyer, K., et al. (2010). Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Research, 70, 2030–2040.

    Article  PubMed  CAS  Google Scholar 

  44. Bidlingmaier, S., Zhu, X., & Liu, B. (2008). The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. Journal of Molecular Medicine, 86, 1025–1032.

    Article  PubMed  CAS  Google Scholar 

  45. Wright, M. H., Calcagno, A. M., Salcido, C. D., Carlson, M. D., Ambudkar, S. V., & Varticovski, L. (2008). Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Research, 10, R10.

    Article  PubMed  Google Scholar 

  46. Clement, V., Dutoit, V., Marino, D., Dietrich, P. Y., & Radovanovic, I. (2009). Limits of CD133 as a marker of glioma self-renewing cells. International Journal of Cancer, 125, 244–248.

    Article  CAS  Google Scholar 

  47. Beier, D., Hau, P., Proescholdt, M., et al. (2007). CD133(+) and CD133(−) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Research, 67, 4010–4015.

    Article  PubMed  CAS  Google Scholar 

  48. Wang, J., Sakariassen, P. O., Tsinkalovsky, O., et al. (2008). CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. International Journal of Cancer, 122, 761–768.

    Article  CAS  Google Scholar 

  49. Zheng, X., Shen, G., Yang, X., & Liu, W. (2007). Most C6 cells are cancer stem cells: evidence from clonal and population analyses. Cancer Research, 67, 3691–3697.

    Article  PubMed  CAS  Google Scholar 

  50. Radotra, B., & McCormick, D. (1997). Glioma invasion in vitro is mediated by CD44-hyaluronan interactions. The Journal of Pathology, 181, 434–438.

    Article  PubMed  CAS  Google Scholar 

  51. Merzak, A., Koocheckpour, S., & Pilkington, G. J. (1994). CD44 mediates human glioma cell adhesion and invasion in vitro. Cancer Research, 54, 3988–3992.

    PubMed  CAS  Google Scholar 

  52. Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C. B., & Seed, B. (1990). CD44 is the principal cell surface receptor for hyaluronate. Cell, 61, 1303–1313.

    Article  PubMed  CAS  Google Scholar 

  53. Penuelas, S., Anido, J., Prieto-Sanchez, R. M., et al. (2009). TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell, 15, 315–327.

    Article  PubMed  CAS  Google Scholar 

  54. Bignami, A., & Asher, R. (1992). Some observations on the localization of hyaluronic acid in adult, newborn and embryonal rat brain. International Journal of Developmental Neuroscience, 10, 45–57.

    Article  PubMed  CAS  Google Scholar 

  55. De Clerck, Y. A., Shimada, H., Gonzalez-Gomez, I., & Raffel, C. (1994). Tumoral invasion in the central nervous system. Journal of Neuro-Oncology, 18, 111–121.

    Article  PubMed  Google Scholar 

  56. Senner, V., Sturm, A., Baur, I., Schrell, U. H., Distel, L., & Paulus, W. (1999). CD24 promotes invasion of glioma cells in vivo. Journal of Neuropathology and Experimental Neurology, 58, 795–802.

    Article  PubMed  CAS  Google Scholar 

  57. Baumann, P., Cremers, N., Kroese, F., et al. (2005). CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Research, 65, 10783–10793.

    Article  PubMed  CAS  Google Scholar 

  58. Lim, S. C., & Oh, S. H. (2005). The role of CD24 in various human epithelial neoplasias. Pathology Research and Practice, 201, 479–486.

    Article  CAS  Google Scholar 

  59. Fukushima, T., Tezuka, T., Shimomura, T., Nakano, S., & Kataoka, H. (2007). Silencing of insulin-like growth factor-binding protein-2 in human glioblastoma cells reduces both invasiveness and expression of progression-associated gene CD24. Journal of Biological Chemistry, 282, 18634–18644.

    Article  PubMed  CAS  Google Scholar 

  60. Dennis, J. E., Esterly, K., Awadallah, A., Parrish, C. R., Poynter, G. M., & Goltry, K. L. (2007). Clinical-scale expansion of a mixed population of bone-marrow-derived stem and progenitor cells for potential use in bone-tissue regeneration. Stem Cells, 25, 2575–2582.

    Article  PubMed  Google Scholar 

  61. Rege, T. A., & Hagood, J. S. (2006). Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. The FASEB Journal, 20, 1045–1054.

    Article  CAS  Google Scholar 

  62. Rege, T. A., & Hagood, J. S. (2006). Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/growth factor responses. Biochimica et Biophysica Acta, 1763, 991–999.

    Article  PubMed  CAS  Google Scholar 

  63. Swart, G. W., Lunter, P. C., Kilsdonk, J. W., & Kempen, L. C. (2005). Activated leukocyte cell adhesion molecule (ALCAM/CD166): signaling at the divide of melanoma cell clustering and cell migration? Cancer Metastasis Reviews, 24, 223–236.

    Article  PubMed  CAS  Google Scholar 

  64. Surowiak, P., Materna, V., Klak, K., et al. (2005). Prognostic value of immunohistochemical estimation of CD24 and Ki67 expression in cisplatin and paclitaxel treated ovarian carcinoma patients. Polish Journal of Pathology, 56, 69–74.

    PubMed  Google Scholar 

  65. King, J. A., Ofori-Acquah, S. F., Stevens, T., Al-Mehdi, A. B., Fodstad, O., & Jiang, W. G. (2004). Activated leukocyte cell adhesion molecule in breast cancer: prognostic indicator. Breast Cancer Research, 6, R478–R487.

    Article  PubMed  CAS  Google Scholar 

  66. Weichert, W., Knosel, T., Bellach, J., Dietel, M., & Kristiansen, G. (2004). ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival. Journal of Clinical Pathology, 57, 1160–1164.

    Article  PubMed  CAS  Google Scholar 

  67. Verma, A., Shukla, N. K., Deo, S. V., Gupta, S. D., & Ralhan, R. (2005). MEMD/ALCAM: a potential marker f or tumor invasion and nodal metastasis in esophageal squamous cell carcinoma. Oncology, 68, 462–470.

    Article  PubMed  CAS  Google Scholar 

  68. Lee, J., Kotliarova, S., Kotliarov, Y., et al. (2006). Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell, 9, 391–403.

    Article  PubMed  CAS  Google Scholar 

  69. Pollard, S. M., Yoshikawa, K., Clarke, I. D., et al. (2009). Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell, 4, 568–580.

    Article  PubMed  CAS  Google Scholar 

  70. Sullivan, M., Galea, P., & Latif, S. (2006). What is the appropriate oxygen tension for in vitro culture? Molecular Human Reproduction, 12, 653.

    Article  PubMed  Google Scholar 

  71. Csete, M. (2005). Oxygen in the cultivation of stem cells. Annals of the New York Academy of Sciences, 1049, 1–8.

    Article  PubMed  CAS  Google Scholar 

  72. Studer, L., Csete, M., Lee, S. H., et al. (2000). Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. Journal of Neuroscience, 20, 7377–7383.

    PubMed  CAS  Google Scholar 

  73. Zhu, L. L., Wu, L. Y., Yew, D. T., & Fan, M. (2005). Effects of hypoxia on the proliferation and differentiation of NSCs. Molecular Neurobiology, 31, 231–242.

    Article  PubMed  CAS  Google Scholar 

  74. Platet, N., Liu, S. Y., Atifi, M. E., et al. (2007). Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Letters, 258, 286–290.

    Article  PubMed  CAS  Google Scholar 

  75. Soeda, A., Park, M., Lee, D., et al. (2009). Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene, 28, 3949–3959.

    Article  PubMed  CAS  Google Scholar 

  76. Kelly, J. J., Stechishin, O., Chojnacki, A., et al. (2009). Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells, 27, 1722–1733.

    Article  PubMed  CAS  Google Scholar 

  77. Pouyssegur, J., Dayan, F., & Mazure, N. M. (2006). Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature, 441, 437–443.

    Article  PubMed  CAS  Google Scholar 

  78. Reynolds, B. A., & Vescovi, A. L. (2009). Brain cancer stem cells: Think twice before going flat. Cell Stem Cell, 5, 466–7. author reply 8–9.

    Article  PubMed  CAS  Google Scholar 

  79. Scheffler, B., Walton, N. M., Lin, D. D., et al. (2005). Phenotypic and functional characterization of adult brain neuropoiesis. Proceedings of the National Academy of Sciences of the United States of America, 102, 9353–9358.

    Article  PubMed  CAS  Google Scholar 

  80. Chong, Y. K., Toh, T. B., Zaiden, N., et al. (2009). Cryopreservation of neurospheres derived from human glioblastoma multiforme. Stem Cells, 27, 29–39.

    Article  PubMed  CAS  Google Scholar 

  81. Stupp, R., van den Bent, M. J., & Hegi, M. E. (2005). Optimal role of temozolomide in the treatment of malignant gliomas. Current Neurology and Neuroscience Reports, 5, 198–206.

    Article  PubMed  CAS  Google Scholar 

  82. Lamszus, K., & Gunther, H. S. (2010). Glioma stem cells as a target for treatment. Targeted Oncology, 5, 211–215.

    Article  PubMed  Google Scholar 

  83. Zabierowski, S. E., & Herlyn, M. (2008). Melanoma stem cells: the dark seed of melanoma. Journal of Clinical Oncology, 26, 2890–2894.

    Article  PubMed  Google Scholar 

  84. Hermann, P. C., Huber, S. L., Herrler, T., et al. (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell, 1, 313–323.

    Article  PubMed  CAS  Google Scholar 

  85. Lapidot, T., Sirard, C., Vormoor, J., et al. (1994). A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 645–648.

    Article  PubMed  CAS  Google Scholar 

  86. Bhatia, M., Wang, J. C., Kapp, U., Bonnet, D., & Dick, J. E. (1997). Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 94, 5320–5325.

    Article  PubMed  CAS  Google Scholar 

  87. Tso, C. L., Shintaku, P., Chen, J., et al. (2006). Primary glioblastomas express mesenchymal stem-like properties. Molecular Cancer Research, 4, 607–619.

    Article  PubMed  CAS  Google Scholar 

  88. Zhang, S., Balch, C., Chan, M. W., et al. (2008). Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Research, 68, 4311–4320.

    Article  PubMed  CAS  Google Scholar 

  89. Takaishi, S., Okumura, T., Tu, S., et al. (2009). Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells, 27, 1006–1020.

    Article  PubMed  CAS  Google Scholar 

  90. Collins, A. T., Berry, P. A., Hyde, C., Stower, M. J., & Maitland, N. J. (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Research, 65, 10946–10951.

    Article  PubMed  CAS  Google Scholar 

  91. Yang, Z. F., Ho, D. W., Ng, M. N., et al. (2008). Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell, 13, 153–166.

    Article  PubMed  CAS  Google Scholar 

  92. Dalerba, P., Dylla, S. J., Park, I. K., et al. (2007). Phenotypic characterization of human colorectal cancer stem cells. Proceedings of the National Academy of Sciences of the United States of America, 104, 10158–10163.

    Article  PubMed  CAS  Google Scholar 

  93. Yang, Y. M., & Chang, J. W. (2008). Bladder cancer initiating cells (BCICs) are among EMA-CD44v6+ subset: novel methods for isolating undetermined cancer stem (initiating) cells. Cancer Investigation, 26, 725–733.

    Article  PubMed  CAS  Google Scholar 

  94. Kim, C. F., Jackson, E. L., Woolfenden, A. E., et al. (2005). Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell, 121, 823–835.

    Article  PubMed  CAS  Google Scholar 

  95. Kang, M. K., & Kang, S. K. (2007). Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem Cells and Development, 16, 837–847.

    Article  PubMed  CAS  Google Scholar 

  96. Tchoghandjian, A., Baeza, N., Colin, C., et al. (2009). A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathology, 20, 211–221.

    Article  PubMed  Google Scholar 

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Acknowledgment

We are especially grateful to Dr. Escobedo-Lucea for her technical advice. Miriam Romaguera-Ros is recipient of a Predoctoral Fellowship from The FIS program (FI05/0087), Ministerio de Sanidad, Spain. Jorge Oliver De La Cruz and Arantxa Pérez García are recipients of a Predoctoral Fellowship from The FPU program (AP2008/02823 and AP2009/1317), Ministerio de Educacion y Ciencia, Spain. This work was supported in part by grants from Generalitat Valenciana (GV/2009/68) (AAS), The Gent x Gent Foundation (AAS) and Fondo de Investigaciones Sanitarias (FIS) del instituto de Salud Carlos III (PI10/01069)(AAS).

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All authors have read and have approved of the manuscripts in their final form. Al authors declare that there is not conflict of interest with any material included in the manuscript.

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Correspondence to Jose Manuel García-Verdugo or Angel Ayuso-Sacido.

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Miriam Romaguera-Ros and María Peris-Celda have equal contribution.

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Romaguera-Ros, M., Peris-Celda, M., Oliver-De La Cruz, J. et al. Cancer-Initiating Enriched Cell Lines from Human Glioblastoma: Preparing for Drug Discovery Assays. Stem Cell Rev and Rep 8, 288–298 (2012). https://doi.org/10.1007/s12015-011-9283-1

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