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Cancers  2011 

Brain Cancer Stem Cells: Current Status on Glioblastoma Multiforme

DOI: 10.3390/cancers3021777

Keywords: polycomb, BMI1, cancer stem cell, glioma, glioblastoma multiforme, astrocyte, astrocytoma, radioresistance, CD133, prominin

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Abstract:

Glioblastoma multiforme (GBM), an aggressive brain tumor of astrocytic/neural stem cell origin, represents one of the most incurable cancers. GBM tumors are highly heterogeneous. However, most tumors contain a subpopulation of cells that display neural stem cell characteristics in vitro and that can generate a new brain tumor upon transplantation in mice. Hence, previously identified molecular pathways regulating neural stem cell biology were found to represent the cornerstone of GBM stem cell self-renewal mechanism. GBM tumors are also notorious for their resistance to radiation therapy. Notably, GBM “cancer stem cells” were also found to be responsible for this radioresistance. Herein, we will analyze the data supporting or not the cancer stem cell model in GBM, overview the current knowledge regarding GBM stem cell self-renewal and radioresistance molecular mechanisms, and discuss the potential therapeutic application of these findings.

References

[1]  Louis, D.N.; Ohgaki, H.; Wiestler, O.D.; Cavenee, W.K.; Burger, P.C.; Jouvet, A.; Scheithauer, B.W.; Kleihues, P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114, 97–109.
[2]  Stupp, R.; Mason, W.P.; van den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U.; Curschmann, J.; Janzer, R.C.; Ludwin, S.K.; Gorlia, T.; Allgeier, A.; Lacombe, D.; Cairncross, J.G.; Eisenhauer, E.; Mirimanoff, R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987–996.
[3]  Pan, E.; Mitchell, S.B.; Tsai, J.S. A retrospective study of the safety of BCNU wafers with concurrent temozolomide and radiotherapy and adjuvant temozolomide for newly diagnosed glioblastoma patients. J. Neurooncol. 2008, 88, 353–357.
[4]  Temple, S. The development of neural stem cells. Nature 2001, 414, 112–117.
[5]  Kriegstein, A.; Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32, 149–184.
[6]  Conti, L.; Cattaneo, E. Neural stem cell systems: physiological players or in vitro entities? Nat. Rev. Neurosci. 2010, 11, 176–187.
[7]  Haubensak, W.; Attardo, A.; Denk, W.; Huttner, W.B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 2004, 101, 3196–3201.
[8]  Miyata, T.; Kawaguchi, A.; Saito, K.; Kawano, M.; Muto, T.; Ogawa, M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004, 131, 3133–3145.
[9]  Englund, C.; Fink, A.; Lau, C.; Pham, D.; Daza, R.A.; Bulfone, A.; Kowalczyk, T.; Hevner, R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 2005, 25, 247–251.
[10]  Sessa, A.; Mao, C.A.; Hadjantonakis, A.K.; Klein, W.H.; Broccoli, V. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 2008, 60, 56–69.
[11]  Gage, F.H. Neurogenesis in the adult brain. J. Neurosci. 2002, 22, 612–613.
[12]  Alvarez-Buylla, A.; Lim, D.A. For the long run: maintaining germinal niches in the adult brain. Neuron 2004, 41, 683–686.
[13]  Mirzadeh, Z.; Merkle, F.T.; Soriano-Navarro, M.; Garcia-Verdugo, J.M.; Alvarez-Buylla, A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008, 3, 265–278.
[14]  Shen, Q.; Wang, Y.; Kokovay, E.; Lin, G.; Chuang, S.M.; Goderie, S.K.; Roysam, B.; Temple, S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3, 289–300.
[15]  Doetsch, F.; Caille, I.; Lim, D.A.; Garcia-Verdugo, J.M.; Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97, 703–716.
[16]  Belluzzi, O.; Benedusi, M.; Ackman, J.; LoTurco, J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 2003, 23, 10411–10418.
[17]  Carleton, A.; Petreanu, L.T.; Lansford, R.; Alvarez-Buylla, A.; Lledo, P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 2003, 6, 507–518.
[18]  Lois, C.; Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264, 1145–1148.
[19]  Coskun, V.; Wu, H.; Blanchi, B.; Tsao, S.; Kim, K.; Zhao, J.; Biancotti, J.C.; Hutnick, L.; Krueger, R.C., Jr.; Fan, G.; de Vellis, J.; Sun, Y.E. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc. Natl. Acad. Sci. USA 2008, 105, 1026–1031.
[20]  Cameron, H.A.; Woolley, C.S.; McEwen, B.S.; Gould, E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56, 337–344.
[21]  Palmer, T.D.; Willhoite, A.R.; Gage, F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425, 479–494.
[22]  Holland, E.C. Gliomagenesis: genetic alterations and mouse models. Nat. Rev. Genet. 2001, 2, 120–129.
[23]  Holland, E.C.; Celestino, J.; Dai, C.; Schaefer, L.; Sawaya, R.E.; Fuller, G.N. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet. 2000, 25, 55–57.
[24]  Uhrbom, L.; Dai, C.; Celestino, J.C.; Rosenblum, M.K.; Fuller, G.N.; Holland, E.C. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res. 2002, 62, 5551–5558.
[25]  Marumoto, T.; Tashiro, A.; Friedmann-Morvinski, D.; Scadeng, M.; Soda, Y.; Gage, F.H.; Verma, I.M. Development of a novel mouse glioma model using lentiviral vectors. Nat. Med. 2009, 15, 110–116.
[26]  Serrano, M.; Lee, H.; Chin, L.; Cordon-Cardo, C.; Beach, D.; DePinho, R.A. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996, 85, 27–37.
[27]  Holland, E.C.; Hively, W.P.; Gallo, V.; Varmus, H.E. Modeling mutations in the G1 arrest pathway in human gliomas: overexpression of CDK4 but not loss of INK4a-ARF induces hyperploidy in cultured mouse astrocytes. Genes Dev. 1998, 12, 3644–3649.
[28]  Kamijo, T.; Bodner, S.; van de Kamp, E.; Randle, D.H.; Sherr, C.J. Tumor spectrum in ARF-deficient mice. Cancer Res. 1999, 59, 2217–2222.
[29]  Donehower, L.A.; Harvey, M.; Slagle, B.L.; McArthur, M.J.; Montgomery, C.A., Jr.; Butel, J.S.; Bradley, A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356, 215–221.
[30]  Yahanda, A.M.; Bruner, J.M.; Donehower, L.A.; Morrison, R.S. Astrocytes derived from p53-deficient mice provide a multistep in vitro model for development of malignant gliomas. Mol. Cell. Biol. 1995, 15, 4249–4259.
[31]  Wang, Y.; Yang, J.; Zheng, H.; Tomasek, G.J.; Zhang, P.; McKeever, P.E.; Lee, E.Y.; Zhu, Y. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell 2009, 15, 514–526.
[32]  Gil-Perotin, S.; Marin-Husstege, M.; Li, J.; Soriano-Navarro, M.; Zindy, F.; Roussel, M.F.; Garcia-Verdugo, J.M.; Casaccia-Bonnefil, P. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J. Neurosci. 2006, 26, 1107–1116.
[33]  Meletis, K.; Wirta, V.; Hede, S.M.; Nister, M.; Lundeberg, J.; Frisen, J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 133, 363–369.
[34]  Jackson, E.L.; Garcia-Verdugo, J.M.; Gil-Perotin, S.; Roy, M.; Quinones-Hinojosa, A.; VandenBerg, S.; Alvarez-Buylla, A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51, 187–199.
[35]  Assanah, M.; Lochhead, R.; Ogden, A.; Bruce, J.; Goldman, J.; Canoll, P. Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J. Neurosci. 2006, 26, 6781–6790.
[36]  Recht, L.; Jang, T.; Savarese, T.; Litofsky, N.S. Neural stem cells and neuro-oncology: quo vadis? J. Cell. Biochem. 2003, 88, 11–19.
[37]  Zook, B.C.; Simmens, S.J.; Jones, R.V. Evaluation of ENU-induced gliomas in rats: nomenclature, immunochemistry, and malignancy. Toxicol. Pathol. 2000, 28, 193–201.
[38]  Alcantara Llaguno, S.; Chen, J.; Kwon, C.H.; Jackson, E.L.; Li, Y.; Burns, D.K.; Alvarez-Buylla, A.; Parada, L.F. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009, 15, 45–56.
[39]  Jacques, T.S.; Swales, A.; Brzozowski, M.J.; Henriquez, N.V.; Linehan, J.M.; Mirzadeh, Z.; C, O.M.; Naumann, H.; Alvarez-Buylla, A.; Brandner, S. Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J. 2010, 29, 222–235.
[40]  Liu, H.K.; Wang, Y.; Belz, T.; Bock, D.; Takacs, A.; Radlwimmer, B.; Barbus, S.; Reifenberger, G.; Lichter, P.; Schutz, G. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev. 2010, 24, 683–695.
[41]  Moon, J.H.; Yoon, B.S.; Kim, B.; Park, G.; Jung, H.Y.; Maeng, I.; Jun, E.K.; Yoo, S.J.; Kim, A.; Oh, S.; Whang, K.Y.; Kim, H.; Kim, D.W.; Kim, K.D.; You, S. Induction of neural stem cell-like cells (NSCLCs) from mouse astrocytes by Bmi1. Biochem. Biophys. Res. Commun. 2008, 371, 267–272.
[42]  Reya, T.; Morrison, S.J.; Clarke, M.F.; Weissman, I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414, 105–111.
[43]  Lobo, N.A.; Shimono, Y.; Qian, D.; Clarke, M.F. The biology of cancer stem cells. Annu. Rev. Cell. Dev. Biol. 2007, 23, 675–699.
[44]  Clarke, M.F.; Fuller, M. Stem cells and cancer: two faces of eve. Cell 2006, 124, 1111–1115.
[45]  Lapidot, T.; Sirard, C.; Vormoor, J.; Murdoch, B.; Hoang, T.; Caceres-Cortes, J.; Minden, M.; Paterson, B.; Caligiuri, M.A.; Dick, J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367, 645–648.
[46]  Bonnet, D.; Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3, 730–737.
[47]  Dick, J.E. Breast cancer stem cells revealed. Proc. Natl. Acad. Sci. USA 2003, 100, 3547–3549.
[48]  Al-Hajj, M.; Becker, M.W.; Wicha, M.; Weissman, I.; Clarke, M.F. Therapeutic implications of cancer stem cells. Curr. Opin. Genet. Dev. 2004, 14, 43–47.
[49]  Hemmati, H.D.; Nakano, I.; Lazareff, J.A.; Masterman-Smith, M.; Geschwind, D.H.; Bronner-Fraser, M.; Kornblum, H.I. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. USA 2003, 100, 15178–15183.
[50]  Singh, S.K.; Clarke, I.D.; Terasaki, M.; Bonn, V.E.; Hawkins, C.; Squire, J.; Dirks, P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63, 5821–5828.
[51]  Singh, S.K.; Hawkins, C.; Clarke, I.D.; Squire, J.A.; Bayani, J.; Hide, T.; Henkelman, R.M.; Cusimano, M.D.; Dirks, P.B. Identification of human brain tumour initiating cells. Nature 2004, 432, 396–401.
[52]  Quintana, E.; Shackleton, M.; Sabel, M.S.; Fullen, D.R.; Johnson, T.M.; Morrison, S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456, 593–598.
[53]  Boiko, A.D.; Razorenova, O.V.; van de Rijn, M.; Swetter, S.M.; Johnson, D.L.; Ly, D.P.; Butler, P.D.; Yang, G.P.; Joshua, B.; Kaplan, M.J.; Longaker, M.T.; Weissman, I.L. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 2010, 466, 133–137.
[54]  Dahlstrand, J.; Collins, V.P.; Lendahl, U. Expression of the class VI intermediate filament nestin in human central nervous system tumors. Cancer Res. 1992, 52, 5334–5341.
[55]  Ellis, P.; Fagan, B.M.; Magness, S.T.; Hutton, S.; Taranova, O.; Hayashi, S.; McMahon, A.; Rao, M.; Pevny, L. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 2004, 26, 148–165.
[56]  Favaro, R.; Valotta, M.; Ferri, A.L.; Latorre, E.; Mariani, J.; Giachino, C.; Lancini, C.; Tosetti, V.; Ottolenghi, S.; Taylor, V.; Nicolis, S.K. Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat. Neurosci. 2009, 12, 1248–1256.
[57]  Gangemi, R.M.; Griffero, F.; Marubbi, D.; Perera, M.; Capra, M.C.; Malatesta, P.; Ravetti, G.L.; Zona, G.L.; Daga, A.; Corte, G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009, 27, 40–48.
[58]  Kong, D.S.; Kim, M.H.; Park, W.Y.; Suh, Y.L.; Lee, J.I.; Park, K.; Kim, J.H.; Nam, D.H. The progression of gliomas is associated with cancer stem cell phenotype. Oncol. Rep. 2008, 19, 639–643.
[59]  Strojnik, T.; Rosland, G.V.; Sakariassen, P.O.; Kavalar, R.; Lah, T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg. Neurol. 2007, 68, 133–143.
[60]  Toda, M.; Iizuka, Y.; Yu, W.; Imai, T.; Ikeda, E.; Yoshida, K.; Kawase, T.; Kawakami, Y.; Okano, H.; Uyemura, K. Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 2001, 34, 1–7.
[61]  Lee, J.; Son, M.J.; Woolard, K.; Donin, N.M.; Li, A.; Cheng, C.H.; Kotliarova, S.; Kotliarov, Y.; Walling, J.; Ahn, S.; Kim, M.; Totonchy, M.; Cusack, T.; Ene, C.; Ma, H.; Su, Q.; Zenklusen, J.C.; Zhang, W.; Maric, D.; Fine, H.A. Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells. Cancer Cell 2008, 13, 69–80.
[62]  Singh, S.K.; Clarke, I.D.; Hide, T.; Dirks, P.B. Cancer stem cells in nervous system tumors. Oncogene 2004, 23, 7267–7273.
[63]  Galli, R.; Binda, E.; Orfanelli, U.; Cipelletti, B.; Gritti, A.; De Vitis, S.; Fiocco, R.; Foroni, C.; Dimeco, F.; Vescovi, A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64, 7011–7021.
[64]  Taylor, M.D.; Poppleton, H.; Fuller, C.; Su, X.; Liu, Y.; Jensen, P.; Magdaleno, S.; Dalton, J.; Calabrese, C.; Board, J.; Macdonald, T.; Rutka, J.; Guha, A.; Gajjar, A.; Curran, T.; Gilbertson, R.J. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 2005, 8, 323–335.
[65]  Yin, A.H.; Miraglia, S.; Zanjani, E.D.; Almeida-Porada, G.; Ogawa, M.; Leary, A.G.; Olweus, J.; Kearney, J.; Buck, D.W. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997, 90, 5002–5012.
[66]  Salven, P.; Mustjoki, S.; Alitalo, R.; Alitalo, K.; Rafii, S. VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 2003, 101, 168–172.
[67]  Uchida, N.; Buck, D.W.; He, D.; Reitsma, M.J.; Masek, M.; Phan, T.V.; Tsukamoto, A.S.; Gage, F.H.; Weissman, I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 2000, 97, 14720–14725.
[68]  Wang, J.; Sakariassen, P.O.; Tsinkalovsky, O.; Immervoll, H.; Boe, S.O.; Svendsen, A.; Prestegarden, L.; Rosland, G.; Thorsen, F.; Stuhr, L.; Molven, A.; Bjerkvig, R.; Enger, P.O. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer 2008, 122, 761–768.
[69]  Reynolds, B.A.; Vescovi, A.L. Brain cancer stem cells: Think twice before going flat. Cell Stem Cell 2009, 5, 466–467. author reply 468-469.
[70]  Abdouh, M.; Facchino, S.; Chatoo, W.; Balasingam, V.; Ferreira, J.; Bernier, G. BMI1 sustains human glioblastoma multiforme stem cell renewal. J. Neurosci. 2009, 29, 8884–8896.
[71]  Campos, B.; Herold-Mende, C.C. Insight into the complex regulation of CD133 in glioma. Int. J. Cancer 2011, 128, 501–510.
[72]  Beier, D.; Hau, P.; Proescholdt, M.; Lohmeier, A.; Wischhusen, J.; Oefner, P.J.; Aigner, L.; Brawanski, A.; Bogdahn, U.; Beier, C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007, 67, 4010–4015.
[73]  Joo, K.M.; Nam, D.H. Prospective identification of cancer stem cells with the surface antigen CD133. Methods Mol. Biol. 2009, 568, 57–71.
[74]  Joo, K.M.; Kim, S.Y.; Jin, X.; Song, S.Y.; Kong, D.S.; Lee, J.I.; Jeon, J.W.; Kim, M.H.; Kang, B.G.; Jung, Y.; Jin, J.; Hong, S.C.; Park, W.Y.; Lee, D.S.; Kim, H.; Nam, D.H. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab. Invest. 2008, 88, 808–815.
[75]  Ogden, A.T.; Waziri, A.E.; Lochhead, R.A.; Fusco, D.; Lopez, K.; Ellis, J.A.; Kang, J.; Assanah, M.; McKhann, G.M.; Sisti, M.B.; McCormick, P.C.; Canoll, P.; Bruce, J.N. Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas. Neurosurgery 2008, 62, 505–514. discussion 514-505.
[76]  Son, M.J.; Woolard, K.; Nam, D.H.; Lee, J.; Fine, H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4, 440–452.
[77]  Capela, A.; Temple, S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev. Biol. 2006, 291, 300–313.
[78]  Capela, A.; Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002, 35, 865–875.
[79]  Chen, R.; Nishimura, M.C.; Bumbaca, S.M.; Kharbanda, S.; Forrest, W.F.; Kasman, I.M.; Greve, J.M.; Soriano, R.H.; Gilmour, L.L.; Rivers, C.S.; Modrusan, Z.; Nacu, S.; Guerrero, S.; Edgar, K.A.; Wallin, J.J.; Lamszus, K.; Westphal, M.; Heim, S.; James, C.D.; VandenBerg, S.R.; Costello, J.F.; Moorefield, S.; Cowdrey, C.J.; Prados, M.; Phillips, H.S. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 2010, 17, 362–375.
[80]  Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444, 756–760.
[81]  Facchino, S.; Abdouh, M.; Chatoo, W.; Bernier, G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J. Neurosci. 2010, 30, 10096–10111.
[82]  Pallini, R.; Ricci-Vitiani, L.; Montano, N.; Mollinari, C.; Biffoni, M.; Cenci, T.; Pierconti, F.; Martini, M.; De Maria, R.; Larocca, L.M. Expression of the stem cell marker CD133 in recurrent glioblastoma and its value for prognosis. Cancer 2010, 117, 162–174.
[83]  Nomura, T.; Goritz, C.; Catchpole, T.; Henkemeyer, M.; Frisen, J. EphB Signaling Controls Lineage Plasticity of Adult Neural Stem Cell Niche Cells. Cell Stem Cell 2010, 7, 730–743.
[84]  Mao, X.G.; Zhang, X.; Xue, X.Y.; Guo, G.; Wang, P.; Zhang, W.; Fei, Z.; Zhen, H.N.; You, S.W.; Yang, H. Brain Tumor Stem-Like Cells Identified by Neural Stem Cell Marker CD15. Transl. Oncol. 2009, 2, 247–257.
[85]  Beckervordersandforth, R.; Tripathi, P.; Ninkovic, J.; Bayam, E.; Lepier, A.; Stempfhuber, B.; Kirchhoff, F.; Hirrlinger, J.; Haslinger, A.; Lie, D.C.; Beckers, J.; Yoder, B.; Irmler, M.; Gotz, M. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 2010, 7, 744–758.
[86]  Cui, H.; Ma, J.; Ding, J.; Li, T.; Alam, G.; Ding, H.F. Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J. Biol. Chem. 2006, 281, 34696–34704.
[87]  Molofsky, A.V.; Pardal, R.; Iwashita, T.; Park, I.K.; Clarke, M.F.; Morrison, S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425, 962–967.
[88]  Fasano, C.A.; Dimos, J.T.; Ivanova, N.B.; Lowry, N.; Lemischka, I.R.; Temple, S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 2007, 1, 87–99.
[89]  Jacobs, J.J.; Kieboom, K.; Marino, S.; DePinho, R.A.; van Lohuizen, M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999, 397, 164–168.
[90]  Hayry, V.; Tynninen, O.; Haapasalo, H.K.; Wolfer, J.; Paulus, W.; Hasselblatt, M.; Sariola, H.; Paetau, A.; Sarna, S.; Niemela, M.; Wartiovaara, K.; Nupponen, N.N. Stem cell protein BMI-1 is an independent marker for poor prognosis in oligodendroglial tumours. Neuropathol. Appl. Neurobiol. 2008, 34, 555–563.
[91]  Bruggeman, S.W.; Hulsman, D.; Tanger, E.; Buckle, T.; Blom, M.; Zevenhoven, J.; van Tellingen, O.; van Lohuizen, M. Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 2007, 12, 328–341.
[92]  Sharma, S.V.; Settleman, J. Exploiting the balance between life and death: targeted cancer therapy and “oncogenic shock”. Biochem. Pharmacol. 2010, 80, 666–673.
[93]  Felsher, D.W. Oncogene addiction versus oncogene amnesia: perhaps more than just a bad habit? Cancer Res. 2008, 68, 3081–3086. discussion 3086.
[94]  Kanamori, M.; Kawaguchi, T.; Nigro, J.M.; Feuerstein, B.G.; Berger, M.S.; Miele, L.; Pieper, R.O. Contribution of Notch signaling activation to human glioblastoma multiforme. J. Neurosurg. 2007, 106, 417–427.
[95]  Piccirillo, S.G.; Reynolds, B.A.; Zanetti, N.; Lamorte, G.; Binda, E.; Broggi, G.; Brem, H.; Olivi, A.; Dimeco, F.; Vescovi, A.L. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006, 444, 761–765.
[96]  Sherry, M.M.; Reeves, A.; Wu, J.K.; Cochran, B.H. STAT3 is required for proliferation and maintenance of multipotency in glioblastoma stem cells. Stem Cells 2009, 27, 2383–2392.
[97]  Bar, E.E.; Chaudhry, A.; Lin, A.; Fan, X.; Schreck, K.; Matsui, W.; Piccirillo, S.; Vescovi, A.L.; DiMeco, F.; Olivi, A.; Eberhart, C.G. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007, 25, 2524–2533.
[98]  Wang, J.; Wang, H.; Li, Z.; Wu, Q.; Lathia, J.D.; McLendon, R.E.; Hjelmeland, A.B.; Rich, J.N. c-Myc is required for maintenance of glioma cancer stem cells. PLoS One 2008, 3, e3769.
[99]  Kim, J.; Woo, A.J.; Chu, J.; Snow, J.W.; Fujiwara, Y.; Kim, C.G.; Cantor, A.B.; Orkin, S.H. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010, 143, 313–324.
[100]  Zheng, H.; Ying, H.; Yan, H.; Kimmelman, A.C.; Hiller, D.J.; Chen, A.J.; Perry, S.R.; Tonon, G.; Chu, G.C.; Ding, Z.; Stommel, J.M.; Dunn, K.L.; Wiedemeyer, R.; You, M.J.; Brennan, C.; Wang, Y.A.; Ligon, K.L.; Wong, W.H.; Chin, L.; DePinho, R.A. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008, 455, 1129–1133.
[101]  Leon, S.P.; Folkerth, R.D.; Black, P.M. Microvessel density is a prognostic indicator for patients with astroglial brain tumors. Cancer 1996, 77, 362–372.
[102]  Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86, 353–364.
[103]  Plate, K.H.; Risau, W. Angiogenesis in malignant gliomas. Glia 1995, 15, 339–347.
[104]  Tavazoie, M.; Van der Veken, L.; Silva-Vargas, V.; Louissaint, M.; Colonna, L.; Zaidi, B.; Garcia-Verdugo, J.M.; Doetsch, F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3, 279–288.
[105]  Bao, S.; Wu, Q.; Sathornsumetee, S.; Hao, Y.; Li, Z.; Hjelmeland, A.B.; Shi, Q.; McLendon, R.E.; Bigner, D.D.; Rich, J.N. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006, 66, 7843–7848.
[106]  Calabrese, C.; Poppleton, H.; Kocak, M.; Hogg, T.L.; Fuller, C.; Hamner, B.; Oh, E.Y.; Gaber, M.W.; Finklestein, D.; Allen, M.; Frank, A.; Bayazitov, I.T.; Zakharenko, S.S.; Gajjar, A.; Davidoff, A.; Gilbertson, R.J. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11, 69–82.
[107]  Folkins, C.; Shaked, Y.; Man, S.; Tang, T.; Lee, C.R.; Zhu, Z.; Hoffman, R.M.; Kerbel, R.S. Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1. Cancer Res. 2009, 69, 7243–7251.
[108]  Batchelor, T.T.; Sorensen, A.G.; di Tomaso, E.; Zhang, W.T.; Duda, D.G.; Cohen, K.S.; Kozak, K.R.; Cahill, D.P.; Chen, P.J.; Zhu, M.; Ancukiewicz, M.; Mrugala, M.M.; Plotkin, S.; Drappatz, J.; Louis, D.N.; Ivy, P.; Scadden, D.T.; Benner, T.; Loeffler, J.S.; Wen, P.Y.; Jain, R.K. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11, 83–95.
[109]  Friedman, H.S.; Prados, M.D.; Wen, P.Y.; Mikkelsen, T.; Schiff, D.; Abrey, L.E.; Yung, W.K.; Paleologos, N.; Nicholas, M.K.; Jensen, R.; Vredenburgh, J.; Huang, J.; Zheng, M.; Cloughesy, T. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 2009, 27, 4733–4740.
[110]  Miletic, H.; Niclou, S.P.; Johansson, M.; Bjerkvig, R. Anti-VEGF therapies for malignant glioma: treatment effects and escape mechanisms. Expert. Opin. Ther. Targets 2009, 13, 455–468.
[111]  Jensen, R.L.; Ragel, B.T.; Whang, K.; Gillespie, D. Inhibition of hypoxia inducible factor-1alpha (HIF-1alpha) decreases vascular endothelial growth factor (VEGF) secretion and tumor growth in malignant gliomas. J. Neurooncol. 2006, 78, 233–247.
[112]  Bar, E.E.; Lin, A.; Mahairaki, V.; Matsui, W.; Eberhart, C.G. Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am. J. Pathol. 2010, 177, 1491–1502.
[113]  Gillespie, D.L.; Whang, K.; Ragel, B.T.; Flynn, J.R.; Kelly, D.A.; Jensen, R.L. Silencing of hypoxia inducible factor-1alpha by RNA interference attenuates human glioma cell growth in vivo. Clin. Cancer Res. 2007, 13, 2441–2448.
[114]  Soeda, A.; Park, M.; Lee, D.; Mintz, A.; Androutsellis-Theotokis, A.; McKay, R.D.; Engh, J.; Iwama, T.; Kunisada, T.; Kassam, A.B.; Pollack, I.F.; Park, D.M. Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 2009, 28, 3949–3959.
[115]  Li, Z.; Bao, S.; Wu, Q.; Wang, H.; Eyler, C.; Sathornsumetee, S.; Shi, Q.; Cao, Y.; Lathia, J.; McLendon, R.E.; Hjelmeland, A.B.; Rich, J.N. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009, 15, 501–513.
[116]  Wang, R.; Chadalavada, K.; Wilshire, J.; Kowalik, U.; Hovinga, K.E.; Geber, A.; Fligelman, B.; Leversha, M.; Brennan, C.; Tabar, V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468, 829–833.
[117]  Ricci-Vitiani, L.; Pallini, R.; Biffoni, M.; Todaro, M.; Invernici, G.; Cenci, T.; Maira, G.; Parati, E.A.; Stassi, G.; Larocca, L.M.; De Maria, R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010, 468, 824–828.
[118]  Pistollato, F.; Abbadi, S.; Rampazzo, E.; Persano, L.; Della Puppa, A.; Frasson, C.; Sarto, E.; Scienza, R.; D'Avella, D.; Basso, G. Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma. Stem Cells 2010, 28, 851–862.
[119]  Hegi, M.E.; Diserens, A.C.; Gorlia, T.; Hamou, M.F.; de Tribolet, N.; Weller, M.; Kros, J.M.; Hainfellner, J.A.; Mason, W.; Mariani, L.; Bromberg, J.E.; Hau, P.; Mirimanoff, R.O.; Cairncross, J.G.; Janzer, R.C.; Stupp, R. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 2005, 352, 997–1003.
[120]  Challen, G.A.; Little, M.H. A side order of stem cells: the SP phenotype. Stem Cells 2006, 24, 3–12.
[121]  Eramo, A.; Ricci-Vitiani, L.; Zeuner, A.; Pallini, R.; Lotti, F.; Sette, G.; Pilozzi, E.; Larocca, L.M.; Peschle, C.; De Maria, R. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 2006, 13, 1238–1241.
[122]  Liu, G.; Yuan, X.; Zeng, Z.; Tunici, P.; Ng, H.; Abdulkadir, I.R.; Lu, L.; Irvin, D.; Black, K.L.; Yu, J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 2006, 5, 67.
[123]  Russo, A.L.; Kwon, H.C.; Burgan, W.E.; Carter, D.; Beam, K.; Weizheng, X.; Zhang, J.; Slusher, B.S.; Chakravarti, A.; Tofilon, P.J.; Camphausen, K. In vitro and in vivo radiosensitization of glioblastoma cells by the poly (ADP-ribose) polymerase inhibitor E7016. Clin. Cancer Res. 2009, 15, 607–612.
[124]  Chalmers, A.J. Overcoming resistance of glioblastoma to conventional cytotoxic therapies by the addition of PARP inhibitors. Anticancer Agents Med. Chem. 2010, 10, 520–533.
[125]  Tamura, K.; Aoyagi, M.; Wakimoto, H.; Ando, N.; Nariai, T.; Yamamoto, M.; Ohno, K. Accumulation of CD133-positive glioma cells after high-dose irradiation by Gamma Knife surgery plus external beam radiation. J. Neurosurg. 2010, 113, 310–318.
[126]  Kalyani, A.; Hobson, K.; Rao, M.S. Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev. Biol. 1997, 186, 202–223.
[127]  Cai, J.; Wu, Y.; Mirua, T.; Pierce, J.L.; Lucero, M.T.; Albertine, K.H.; Spangrude, G.J.; Rao, M.S. Properties of a fetal multipotent neural stem cell (NEP cell). Dev. Biol. 2002, 251, 221–240.
[128]  Shin, S.; Mitalipova, M.; Noggle, S.; Tibbitts, D.; Venable, A.; Rao, R.; Stice, S.L. Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions. Stem Cells 2006, 24, 125–138.
[129]  Tohyama, T.; Lee, V.M.; Rorke, L.B.; Marvin, M.; McKay, R.D.; Trojanowski, J.Q. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest. 1992, 66, 303–313.
[130]  Duparc, R.H.; Abdouh, M.; David, J.; Lepine, M.; Tetreault, N.; Bernier, G. Pax6 controls the proliferation rate of neuroepithelial progenitors from the mouse optic vesicle. Dev. Biol. 2007, 301, 374–387.
[131]  Clarke, S.R.; Shetty, A.K.; Bradley, J.L.; Turner, D.A. Reactive astrocytes express the embryonic intermediate neurofilament nestin. Neuroreport 1994, 5, 1885–1888.
[132]  Misson, J.P.; Edwards, M.A.; Yamamoto, M.; Caviness, V.S., Jr. Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Brain Res. Dev. Brain Res. 1988, 44, 95–108.
[133]  Feng, L.; Hatten, M.E.; Heintz, N. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 1994, 12, 895–908.
[134]  Shibata, T.; Yamada, K.; Watanabe, M.; Ikenaka, K.; Wada, K.; Tanaka, K.; Inoue, Y. Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci. 1997, 17, 9212–9219.
[135]  Warren, N.; Caric, D.; Pratt, T.; Clausen, J.A.; Asavaritikrai, P.; Mason, J.O.; Hill, R.E.; Price, D.J. The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb. Cortex 1999, 9, 627–635.
[136]  Woodhams, P.L.; Basco, E.; Hajos, F.; Csillag, A.; Balazs, R. Radial glia in the developing mouse cerebral cortex and hippocampus. Anat. Embryol. (Berl) 1981, 163, 331–343.
[137]  Sarnat, H.B. Molecular genetic classification of central nervous system malformations. J. Child. Neurol. 2000, 15, 675–687.
[138]  Nam, H.S.; Benezra, R. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 2009, 5, 515–526.
[139]  Doetsch, F.; Garcia-Verdugo, J.M.; Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17, 5046–5061.
[140]  Doetsch, F.; Petreanu, L.; Caille, I.; Garcia-Verdugo, J.M.; Alvarez-Buylla, A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002, 36, 1021–1034.
[141]  Liu, H.K.; Belz, T.; Bock, D.; Takacs, A.; Wu, H.; Lichter, P.; Chai, M.; Schutz, G. The nuclear receptor tailless is required for neurogenesis in the adult subventricular zone. Genes Dev. 2008, 22, 2473–2478.
[142]  Sakakibara, S.; Okano, H. Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J. Neurosci. 1997, 17, 8300–8312.
[143]  Lagace, D.C.; Whitman, M.C.; Noonan, M.A.; Ables, J.L.; DeCarolis, N.A.; Arguello, A.A.; Donovan, M.H.; Fischer, S.J.; Farnbauch, L.A.; Beech, R.D.; DiLeone, R.J.; Greer, C.A.; Mandyam, C.D.; Eisch, A.J. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 2007, 27, 12623–12629.
[144]  Hartfuss, E.; Galli, R.; Heins, N.; Gotz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 2001, 229, 15–30.
[145]  Bruggeman, S.W.; Hulsman, D.; van Lohuizen, M. Bmi1 deficient neural stem cells have increased integrin dependent adhesion to self-secreted matrix. Biochim. Biophys. Acta 2009, 1790, 351–360.
[146]  Bhoopathi, P.; Chetty, C.; Kunigal, S.; Vanamala, S.K.; Rao, J.S.; Lakka, S.S. Blockade of tumor growth due to matrix metalloproteinase-9 inhibition is mediated by sequential activation of beta1-integrin, ERK, and NF-kappaB. J. Biol. Chem. 2008, 283, 1545–1552.
[147]  Park, I.K.; Qian, D.; Kiel, M.; Becker, M.W.; Pihalja, M.; Weissman, I.L.; Morrison, S.J.; Clarke, M.F. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003, 423, 302–305.

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