Brain tumor stem cells: Molecular characteristics and their impact on therapy

Molecular Aspects of Medicine

Volumn 39, Issue , 2013, Pages 82-101

  Schonberg, David L ^a   Lubelski, Daniel ^a,b   Miller, Tyler E ^a,c   Rich, Jeremy N ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epigenetics; Glioma stem cells; Hypoxia; Microenvironment; Therapeutic resistance

Indexed keywords

BETA CATENIN; BMI1 PROTEIN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; CARBOPLATIN; ETOPOSIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MICRORNA; MICRORNA 124; MICRORNA 128; MICRORNA 146A; MICRORNA 34A; MYC PROTEIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PACLITAXEL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SONIC HEDGEHOG PROTEIN; STAT3 PROTEIN; TEMOZOLOMIDE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

CANCER STEM CELL; CELL EXPANSION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; DNA METHYLATION; GENE OVEREXPRESSION; GLIOBLASTOMA; HISTONE METHYLATION; HUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE; THERAPY RESISTANCE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; TUMOR MICROENVIRONMENT; ANIMAL; BRAIN NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; GENETIC EPIGENESIS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; RADIATION DOSE; RADIATION RESPONSE;

ANIMALS; BRAIN NEOPLASMS; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; GLIOBLASTOMA; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; RADIATION TOLERANCE; SIGNAL TRANSDUCTION;

EID: 84907003006     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2013.06.004     Document Type: Review

References (249)

1. M. Abdouh, S. Facchino, W. Chatoo, V. Balasingam, J. Ferreira, and G. Bernier BMI1 sustains human glioblastoma multiforme stem cell renewal J. Neurosci. Off. J. Soc. Neurosci. 29 2009 8884 8896
2. S. Acquati, A. Greco, D. Licastro, H. Bhagat, D. Ceric, Z. Rossini, J. Grieve, M. Shaked-Rabi, N.V. Henriquez, S. Brandner, E. Stupka, and S. Marino Epigenetic regulation of survivin by Bmi1 is cell type specific during corticogenesis and in gliomas Stem Cells (Dayton Ohio) 31 2013 190 202
3. C. Adamson, O.O. Kanu, A.I. Mehta, C. Di, N. Lin, A.K. Mattox, and D.D. Bigner Glioblastoma multiforme: a review of where we have been and where we are going Expert Opin. Investig. Drugs 18 2009 1061 1083
4. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. USA 100 2003 3983 3988
5. M.M. Alonso, H. Jiang, C. Gomez-Manzano, and J. Fueyo Targeting brain tumor stem cells with oncolytic adenoviruses Methods Mol. Biol. Clifton NJ 797 2012 111 125
6. J.M. Angelastro, and M.W. Lamé Overexpression of CD133 promotes drug resistance in C6 glioma cells Mol. Cancer Res. 8 2010 1105 1115
7. J. Anido, A. Sáez-Borderías, A. Gonzàlez-Juncà, L. Rodón, G. Folch, M.A. Carmona, R.M. Prieto-Sánchez, I. Barba, E. Martínez-Sáez, L. Prudkin, I. Cuartas, C. Raventós, F. Martínez-Ricarte, M.A. Poca, D. García-Dorado, M.M. Lahn, J.M. Yingling, J. Rodón, J. Sahuquillo, J. Baselga, and J. Seoane TGF-β receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma Cancer Cell 18 2010 655 668
8. S. Asuthkar, K.K. Velpula, C. Chetty, B. Gorantla, and J.S. Rao Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity Oncotarget 3 2012 1439 1454
9. S. Bao, Q. Wu, Z. Li, S. Sathornsumetee, H. Wang, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Targeting cancer stem cells through L1CAM suppresses glioma growth Cancer Res. 68 2008 6043 6048
10. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, A.B. Hjelmeland, M.W. Dewhirst, D.D. Bigner, and J.N. Rich Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760
11. S. Bao, Q. Wu, S. Sathornsumetee, Y. Hao, Z. Li, A.B. Hjelmeland, Q. Shi, R.E. McLendon, D.D. Bigner, and J.N. Rich Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor Cancer Res. 66 2006 7843 7848
12. E.E. Bar, A. Chaudhry, A. Lin, X. Fan, K. Schreck, W. Matsui, S. Piccirillo, A.L. Vescovi, F. DiMeco, A. Olivi, and C.G. Eberhart Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma Stem Cells (Dayton Ohio) 25 2007 2524 2533
13. E.E. Bar, A. Lin, V. Mahairaki, W. Matsui, and C.G. Eberhart Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres Am. J. Pathol. 177 2010 1491 1502
14. L.E. Barrett, Z. Granot, C. Coker, A. Iavarone, D. Hambardzumyan, E.C. Holland, H. Nam, and R. Benezra Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma Cancer Cell 21 2012 11 24
15. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
16. T.T. Batchelor, D.G. Duda, E. di Tomaso, M. Ancukiewicz, S.R. Plotkin, E. Gerstner, A.F. Eichler, J. Drappatz, F.H. Hochberg, T. Benner, D.N. Louis, K.S. Cohen, H. Chea, A. Exarhopoulos, J.S. Loeffler, M.A. Moses, P. Ivy, A.G. Sorensen, P.Y. Wen, and R.K. Jain Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 28 2010 2817 2823
17. T.T. Batchelor, A.G. Sorensen, E. di Tomaso, W.-T. Zhang, D.G. Duda, K.S. Cohen, K.R. Kozak, D.P. Cahill, P.-J. Chen, M. Zhu, M. Ancukiewicz, M.M. Mrugala, S. Plotkin, J. Drappatz, D.N. Louis, P. Ivy, D.T. Scadden, T. Benner, J.S. Loeffler, P.Y. Wen, and R.K. Jain AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients Cancer Cell 11 2007 83 95
18. D. Beier, S. Röhrl, D.R. Pillai, S. Schwarz, L.A. Kunz-Schughart, P. Leukel, M. Proescholdt, A. Brawanski, U. Bogdahn, A. Trampe-Kieslich, B. Giebel, J. Wischhusen, G. Reifenberger, P. Hau, and C.P. Beier Temozolomide preferentially depletes cancer stem cells in glioblastoma Cancer Res. 68 2008 5706 5715
19. D. Bexell, S. Gunnarsson, P. Siesjö, J. Bengzon, and A. Darabi CD133+ and nestin+ tumor-initiating cells dominate in N29 and N32 experimental gliomas Int. J. Cancer J. Int. Cancer 125 2009 15 22
20. K.P.L. Bhat, K.L. Salazar, V. Balasubramaniyan, K. Wani, L. Heathcock, F. Hollingsworth, J.D. James, J. Gumin, K.L. Diefes, S.H. Kim, A. Turski, Y. Azodi, Y. Yang, T. Doucette, H. Colman, E.P. Sulman, F.F. Lang, G. Rao, S. Copray, B.D. Vaillant, and K.D. Aldape The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma Genes Dev. 25 2011 2594 2609
21. J.M. Bishop Retroviruses and cancer genes Adv. Cancer Res. 37 1982 1 32
22. E.R. Blazek, J.L. Foutch, and G. Maki Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133- cells, and the CD133+ sector is enlarged by hypoxia Int. J. Radiat. Oncol. Biol. Phys. 67 2007 1 5
23. A.-M. Bleau, D. Hambardzumyan, T. Ozawa, E.I. Fomchenko, J.T. Huse, C.W. Brennan, and E.C. Holland PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells Cell Stem Cell 4 2009 226 235
24. D. Bonnet, and J.E. Dick Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat. Med. 3 1997 730 737
25. K.W.R. Broadley, M.K. Hunn, K.J. Farrand, K.M. Price, C. Grasso, R.J. Miller, I.F. Hermans, and M.J. McConnell Side population is not necessary or sufficient for a cancer stem cell phenotype in glioblastoma multiforme Stem Cells (Dayton Ohio) 29 2011 452 461
26. S.W.M. Bruggeman, D. Hulsman, E. Tanger, T. Buckle, M. Blom, J. Zevenhoven, O. van Tellingen, and M. van Lohuizen Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma Cancer Cell 12 2007 328 341
27. A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, L.S. Hu, M.J. Anderson, K.C. Arden, J. Blenis, and M.E. Greenberg Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 96 1999 857 868
28. C. Calabrese, H. Poppleton, M. Kocak, T.L. Hogg, C. Fuller, B. Hamner, E.Y. Oh, M.W. Gaber, D. Finklestein, M. Allen, A. Frank, I.T. Bayazitov, S.S. Zakharenko, A. Gajjar, A. Davidoff, and R.J. Gilbertson A perivascular niche for brain tumor stem cells Cancer Cell 11 2007 69 82
29. Y. Cao, J.D. Lathia, C.E. Eyler, Q. Wu, Z. Li, H. Wang, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Erythropoietin receptor signaling through STAT3 is required for glioma stem cell maintenance Genes Cancer 1 2010 50 61
30. M.H. Cardone, N. Roy, H.R. Stennicke, G.S. Salvesen, T.F. Franke, E. Stanbridge, S. Frisch, and J.C. Reed Regulation of cell death protease caspase-9 by phosphorylation Science 282 1998 1318 1321
31. H. Carén, S.M. Pollard, and S. Beck The good, the bad and the ugly: epigenetic mechanisms in glioblastoma Mol. Aspects Med. 34 2013 849 862
32. P. Carmeliet, and R.K. Jain Angiogenesis in cancer and other diseases Nature 407 2000 249 257
33. J. Cayuso, F. Ulloa, B. Cox, J. Briscoe, and E. Martí The Sonic hedgehog pathway independently controls the patterning, proliferation and survival of neuroepithelial cells by regulating Gli activity Dev. Camb. Eng. 133 2006 517 528
34. J. Chen, Y. Li, T.-S. Yu, R.M. McKay, D.K. Burns, S.G. Kernie, and L.F. Parada A restricted cell population propagates glioblastoma growth after chemotherapy Nature 488 2012 522 526
35. X. Chen, L. Chen, R. Zhang, Y. Yi, Y. Ma, K. Yan, X. Jiang, and X. Wang ADAM17 regulates self-renewal and differentiation of U87 glioblastoma stem cells Neurosci. Lett. 537 2013 44 49
36. L. Cheng, S. Bao, and J.N. Rich Potential therapeutic implications of cancer stem cells in glioblastoma Biochem. Pharmacol. 80 2010 654 665
37. L. Cheng, Z. Huang, W. Zhou, Q. Wu, S. Donnola, J.K. Liu, X. Fang, A.E. Sloan, Y. Mao, J.D. Lathia, W. Min, R.E. McLendon, J.N. Rich, and S. Bao Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth Cell 153 2013 139 152
38. L. Cheng, Q. Wu, Z. Huang, O.A. Guryanova, Q. Huang, W. Shou, J.N. Rich, and S. Bao L1CAM regulates DNA damage checkpoint response of glioblastoma stem cells through NBS1 Embo J. 30 2011 800 813
39. D.A. Chistiakov, and V.P. Chekhonin Contribution of microRNAs to radio- and chemoresistance of brain tumors and their therapeutic potential Eur. J. Pharmacol. 684 2012 8 18
40. G. Choe, S. Horvath, T.F. Cloughesy, K. Crosby, D. Seligson, A. Palotie, L. Inge, B.L. Smith, C.L. Sawyers, and P.S. Mischel Analysis of the phosphatidylinositol 3′-kinase signaling pathway in glioblastoma patients in vivo Cancer Res. 63 2003 2742 2746
41. V. Clement, P. Sanchez, N. de Tribolet, I. Radovanovic, and A. Ruiz i Altaba HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity Curr. Biol. 17 2007 165 172
42. H. Clevers Wnt/beta-catenin signaling in development and disease Cell 127 2006 469 480
43. C.J. Creighton, X. Li, M. Landis, J.M. Dixon, V.M. Neumeister, A. Sjolund, D.L. Rimm, H. Wong, A. Rodriguez, J.I. Herschkowitz, C. Fan, X. Zhang, X. He, A. Pavlick, M.C. Gutierrez, L. Renshaw, A.A. Larionov, D. Faratian, S.G. Hilsenbeck, C.M. Perou, M.T. Lewis, J.M. Rosen, and J.C. Chang Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features Proc. Natl. Acad. Sci. USA 106 2009 13820 13825
44. S.R. Datta, H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M.E. Greenberg Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 91 1997 231 241
45. N. De la Iglesia, G. Konopka, S.V. Puram, J.A. Chan, R.M. Bachoo, M.J. You, D.E. Levy, R.A. Depinho, and A. Bonni Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway Genes Dev. 22 2008 449 462
46. N. De la Iglesia, S.V. Puram, and A. Bonni STAT3 regulation of glioblastoma pathogenesis Curr. Mol. Med. 9 2009 580 590
47. A. Desjardins, D.A. Reardon, J.E. Herndon 2nd, J. Marcello, J.A. Quinn, J.N. Rich, S. Sathornsumetee, S. Gururangan, J. Sampson, L. Bailey, D.D. Bigner, A.H. Friedman, H.S. Friedman, and J.J. Vredenburgh Bevacizumab plus irinotecan in recurrent WHO grade 3 malignant gliomas Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 14 2008 7068 7073
48. M.W. Dewhirst, Y. Cao, and B. Moeller Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response Nat. Rev. Cancer 8 2008 425 437
49. P. Diamandis, J. Wildenhain, I.D. Clarke, A.G. Sacher, J. Graham, D.S. Bellows, E.K.M. Ling, R.J. Ward, L.G. Jamieson, M. Tyers, and P.B. Dirks Chemical genetics reveals a complex functional ground state of neural stem cells Nat. Chem. Biol. 3 2007 268 273
50. Z. Du, D. Jia, S. Liu, F. Wang, G. Li, Y. Zhang, X. Cao, E.-A. Ling, and A. Hao Oct4 is expressed in human gliomas and promotes colony formation in glioma cells Glia 57 2009 724 733
51. M. Ehtesham, A. Sarangi, J.G. Valadez, S. Chanthaphaychith, M.W. Becher, T.W. Abel, R.C. Thompson, and M.K. Cooper Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells Oncogene 26 2007 5752 5761
52. C.I. Ene, L. Edwards, G. Riddick, M. Baysan, K. Woolard, S. Kotliarova, C. Lai, G. Belova, M. Cam, J. Walling, M. Zhou, H. Stevenson, H.S. Kim, K. Killian, T. Veenstra, R. Bailey, H. Song, W. Zhang, and H.A. Fine Histone demethylase Jumonji D3 (JMJD3) as a tumor suppressor by regulating p53 protein nuclear stabilization Plos One 7 2012 e51407
53. S.M. Evans, K.W. Jenkins, H.I. Chen, W.T. Jenkins, K.D. Judy, W.-T. Hwang, R.A. Lustig, A.R. Judkins, M.S. Grady, S.M. Hahn, and C.J. Koch The relationship among hypoxia, proliferation, and outcome in patients with de novo glioblastoma: a pilot study Transl. Oncol. 3 2010 160 169
54. C.E. Eyler, W.-C. Foo, K.M. LaFiura, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Brain cancer stem cells display preferential sensitivity to Akt inhibition Stem Cells (Dayton Ohio) 26 2008 3027 3036
55. S. Facchino, M. Abdouh, W. Chatoo, and G. Bernier BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery J. Neurosci. Off. J. Soc. Neurosci. 30 2010 10096 10111
56. X. Fan, L. Khaki, T.S. Zhu, M.E. Soules, C.E. Talsma, N. Gul, C. Koh, J. Zhang, Y.-M. Li, J. Maciaczyk, G. Nikkhah, F. Dimeco, S. Piccirillo, A.L. Vescovi, and C.G. Eberhart NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts Stem Cells (Dayton Ohio) 28 2010 5 16
57. X. Fan, W. Matsui, L. Khaki, D. Stearns, J. Chun, Y.-M. Li, and C.G. Eberhart Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors Cancer Res. 66 2006 7445 7452
58. C. Folkins, Y. Shaked, S. Man, T. Tang, C.R. Lee, Z. Zhu, R.M. Hoffman, and R.S. Kerbel Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1 Cancer Res. 69 2009 7243 7251
59. F.B. Furnari, T. Fenton, R.M. Bachoo, A. Mukasa, J.M. Stommel, A. Stegh, W.C. Hahn, K.L. Ligon, D.N. Louis, C. Brennan, L. Chin, R.A. DePinho, and W.K. Cavenee Malignant astrocytic glioma: genetics, biology, and paths to treatment Genes Dev. 21 2007 2683 2710
60. R. Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. Gritti, S. De Vitis, R. Fiocco, C. Foroni, F. Dimeco, and A. Vescovi Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma Cancer Res. 64 2004 7011 7021
61. G.L. Gallia, B.M. Tyler, C.L. Hann, I.-M. Siu, V.L. Giranda, A.L. Vescovi, H. Brem, and G.J. Riggins Inhibition of Akt inhibits growth of glioblastoma and glioblastoma stem-like cells Mol. Cancer Ther. 8 2009 386 393
62. M. Gallo, J. Ho, F.J. Coutinho, R. Vanner, L. Lee, R. Head, E.K.M. Ling, I.D. Clarke, and P.B. Dirks A tumorigenic MLL-homeobox network in human glioblastoma stem cells Cancer Res. 73 2013 417 427
63. R.M.R. Gangemi, F. Griffero, D. Marubbi, M. Perera, M.C. Capra, P. Malatesta, G.L. Ravetti, G.L. Zona, A. Daga, and G. Corte SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity Stem Cells (Dayton Ohio) 27 2009 40 48
64. N. Gaspar, L. Marshall, L. Perryman, D.A. Bax, S.E. Little, M. Viana-Pereira, S.Y. Sharp, G. Vassal, A.D.J. Pearson, R.M. Reis, D. Hargrave, P. Workman, and C. Jones MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature Cancer Res. 70 2010 9243 9252
65. Y. Ge, F. Zhou, H. Chen, C. Cui, D. Liu, Q. Li, Z. Yang, G. Wu, S. Sun, J. Gu, Y. Wei, and J. Jiang Sox2 is translationally activated by eukaryotic initiation factor 4E in human glioma-initiating cells Biochem. Biophys. Res. Commun. 397 2010 711 717
66. C.A. Gilbert, M.-C. Daou, R.P. Moser, and A.H. Ross Gamma-secretase inhibitors enhance temozolomide treatment of human gliomas by inhibiting neurosphere repopulation and xenograft recurrence Cancer Res. 70 2010 6870 6879
67. R.J. Gilbertson, and J.N. Rich Making a tumour's bed: glioblastoma stem cells and the vascular niche Nat. Rev. Cancer 7 2007 733 736
68. J. Godlewski, H.B. Newton, E.A. Chiocca, and S.E. Lawler MicroRNAs and glioblastoma; the stem cell connection Cell Death Differ. 17 2010 221 228
69. J. Godlewski, M.O. Nowicki, A. Bronisz, S. Williams, A. Otsuki, G. Nuovo, A. Raychaudhury, H.B. Newton, E.A. Chiocca, and S. Lawler Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal Cancer Res. 68 2008 9125 9130
70. A. Golebiewska, S. Bougnaud, D. Stieber, N.H.C. Brons, L. Vallar, F. Hertel, B. Klink, E. Schröck, R. Bjerkvig, and S.P. Niclou Side population in human glioblastoma is non-tumorigenic and characterizes brain endothelial cells Brain J. Neurol. 136 2013 1462 1475
71. A. Gong, and S. Huang FoxM1 and Wnt/β-catenin signaling in glioma stem cells Cancer Res. 72 2012 5658 5662
72. P. González-Gómez, P. Sánchez, and H. Mira MicroRNAs as regulators of neural stem cell-related pathways in glioblastoma multiforme Mol. Neurobiol. 44 2011 235 249
73. G. Gopisetty, J. Xu, D. Sampath, H. Colman, and V.K. Puduvalli Epigenetic regulation of CD133/PROM1 expression in glioma stem cells by Sp1/myc and promoter methylation 2012 Oncogene
74. T. Grigoryan, P. Wend, A. Klaus, and W. Birchmeier Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice Genes Dev. 22 2008 2308 2341
75. F. Guessous, Y. Zhang, A. Kofman, A. Catania, Y. Li, D. Schiff, B. Purow, and R. Abounader MicroRNA-34a is tumor suppressive in brain tumors and glioma stem cells Cell Cycle (Georgetown Tex.) 9 2010 1031 1036
76. P.-O. Guichet, I. Bieche, M. Teigell, C. Serguera, B. Rothhut, V. Rigau, F. Scamps, C. Ripoll, S. Vacher, S. Taviaux, H. Chevassus, H. Duffau, J. Mallet, A. Susini, D. Joubert, L. Bauchet, and J.-P. Hugnot Cell death and neuronal differentiation of glioblastoma stem-like cells induced by neurogenic transcription factors Glia 61 2013 225 239
77. Y. Guo, S. Liu, P. Wang, S. Zhao, F. Wang, L. Bing, Y. Zhang, E.-A. Ling, J. Gao, and A. Hao Expression profile of embryonic stem cell-associated genes Oct4, Sox2 and Nanog in human gliomas Histopathology 59 2011 763 775
78. O.A. Guryanova, Q. Wu, L. Cheng, J.D. Lathia, Z. Huang, J. Yang, J. MacSwords, C.E. Eyler, R.E. McLendon, J.M. Heddleston, W. Shou, D. Hambardzumyan, J. Lee, A.B. Hjelmeland, A.E. Sloan, M. Bredel, G.R. Stark, J.N. Rich, and S. Bao Nonreceptor tyrosine kinase BMX maintains self-renewal and tumorigenic potential of glioblastoma stem cells by activating STAT3 Cancer Cell 19 2011 498 511
79. D. Hägerstrand, X. He, M. Bradic Lindh, S. Hoefs, G. Hesselager, A. Ostman, and M. Nistér Identification of a SOX2-dependent subset of tumor- and sphere-forming glioblastoma cells with a distinct tyrosine kinase inhibitor sensitivity profile Neuro Oncol. 13 2011 1178 1191
80. D. Hambardzumyan, O.J. Becher, and E.C. Holland Cancer stem cells and survival pathways Cell Cycle (Georgetown Tex.) 7 2008 1371 1378
81. D. Hambardzumyan, O.J. Becher, M.K. Rosenblum, P.P. Pandolfi, K. Manova-Todorova, and E.C. Holland PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo Genes Dev. 22 2008 436 448
82. D. Hambardzumyan, M. Squatrito, E. Carbajal, and E.C. Holland Glioma formation, cancer stem cells, and akt signaling Stem Cell Rev. 4 2008 203 210
83. A.L. Harris Hypoxia-a key regulatory factor in tumour growth Nat. Rev. Cancer 2 2002 38 47
84. M.A. Harris, H. Yang, B.E. Low, J. Mukherjee, J. Mukherje, A. Guha, R.T. Bronson, L.D. Shultz, M.A. Israel, and K. Yun Cancer stem cells are enriched in the side population cells in a mouse model of glioma Cancer Res. 68 2008 10051 10059
85. W. Hartmann, B. Digon-Söntgerath, A. Koch, A. Waha, E. Endl, I. Dani, D. Denkhaus, C.G. Goodyer, N. Sörensen, O.D. Wiestler, and T. Pietsch Phosphatidylinositol 3′-kinase/AKT signaling is activated in medulloblastoma cell proliferation and is associated with reduced expression of PTEN Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 12 2006 3019 3027
86. V. Häyry, O. Tynninen, H.K. Haapasalo, J. Wölfer, W. Paulus, M. Hasselblatt, H. Sariola, A. Paetau, S. Sarna, M. Niemelä, K. Wartiovaara, and N.N. Nupponen Stem cell protein BMI-1 is an independent marker for poor prognosis in oligodendroglial tumours Neuropathol. Appl. Neurobiol. 34 2008 555 563
87. J.M. Heddleston, M. Hitomi, M. Venere, W.A. Flavahan, K. Yang, Y. Kim, S. Minhas, J.N. Rich, and A.B. Hjelmeland Glioma stem cell maintenance: the role of the microenvironment Curr. Pharm. Des. 17 2011 2386 2401
88. J.M. Heddleston, Z. Li, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype Cell Cycle (Georgetown Tex.) 8 2009 3274 3284
89. J.M. Heddleston, Q. Wu, M. Rivera, S. Minhas, J.D. Lathia, A.E. Sloan, O. Iliopoulos, A.B. Hjelmeland, and J.N. Rich Hypoxia-induced mixed-lineage leukemia 1 regulates glioma stem cell tumorigenic potential Cell Death Differ. 19 2012 428 439
90. M.E. Hegi, A.-C. Diserens, T. Gorlia, M.-F. Hamou, N. de Tribolet, M. Weller, J.M. Kros, J.A. Hainfellner, W. Mason, L. Mariani, J.E.C. Bromberg, P. Hau, R.O. Mirimanoff, J.G. Cairncross, R.C. Janzer, and R. Stupp MGMT gene silencing and benefit from temozolomide in glioblastoma N. Engl. J. Med. 352 2005 997 1003
91. H.D. Hemmati, I. Nakano, J.A. Lazareff, M. Masterman-Smith, D.H. Geschwind, M. Bronner-Fraser, and H.I. Kornblum Cancerous stem cells can arise from pediatric brain tumors Proc. Natl. Acad. Sci. USA 100 2003 15178 15183
92. A.B. Hjelmeland, Q. Wu, J.M. Heddleston, G.S. Choudhary, J. MacSwords, J.D. Lathia, R. McLendon, D. Lindner, A. Sloan, and J.N. Rich Acidic stress promotes a glioma stem cell phenotype Cell Death Differ. 18 2011 829 840
93. T. Hoey, W.-C. Yen, F. Axelrod, J. Basi, L. Donigian, S. Dylla, M. Fitch-Bruhns, S. Lazetic, I.-K. Park, A. Sato, S. Satyal, X. Wang, M.F. Clarke, J. Lewicki, and A. Gurney DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency Cell Stem Cell 5 2009 168 177
94. E.C. Holland, W.P. Hively, R.A. DePinho, and H.E. Varmus A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice Genes Dev. 12 1998 3675 3685
95. Z. Huang, L. Cheng, O.A. Guryanova, Q. Wu, and S. Bao Cancer stem cells in glioblastoma-molecular signaling and therapeutic targeting Protein Cell 1 2010 638 655
96. H. Ikushima, T. Todo, Y. Ino, M. Takahashi, K. Miyazawa, and K. Miyazono Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors Cell Stem Cell 5 2009 504 514
97. H. Ikushima, T. Todo, Y. Ino, M. Takahashi, N. Saito, K. Miyazawa, and K. Miyazono Glioma-initiating cells retain their tumorigenicity through integration of the Sox axis and Oct4 protein J. Biol. Chem. 286 2011 41434 41441
98. H.-M. Jeon, X. Jin, J.-S. Lee, S.-Y. Oh, Y.-W. Sohn, H.-J. Park, K.M. Joo, W.-Y. Park, D.-H. Nam, R.A. DePinho, L. Chin, and H. Kim Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling Genes Dev. 22 2008 2028 2033
99. --mediated suppression of SOX2 Cancer Res. 71 2011 3410 3421
100. H. Jiang, and J. Fueyo Eradication of brain tumor stem cells with an oncolytic adenovirus Discov. Med. 10 2010 24 28
101. H. Jiang, C. Gomez-Manzano, H. Aoki, M.M. Alonso, S. Kondo, F. McCormick, J. Xu, Y. Kondo, B.N. Bekele, H. Colman, F.F. Lang, and J. Fueyo Examination of the therapeutic potential of Delta-24-RGD in brain tumor stem cells: role of autophagic cell death J. Natl. Cancer Inst. 99 2007 1410 1414
102. H. Jiang, C. Gomez-Manzano, F.F. Lang, R. Alemany, and J. Fueyo Oncolytic adenovirus: preclinical and clinical studies in patients with human malignant gliomas Curr. Gene Ther. 9 2009 422 427
103. X. Jin, H.-Y. Jeon, K.M. Joo, J.-K. Kim, J. Jin, S.H. Kim, B.G. Kang, S. Beck, S.J. Lee, J.K. Kim, A.-K. Park, W.-Y. Park, Y.-J. Choi, D.-H. Nam, and H. Kim Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation Cancer Res. 71 2011 3066 3075
104. X. Jin, Sung.-Hak. Kim, H.-M. Jeon, S. Beck, Y.-W. Sohn, J. Yin, J.-K. Kim, Y.C. Lim, J.-H. Lee, Se.-Hyuk. Kim, S.-H. Kang, X. Pian, M.-S. Song, J.B. Park, Y.-S. Chae, Y.-G. Chung, S.-H. Lee, Y.-J. Choi, D.-H. Nam, Y.K. Choi, and H. Kim Interferon regulatory factor 7 regulates glioma stem cells via interleukin-6 and Notch signalling Brain J. Neurol. 135 2012 1055 1069
105. M. Kanamori, T. Kawaguchi, J.M. Nigro, B.G. Feuerstein, M.S. Berger, L. Miele, and R.O. Pieper Contribution of Notch signaling activation to human glioblastoma multiforme J. Neurosurg. 106 2007 417 427
106. M.-K. Kang, and S.-K. Kang Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma Stem Cells Dev. 16 2007 837 847
107. K. Katsushima, K. Shinjo, A. Natsume, F. Ohka, M. Fujii, H. Osada, Y. Sekido, and Y. Kondo Contribution of microRNA-1275 to Claudin11 protein suppression via a polycomb-mediated silencing mechanism in human glioma stem-like cells J. Biol. Chem. 287 2012 27396 27406
108. N. Kaur, S. Chettiar, S. Rathod, P. Rath, D. Muzumdar, M.L. Shaikh, and A. Shiras Wnt3a mediated activation of Wnt/β-catenin signaling promotes tumor progression in glioblastoma Mol. Cell. Neurosci. 54 2013 44 57
109. B. Keith, and M.C. Simon Hypoxia-inducible factors, stem cells, and cancer Cell 129 2007 465 472
110. Y. Kim, K.H. Kim, Jeena. Lee, Y.-A. Lee, M. Kim, S.J. Lee, K. Park, H. Yang, J. Jin, K.M. Joo, Jeongwu. Lee, and D.-H. Nam Wnt activation is implicated in glioblastoma radioresistance Lab. Investig. J. Tech. Methods Pathol. 92 2012 466 473
111. R. Kopan Notch: a membrane-bound transcription factor J. Cell Sci. 115 2002 1095 1097
112. T. Lapidot, C. Sirard, J. Vormoor, B. Murdoch, T. Hoang, J. Caceres-Cortes, M. Minden, B. Paterson, M.A. Caligiuri, and J.E. Dick A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature 367 1994 645 648
113. J.D. Lathia, J. Gallagher, J.M. Heddleston, J. Wang, C.E. Eyler, J. Macswords, Q. Wu, A. Vasanji, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Integrin alpha 6 regulates glioblastoma stem cells Cell Stem Cell 6 2010 421 432
114. J.D. Lathia, M. Li, P.E. Hall, J. Gallagher, J.S. Hale, Q. Wu, M. Venere, E. Levy, M.R.S. Rani, P. Huang, E. Bae, J. Selfridge, L. Cheng, H. Guvenc, R.E. McLendon, I. Nakano, A.E. Sloan, H.S. Phillips, A. Lai, C.L. Gladson, M. Bredel, S. Bao, A.B. Hjelmeland, and J.N. Rich Laminin alpha 2 enables glioblastoma stem cell growth Ann. Neurol. 72 2012 766 778
115. J.D. Lathia, M.P. Mattson, and A. Cheng Notch: from neural development to neurological disorders J. Neurochem. 107 2008 1471 1481
116. J. Lee, S. Kotliarova, Y. Kotliarov, A. Li, Q. Su, N.M. Donin, S. Pastorino, B.W. Purow, N. Christopher, W. Zhang, J.K. Park, and H.A. Fine 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 2006 391 403
117. J. Lee, M.J. Son, K. Woolard, N.M. Donin, A. Li, C.H. Cheng, S. Kotliarova, Y. Kotliarov, J. Walling, S. Ahn, M. Kim, M. Totonchy, T. Cusack, C. Ene, H. Ma, Q. Su, J.C. Zenklusen, W. Zhang, D. Maric, and H.A. Fine Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells Cancer Cell 13 2008 69 80
118. T.R. Leonardo, H.L. Schultheisz, J.F. Loring, and L.C. Laurent The functions of microRNAs in pluripotency and reprogramming Nat. Cell Biol. 14 2012 1114 1121
119. J.-L. Li, R.C.A. Sainson, C.E. Oon, H. Turley, R. Leek, H. Sheldon, E. Bridges, W. Shi, C. Snell, E.T. Bowden, H. Wu, P.S. Chowdhury, A.J. Russell, C.P. Montgomery, R. Poulsom, and A.L. Harris DLL4-Notch signaling mediates tumor resistance to anti-VEGF therapy in vivo Cancer Res. 71 2011 6073 6083
120. J.-L. Li, R.C.A. Sainson, W. Shi, R. Leek, L.S. Harrington, M. Preusser, S. Biswas, H. Turley, E. Heikamp, J.A. Hainfellner, and A.L. Harris Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo Cancer Res. 67 2007 11244 11253
121. X. Li, M.T. Lewis, J. Huang, C. Gutierrez, C.K. Osborne, M.-F. Wu, S.G. Hilsenbeck, A. Pavlick, X. Zhang, G.C. Chamness, H. Wong, J. Rosen, and J.C. Chang Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy J. Natl. Cancer Inst. 100 2008 672 679
122. Z. Li, S. Bao, Q. Wu, H. Wang, C. Eyler, S. Sathornsumetee, Q. Shi, Y. Cao, J. Lathia, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells Cancer Cell 15 2009 501 513
123. Z. Li, H. Wang, C.E. Eyler, A.B. Hjelmeland, and J.N. Rich Turning cancer stem cells inside out: an exploration of glioma stem cell signaling pathways J. Biol. Chem. 284 2009 16705 16709
124. K.L. Ligon, J.A. Alberta, A.T. Kho, J. Weiss, M.R. Kwaan, C.L. Nutt, D.N. Louis, C.D. Stiles, and D.H. Rowitch The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas J. Neuropathol. Exp. Neurol. 63 2004 499 509
125. K.L. Ligon, E. Huillard, S. Mehta, S. Kesari, H. Liu, J.A. Alberta, R.M. Bachoo, M. Kane, D.N. Louis, R.A. Depinho, D.J. Anderson, C.D. Stiles, and D.H. Rowitch Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma Neuron 53 2007 503 517
126. F.R.S. Lima, S.A. Kahn, R.C. Soletti, D. Biasoli, T. Alves, A.C.C. da Fonseca, C. Garcia, L. Romão, J. Brito, R. Holanda-Afonso, J. Faria, H. Borges, and V. Moura-Neto Glioblastoma: therapeutic challenges, what lies ahead Biochim. Biophys. Acta 1826 2012 338 349
127. M.M. Lino, A. Merlo, and J.-L. Boulay Notch signaling in glioblastoma: a developmental drug target? BMC Med. 8 2010 72
128. G. Liu, X. Yuan, Z. Zeng, P. Tunici, H. Ng, I.R. Abdulkadir, L. Lu, D. Irvin, K.L. Black, and J.S. Yu Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma Mol. Cancer 5 2006 67
129. S.L. Lomonaco, S. Finniss, C. Xiang, A. Decarvalho, F. Umansky, S.N. Kalkanis, T. Mikkelsen, and C. Brodie The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells Int. J. Cancer J. Int. Cancer 125 2009 717 722
130. S.L. Lomonaco, S. Finniss, C. Xiang, H.K. Lee, W. Jiang, N. Lemke, S.A. Rempel, T. Mikkelsen, and C. Brodie Cilengitide induces autophagy-mediated cell death in glioma cells Neuro Oncol. 13 2011 857 865
131. B. Manoranjan, X. Wang, R.M. Hallett, C. Venugopal, S.C. Mack, N. McFarlane, S.M. Nolte, K. Scheinemann, T. Gunnarsson, J.A. Hassell, M.D. Taylor, C. Lee, J. Triscott, C.M. Foster, C. Dunham, C. Hawkins, S.E. Dunn, and S.K. Singh FoxG1 interacts with Bmi1 to regulate self-renewal and tumorigenicity of medulloblastoma stem cells Stem Cells 31 2013 1266 1277
132. X. Mao, M. Yan, X. Xue, X. Zhang, H. Ren, G. Guo, P. Wang, W. Zhang, and J. Huo Overexpression of ZNF217 in glioblastoma contributes to the maintenance of glioma stem cells regulated by hypoxia-inducible factors Lab. Investig. J. Tech. Methods Pathol. 91 2011 1068 1078
133. V. Martín, A.M. Sanchez-Sanchez, F. Herrera, C. Gomez-Manzano, J. Fueyo, M.A. Alvarez-Vega, I. Antolín, and C. Rodriguez Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells Br. J. Cancer 108 2013 2005 2012
134. J. Mathieu, Z. Zhang, W. Zhou, A.J. Wang, J.M. Heddleston, C.M.A. Pinna, A. Hubaud, B. Stadler, M. Choi, M. Bar, M. Tewari, A. Liu, R. Vessella, R. Rostomily, D. Born, M. Horwitz, C. Ware, C.A. Blau, M.A. Cleary, J.N. Rich, and H. Ruohola-Baker HIF induces human embryonic stem cell markers in cancer cells Cancer Res. 71 2011 4640 4652
135. L.D. Mayo, and D.B. Donner A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus Proc. Natl. Acad. Sci. USA 98 2001 11598 11603
136. J. Mei, R. Bachoo, and C.-L. Zhang MicroRNA-146a inhibits glioma development by targeting Notch1 Mol. Cell. Biol. 31 2011 3584 3592
137. K. Mizutani, K. Yoon, L. Dang, A. Tokunaga, and N. Gaiano Differential Notch signalling distinguishes neural stem cells from intermediate progenitors Nature 449 2007 351 355
138. D.K. Moscatello, M. Holgado-Madruga, D.R. Emlet, R.B. Montgomery, and A.J. Wong Constitutive activation of phosphatidylinositol 3-kinase by a naturally occurring mutant epidermal growth factor receptor J. Biol. Chem. 273 1998 200 206
139. A. Murat, E. Migliavacca, T. Gorlia, W.L. Lambiv, T. Shay, M.-F. Hamou, N. de Tribolet, L. Regli, W. Wick, M.C.M. Kouwenhoven, J.A. Hainfellner, F.L. Heppner, P.-Y. Dietrich, Y. Zimmer, J.G. Cairncross, R.-C. Janzer, E. Domany, M. Delorenzi, R. Stupp, and M.E. Hegi Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26 2008 3015 3024
140. S. Nakata, B. Campos, J. Bageritz, J.L. Bermejo, N. Becker, F. Engel, T. Acker, S. Momma, C. Herold-Mende, P. Lichter, B. Radlwimmer, and V. Goidts LGR5 is a marker of poor prognosis in glioblastoma and is required for survival of brain cancer stem-like cells Brain Pathol. Zurich Switz. 23 2013 60 72
141. C.-S. Niu, D.-X. Li, Y.-H. Liu, X.-M. Fu, S.-F. Tang, and J. Li Expression of NANOG in human gliomas and its relationship with undifferentiated glioma cells Oncol. Rep. 26 2011 593 601
142. H. Noushmehr, D.J. Weisenberger, K. Diefes, H.S. Phillips, K. Pujara, B.P. Berman, F. Pan, C.E. Pelloski, E.P. Sulman, K.P. Bhat, R.G.W. Verhaak, K.A. Hoadley, D.N. Hayes, C.M. Perou, H.K. Schmidt, L. Ding, R.K. Wilson, D. Van Den Berg, H. Shen, H. Bengtsson, P. Neuvial, L.M. Cope, J. Buckley, J.G. Herman, S.B. Baylin, P.W. Laird, K. Aldape Cancer Genome Atlas.Research Network Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma Cancer Cell 17 2010 510 522
143. A.T. Ogden, A.E. Waziri, R.A. Lochhead, D. Fusco, K. Lopez, J.A. Ellis, J. Kang, M. Assanah, G.M. McKhann, M.B. Sisti, P.C. McCormick, P. Canoll, and J.N. Bruce Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas Neurosurgery 62 2008 505 514 discussion
144. K. Ohishi, B. Varnum-Finney, and I.D. Bernstein Delta-1 enhances marrow and thymus repopulating ability of human CD34(+)CD38(-) cord blood cells J. Clin. Invest. 110 2002 1165 1174
145. N. Oka, A. Soeda, A. Inagaki, M. Onodera, H. Maruyama, A. Hara, T. Kunisada, H. Mori, and T. Iwama VEGF promotes tumorigenesis and angiogenesis of human glioblastoma stem cells Biochem. Biophys. Res. Commun. 360 2007 553 559
146. S. Osuka, O. Sampetrean, T. Shimizu, I. Saga, N. Onishi, E. Sugihara, J. Okubo, S. Fujita, S. Takano, A. Matsumura, and H. Saya IGF1 receptor signaling regulates adaptive radioprotection in glioma stem cells Stem Cells (Dayton Ohio) 31 2012 627 640
147. D.M. Panchision, and R.D.G. McKay The control of neural stem cells by morphogenic signals Curr. Opin. Genet. Dev. 12 2002 478 487
148. B. Papp, and K. Plath Epigenetics of reprogramming to induced pluripotency Cell 152 2013 1324 1343
149. S. Pellegatta, P.L. Poliani, D. Corno, F. Menghi, F. Ghielmetti, B. Suarez-Merino, V. Caldera, S. Nava, M. Ravanini, F. Facchetti, M.G. Bruzzone, and G. Finocchiaro Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas Cancer Res. 66 2006 10247 10252
150. H.S. Phillips, S. Kharbanda, R. Chen, W.F. Forrest, R.H. Soriano, T.D. Wu, A. Misra, J.M. Nigro, H. Colman, L. Soroceanu, P.M. Williams, Z. Modrusan, B.G. Feuerstein, and K. Aldape Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis Cancer Cell 9 2006 157 173
151. S.G.M. Piccirillo, B.A. Reynolds, N. Zanetti, G. Lamorte, E. Binda, G. Broggi, H. Brem, A. Olivi, F. Dimeco, and A.L. Vescovi Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells Nature 444 2006 761 765
152. F. Pistollato, S. Abbadi, E. Rampazzo, L. Persano, A. Della Puppa, C. Frasson, E. Sarto, R. Scienza, D. D'avella, and G. Basso Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma Stem Cells (Dayton Ohio) 28 2010 851 862
153. N. Platet, S.Y. Liu, M.E. Atifi, L. Oliver, F.M. Vallette, F. Berger, and D. Wion Influence of oxygen tension on CD133 phenotype in human glioma cell cultures Cancer Lett. 258 2007 286 290
154. A. Presente, A. Andres, and J.S. Nye Requirement of Notch in adulthood for neurological function and longevity Neuroreport 12 2001 3321 3325
155. T. Pulvirenti, M. Van Der Heijden, L.A. Droms, J.T. Huse, V. Tabar, and A. Hall Dishevelled 2 signaling promotes self-renewal and tumorigenicity in human gliomas Cancer Res. 71 2011 7280 7290
156. S.V. Puram, C.M. Yeung, A. Jahani-Asl, C. Lin, N. de la Iglesia, G. Konopka, L. Jackson-Grusby, and A. Bonni STAT3-iNOS signaling mediates EGFRvIII-induced glial proliferation and transformation J. Neurosci. Off. J. Soc. Neurosci. 32 2012 7806 7818
157. B.W. Purow, R.M. Haque, M.W. Noel, Q. Su, M.J. Burdick, J. Lee, T. Sundaresan, S. Pastorino, J.K. Park, I. Mikolaenko, D. Maric, C.G. Eberhart, and H.A. Fine Expression of Notch-1 and its ligands, delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation Cancer Res. 65 2005 2353 2363
158. -/-astrocytes and render these cells gliomagenic in the brain of immunocompetent mice Plos One 8 2013 e56691
159. M. Rahman, L. Deleyrolle, V. Vedam-Mai, H. Azari, M. Abd-El-Barr, and B.A. Reynolds The cancer stem cell hypothesis: failures and pitfalls Neurosurgery 68 2011 531 545
160. T.-A. Read, M.P. Fogarty, S.L. Markant, R.E. McLendon, Z. Wei, D.W. Ellison, P.G. Febbo, and R.J. Wechsler-Reya Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma Cancer Cell 15 2009 135 147
161. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111
162. L. Ricci-Vitiani, R. Pallini, M. Biffoni, M. Todaro, G. Invernici, T. Cenci, G. Maira, E.A. Parati, G. Stassi, L.M. Larocca, and R. De Maria Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells Nature 468 2010 824 828
163. J.N. Rich The implications of the cancer stem cell hypothesis for neuro-oncology and neurology Future Neurol. 3 2008 265 273
164. J.N. Rich, and C.E. Eyler Cancer stem cells in brain tumor biology Cold Spring Harb. Symp. Quant. Biol. 73 2008 411 420
165. F.J. Rodriguez, B.A. Orr, K.L. Ligon, and C.G. Eberhart Neoplastic cells are a rare component in human glioblastoma microvasculature Oncotarget 3 2012 98 106
166. H.A. Rogers, S. Sousa, C. Salto, E. Arenas, B. Coyle, and R.G. Grundy WNT/β-catenin pathway activation in Myc immortalised cerebellar progenitor cells inhibits neuronal differentiation and generates tumours resembling medulloblastoma Br. J. Cancer 107 2012 1144 1152
167. M. Ropolo, A. Daga, F. Griffero, M. Foresta, G. Casartelli, A. Zunino, A. Poggi, E. Cappelli, G. Zona, R. Spaziante, G. Corte, and G. Frosina Comparative analysis of DNA repair in stem and nonstem glioma cell cultures Mol. Cancer Res. Mcr 7 2009 383 392
168. J.M. Rosen, and C.T. Jordan The increasing complexity of the cancer stem cell paradigm Science 324 2009 1670 1673
169. M. Rossi, L. Magnoni, C. Miracco, E. Mori, P. Tosi, L. Pirtoli, P. Tini, G. Oliveri, E. Cosci, and A. Bakker β-Catenin and Gli1 are prognostic markers in glioblastoma Cancer Biol. Ther. 11 2011 753 761
170. C.M. Rudin, C.L. Hann, J. Laterra, R.L. Yauch, C.A. Callahan, L. Fu, T. Holcomb, J. Stinson, S.E. Gould, B. Coleman, P.M. LoRusso, D.D. Von Hoff, F.J. de Sauvage, and J.A. Low Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449 N. Engl. J. Med. 361 2009 1173 1178
171. B. Ruiz i Altaba, A., Mas, C., Stecca The Gli code: an information nexus regulating cell fate, stemness and cancer Trends Cell Biol. 17 2007 438 447
172. K. Sai, S. Wang, V. Balasubramaniyan, C. Conrad, F.F. Lang, K. Aldape, S. Szymanski, I. Fokt, A. Dasgupta, T. Madden, S. Guan, Z. Chen, W.K. Alfred Yung, W. Priebe, and H. Colman Induction of cell-cycle arrest and apoptosis in glioblastoma stem-like cells by WP1193, a novel small molecule inhibitor of the JAK2/STAT3 pathway J. Neurooncol. 107 2012 487 501
173. N. Sanai, A. Alvarez-Buylla, and M.S. Berger Neural stem cells and the origin of gliomas N. Engl. J. Med. 353 2005 811 822
174. S. Sathornsumetee, Y. Cao, J.E. Marcello, J.E. Herndon 2nd, R.E. McLendon, A. Desjardins, H.S. Friedman, M.W. Dewhirst, J.J. Vredenburgh, and J.N. Rich Tumor angiogenic and hypoxic profiles predict radiographic response and survival in malignant astrocytoma patients treated with bevacizumab and irinotecan J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26 2008 271 278
175. A. Sato, M. Okada, K. Shibuya, E. Watanabe, S. Seino, K. Suzuki, Y. Narita, S. Shibui, T. Kayama, and C. Kitanaka Resveratrol promotes proteasome-dependent degradation of Nanog via p53 activation and induces differentiation of glioma stem cells Stem Cell Res. 11 2013 601 610
176. A.F. Schott, M.D. Landis, G. Dontu, K.A. Griffith, R.M. Layman, I. Krop, L.A. Paskett, H. Wong, L.E. Dobrolecki, M.T. Lewis, A.M. Froehlich, J. Paranilam, D.F. Hayes, M.S. Wicha, and J.C. Chang Preclinical and clinical studies of gamma secretase inhibitors with docetaxel on human breast tumors Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 19 2013 1512 1524
177. R. Schüle, C. Dictus, B. Campos, F. Wan, J. Felsberg, R. Ahmadi, F.-S. Centner, N. Grabe, G. Reifenberger, J.L. Bermejo, A. Unterberg, and C. Herold-Mende Potential canonical wnt pathway activation in high-grade astrocytomas ScientificWorldJournal 2012 2012 697313
178. S. Seidel, B.K. Garvalov, V. Wirta, L. von Stechow, A. Schänzer, K. Meletis, M. Wolter, D. Sommerlad, A.-T. Henze, M. Nistér, G. Reifenberger, J. Lundeberg, J. Frisén, and T. Acker A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha Brain J. Neurol. 133 2010 983 995
179. M. Shackleton, E. Quintana, E.R. Fearon, and S.J. Morrison Heterogeneity in cancer: cancer stem cells versus clonal evolution Cell 138 2009 822 829
180. M.H. Shahi, A. Lorente, and J.S. Castresana Hedgehog signalling in medulloblastoma, glioblastoma and neuroblastoma Oncol. Rep. 19 2008 681 688
181. D. Sheiness, L. Fanshier, and J.M. Bishop Identification of nucleotide sequences which may encode the oncogenic capacity of avian retrovirus MC29 J. Virol. 28 1978 600 610
182. A. Shervington, and C. Lu Expression of multidrug resistance genes in normal and cancer stem cells Cancer Invest. 26 2008 535 542
183. L. Shi, S. Zhang, K. Feng, F. Wu, Y. Wan, Z. Wang, J. Zhang, Y. Wang, W. Yan, Z. Fu, and Y. You MicroRNA-125b-2 confers human glioblastoma stem cells resistance to temozolomide through the mitochondrial pathway of apoptosis Int. J. Oncol. 40 2012 119 129
184. A.H. Shih, and E.C. Holland Notch signaling enhances nestin expression in gliomas Neoplasia (New York, N.Y.) 8 2006 1072 1082
185. A. Shiras, S.T. Chettiar, V. Shepal, G. Rajendran, G.R. Prasad, and P. Shastry Spontaneous transformation of human adult nontumorigenic stem cells to cancer stem cells is driven by genomic instability in a human model of glioblastoma Stem Cells (Dayton Ohio) 25 2007 1478 1489
186. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, J. Squire, and P.B. Dirks Identification of a cancer stem cell in human brain tumors Cancer Res. 63 2003 5821 5828
187. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks Identification of human brain tumour initiating cells Nature 432 2004 396 401
188. Z.D. Smith, and A. Meissner DNA methylation: roles in mammalian development Nat. Rev. Genet. 14 2013 204 220
189. Y. Soda, T. Marumoto, D. Friedmann-Morvinski, M. Soda, F. Liu, H. Michiue, S. Pastorino, M. Yang, R.M. Hoffman, S. Kesari, and I.M. Verma Transdifferentiation of glioblastoma cells into vascular endothelial cells Proc. Natl. Acad. Sci. USA 108 2011 4274 4280
190. A. Soeda, A. Inagaki, N. Oka, Y. Ikegame, H. Aoki, S.-I. Yoshimura, S. Nakashima, T. Kunisada, and T. Iwama Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells J. Biol. Chem. 283 2008 10958 10966
191. A. Soeda, M. Park, D. Lee, A. Mintz, A. Androutsellis-Theotokis, R.D. McKay, J. Engh, T. Iwama, T. Kunisada, A.B. Kassam, I.F. Pollack, and D.M. Park Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha Oncogene 28 2009 3949 3959
192. M.J. Son, K. Woolard, D.-H. Nam, J. Lee, and H.A. Fine SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma Cell Stem Cell 4 2009 440 452
193. B. Stecca, and A. Ruiz i Altaba Brain as a paradigm of organ growth: Hedgehog-Gli signaling in neural stem cells and brain tumors J. Neurobiol. 64 2005 476 490
194. S.H. Stricker, A. Feber, P.G. Engström, H. Carén, K.M. Kurian, Y. Takashima, C. Watts, M. Way, P. Dirks, P. Bertone, A. Smith, S. Beck, and S.M. Pollard Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner Genes Dev. 27 2013 654 669
195. R. Stupp, M.E. Hegi, W.P. Mason, M.J. van den Bent, M.J.B. Taphoorn, R.C. Janzer, S.K. Ludwin, A. Allgeier, B. Fisher, K. Belanger, P. Hau, A.A. Brandes, J. Gijtenbeek, C. Marosi, C.J. Vecht, K. Mokhtari, P. Wesseling, S. Villa, E. Eisenhauer, T. Gorlia, M. Weller, D. Lacombe, J.G. Cairncross, and R.-O. Mirimanoff Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial Lancet Oncol. 10 2009 459 466
196. P. Sun, S. Xia, B. Lal, C.G. Eberhart, A. Quinones-Hinojosa, J. Maciaczyk, W. Matsui, F. Dimeco, S.M. Piccirillo, A.L. Vescovi, and J. Laterra DNER, an epigenetically modulated gene, regulates glioblastoma-derived neurosphere cell differentiation and tumor propagation Stem Cells (Dayton Ohio) 27 2009 1473 1486
197. M.L. Suvà, N. Riggi, and B.E. Bernstein Epigenetic reprogramming in cancer Science 339 2013 1567 1570
198. M.-L. Suvà, N. Riggi, M. Janiszewska, I. Radovanovic, P. Provero, J.-C. Stehle, K. Baumer, M.-A. Le Bitoux, D. Marino, L. Cironi, V.E. Marquez, V. Clément, and I. Stamenkovic EZH2 is essential for glioblastoma cancer stem cell maintenance Cancer Res. 69 2009 9211 9218
199. N. Syed, J. Langer, K. Janczar, P. Singh, C. Lo Nigro, L. Lattanzio, H.M. Coley, E. Hatzimichael, J. Bomalaski, P. Szlosarek, M. Awad, K. O'Neil, F. Roncaroli, and T. Crook Epigenetic status of argininosuccinate synthetase and argininosuccinate lyase modulates autophagy and cell death in glioblastoma Cell Death Dis. 4 2013 e458
200. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
201. H. Takebayashi, S. Yoshida, M. Sugimori, H. Kosako, R. Kominami, M. Nakafuku, and Y. Nabeshima Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3 Mech. Dev. 99 2000 143 148
202. S. Tanaka, D.N. Louis, W.T. Curry, T.T. Batchelor, and J. Dietrich Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat. Rev. Clin. Oncol. 10 2013 14 26
203. M.D. Taylor, H. Poppleton, C. Fuller, X. Su, Y. Liu, P. Jensen, S. Magdaleno, J. Dalton, C. Calabrese, J. Board, T. Macdonald, J. Rutka, A. Guha, A. Gajjar, T. Curran, and R.J. Gilbertson Radial glia cells are candidate stem cells of ependymoma Cancer Cell 8 2005 323 335
204. A. Tchoghandjian, N. Baeza, C. Colin, M. Cayre, P. Metellus, C. Beclin, L. Ouafik, and D. Figarella-Branger A2B5 cells from human glioblastoma have cancer stem cell properties Brain Pathol. Zurich Switz. 20 2010 211 221
205. J.S. Tchorz, M. Tome, D. Cloëtta, B. Sivasankaran, M. Grzmil, R.M. Huber, F. Rutz-Schatzmann, F. Kirchhoff, N. Schaeren-Wiemers, M. Gassmann, B.A. Hemmings, A. Merlo, and B. Bettler Constitutive Notch2 signaling in neural stem cells promotes tumorigenic features and astroglial lineage entry Cell Death Dis. 3 2012 e325
206. D. Televantou, G. Karkavelas, P. Hytiroglou, S. Lampaki, G. Iliadis, P. Selviaridis, K.S. Polyzoidis, G. Fountzilas, and V. Kotoula DARPP32, STAT5 and STAT3 mRNA expression ratios in glioblastomas are associated with patient outcome Pathol. Oncol. Res. 19 2013 329 343
207. M.C. Thompson, C. Fuller, T.L. Hogg, J. Dalton, D. Finkelstein, C.C. Lau, M. Chintagumpala, A. Adesina, D.M. Ashley, S.J. Kellie, M.D. Taylor, T. Curran, A. Gajjar, and R.J. Gilbertson Genomics identifies medulloblastoma subgroups that are enriched for specific genetic alterations J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 24 2006 1924 1931
208. N. Thon, K. Damianoff, J. Hegermann, S. Grau, B. Krebs, O. Schnell, J.-C. Tonn, and R. Goldbrunner Presence of pluripotent CD133+ cells correlates with malignancy of gliomas Mol. Cell. Neurosci. 43 2010 51 59
209. A. Tobias, A. Ahmed, K.-S. Moon, and M.S. Lesniak The art of gene therapy for glioma: a review of the challenging road to the bedside J. Neurol. Neurosurg. Psychiatry 84 2013 213 222
210. M. Todaro, M.P. Alea, A.B. Di Stefano, P. Cammareri, L. Vermeulen, F. Iovino, C. Tripodo, A. Russo, G. Gulotta, J.P. Medema, and G. Stassi Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4 Cell Stem Cell 1 2007 389 402
211. S. Turcan, D. Rohle, A. Goenka, L.A. Walsh, F. Fang, E. Yilmaz, C. Campos, A.W.M. Fabius, C. Lu, P.S. Ward, C.B. Thompson, A. Kaufman, O. Guryanova, R. Levine, A. Heguy, A. Viale, L.G.T. Morris, J.T. Huse, I.K. Mellinghoff, and T.A. Chan IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype Nature 483 2012 479 483
212. -in glioma initiating cells requires NOTCH-1 signaling Stem Cells 31 2013 1252 1265
213. H. Uchida, K. Arita, S. Yunoue, H. Yonezawa, Y. Shinsato, H. Kawano, H. Hirano, R. Hanaya, and H. Tokimura Role of sonic hedgehog signaling in migration of cell lines established from CD133-positive malignant glioma cells J. Neurooncol. 104 2011 697 704
214. I.V. Ulasov, S. Nandi, M. Dey, A.M. Sonabend, and M.S. Lesniak Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy Mol. Med. Camb. Mass 17 2011 103 112
215. R.G.W. Verhaak, K.A. Hoadley, E. Purdom, V. Wang, Y. Qi, M.D. Wilkerson, C.R. Miller, L. Ding, T. Golub, J.P. Mesirov, G. Alexe, M. Lawrence, M. O'Kelly, P. Tamayo, B.A. Weir, S. Gabriel, W. Winckler, S. Gupta, L. Jakkula, H.S. Feiler, J.G. Hodgson, C.D. James, J.N. Sarkaria, C. Brennan, A. Kahn, P.T. Spellman, R.K. Wilson, T.P. Speed, J.W. Gray, M. Meyerson, G. Getz, C.M. Perou, D.N. Hayes, and Cancer.Genome.Atlas.Research. Network Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 Cancer Cell 17 2010 98 110
216. A.L. Vescovi, R. Galli, and B.A. Reynolds Brain tumour stem cells Nat. Rev. Cancer 6 2006 425 436
217. J.J. Vredenburgh, A. Desjardins, J.E. Herndon 2nd, J.M. Dowell, D.A. Reardon, J.A. Quinn, J.N. Rich, S. Sathornsumetee, S. Gururangan, M. Wagner, D.D. Bigner, A.H. Friedman, and H.S. Friedman Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 13 2007 1253 1259
218. H. Wakimoto, S. Kesari, C.J. Farrell, W.T. Curry Jr, C. Zaupa, M. Aghi, T. Kuroda, A. Stemmer-Rachamimov, K. Shah, T.-C. Liu, D.S. Jeyaretna, J. Debasitis, J. Pruszak, R.L. Martuza, and S.D. Rabkin Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors Cancer Res. 69 2009 3472 3481
219. H. Wang, J.D. Lathia, Q. Wu, J. Wang, Z. Li, J.M. Heddleston, C.E. Eyler, J. Elderbroom, J. Gallagher, J. Schuschu, J. MacSwords, Y. Cao, R.E. McLendon, X.-F. Wang, A.B. Hjelmeland, and J.N. Rich Targeting interleukin 6 signaling suppresses glioma stem cell survival and tumor growth Stem Cells (Dayton Ohio) 27 2009 2393 2404
220. J. Wang, T.P. Wakeman, J.D. Lathia, A.B. Hjelmeland, X.-F. Wang, R.R. White, J.N. Rich, and B.A. Sullenger Notch promotes radioresistance of glioma stem cells Stem Cells (Dayton Ohio) 28 2010 17 28
221. J. Wang, H. Wang, Z. Li, Q. Wu, J.D. Lathia, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich C-Myc is required for maintenance of glioma cancer stem cells Plos One 3 2008 e3769
222. R. Wang, K. Chadalavada, J. Wilshire, U. Kowalik, K.E. Hovinga, A. Geber, B. Fligelman, M. Leversha, C. Brennan, and V. Tabar Glioblastoma stem-like cells give rise to tumour endothelium Nature 468 2010 829 833
223. W.-J. Wang, L.-M. Long, N. Yang, Q.-Q. Zhang, W.-J. Ji, J.-H. Zhao, Z.-H. Qin, Z. Wang, G. Chen, and Z.-Q. Liang NVP-BEZ235, a novel dual PI3K/mTOR inhibitor, enhances the radiosensitivity of human glioma stem cells in vitro Acta Pharmacol. Sin. 34 2013 681 690
224. X. Wang, C. Venugopal, B. Manoranjan, N. McFarlane, E. O'Farrell, S. Nolte, T. Gunnarsson, R. Hollenberg, J. Kwiecien, P. Northcott, M.D. Taylor, C. Hawkins, and S.K. Singh Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells Oncogene 31 2012 187 199
225. R.J. Ward, L. Lee, K. Graham, T. Satkunendran, K. Yoshikawa, E. Ling, L. Harper, R. Austin, E. Nieuwenhuis, I.D. Clarke, C.-C. Hui, and P.B. Dirks Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma Cancer Res. 69 2009 4682 4690
226. J. Wei, J. Barr, L.-Y. Kong, Y. Wang, A. Wu, A.K. Sharma, J. Gumin, V. Henry, H. Colman, W. Priebe, R. Sawaya, F.F. Lang, and A.B. Heimberger Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway Mol. Cancer Ther. 9 2010 67 78
227. J. Wei, A. Wu, L.-Y. Kong, Y. Wang, G. Fuller, I. Fokt, G. Melillo, W. Priebe, and A.B. Heimberger Hypoxia potentiates glioma-mediated immunosuppression Plos One 6 2011 e16195
228. Y. Wei, Y. Jiang, F. Zou, Yingchao. Liu, S. Wang, N. Xu, W. Xu, C. Cui, Y. Xing, Ying. Liu, B. Cao, C. Liu, G. Wu, H. Ao, X. Zhang, and J. Jiang Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells Proc. Natl. Acad. Sci. USA 110 2013 6829 6834
229. C.K. Williams, M. Segarra, M.D.L.L. Sierra, R.C.A. Sainson, G. Tosato, and A.L. Harris Regulation of CXCR4 by the Notch ligand delta-like 4 in endothelial cells Cancer Res. 68 2008 1889 1895
230. W.A. Woodward, M.S. Chen, F. Behbod, M.P. Alfaro, T.A. Buchholz, and J.M. Rosen WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells Proc. Natl. Acad. Sci. USA 104 2007 618 623
231. A. Wu, J. Wei, L.-Y. Kong, Y. Wang, W. Priebe, W. Qiao, R. Sawaya, and A.B. Heimberger Glioma cancer stem cells induce immunosuppressive macrophages/microglia Neuro-Oncol. 12 2010 1113 1125
232. G.G. Wulf, R.Y. Wang, I. Kuehnle, D. Weidner, F. Marini, M.K. Brenner, M. Andreeff, and M.A. Goodell A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia Blood 98 2001 1166 1173
233. H. Xia, W.K.C. Cheung, S.S. Ng, X. Jiang, S. Jiang, J. Sze, G.K.K. Leung, G. Lu, D.T.M. Chan, X.-W. Bian, H. Kung, W.S. Poon, and M.C. Lin Loss of brain-enriched miR-124 microRNA enhances stem-like traits and invasiveness of glioma cells J. Biol. Chem. 287 2012 9962 9971
234. Q. Xu, X. Yuan, G. Liu, K.L. Black, and J.S. Yu Hedgehog signaling regulates brain tumor-initiating cell proliferation and portends shorter survival for patients with PTEN-coexpressing glioblastomas Stem Cells (Dayton Ohio) 26 2008 3018 3026
235. Y.-P. Yang, Y. Chien, G.-Y. Chiou, J.-Y. Cherng, M.-L. Wang, W.-L. Lo, Y.-L. Chang, P.-I. Huang, Y.-W. Chen, Y.-H. Shih, M.-T. Chen, and S.-H. Chiou Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI Biomaterials 33 2012 1462 1476
236. C.-H. Yoon, M.-J. Kim, R.-K. Kim, E.-J. Lim, K.-S. Choi, S. An, S.-G. Hwang, S.-G. Kang, Y. Suh, M.-J. Park, and S.-J. Lee C-Jun N-terminal kinase has a pivotal role in the maintenance of self-renewal and tumorigenicity in glioma stem-like cells Oncogene 31 2012 4655 4666
237. Y. Yoshida, K. Takahashi, K. Okita, T. Ichisaka, and S. Yamanaka Hypoxia enhances the generation of induced pluripotent stem cells Cell Stem Cell 5 2009 237 241
238. X. Yuan, J. Curtin, Y. Xiong, G. Liu, S. Waschsmann-Hogiu, D.L. Farkas, K.L. Black, and J.S. Yu Isolation of cancer stem cells from adult glioblastoma multiforme Oncogene 23 2004 9392 9400
239. K. Yuki, A. Natsume, H. Yokoyama, Y. Kondo, M. Ohno, T. Kato, P. Chansakul, M. Ito, S.-U. Kim, and T. Wakabayashi Induction of oligodendrogenesis in glioblastoma-initiating cells by IFN-mediated activation of STAT3 signaling Cancer Lett. 284 2009 71 79
240. M. Zbinden, A. Duquet, A. Lorente-Trigos, S.-N. Ngwabyt, I. Borges, and A. Ruiz i Altaba NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53 Embo J. 29 2010 2659 2674
241. M. Zhang, T. Song, L. Yang, R. Chen, L. Wu, Z. Yang, and J. Fang Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients J. Exp. Clin. Cancer Res. CR 27 2008 85
242. N. Zhang, P. Wei, A. Gong, W.-T. Chiu, H.-T. Lee, H. Colman, H. Huang, J. Xue, M. Liu, Y. Wang, R. Sawaya, K. Xie, W.K.A. Yung, R.H. Medema, X. He, and S. Huang FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis Cancer Cell 20 2011 427 442
243. Y. Zhang, A. Dutta, and R. Abounader The role of microRNAs in glioma initiation and progression Front. Biosci. J. Virtual Library 17 2012 700 712
244. H. Zheng, H. Ying, H. Yan, A.C. Kimmelman, D.J. Hiller, A.-J. Chen, S.R. Perry, G. Tonon, G.C. Chu, Z. Ding, J.M. Stommel, K.L. Dunn, R. Wiedemeyer, M.J. You, C. Brennan, Y.A. Wang, K.L. Ligon, W.H. Wong, L. Chin, and R.A. dePinho Pten and p53 converge on c-Myc to control differentiation, self-renewal, and transformation of normal and neoplastic stem cells in glioblastoma Cold Spring Harb. Symp. Quant. Biol. 73 2008 427 437
245. H. Zheng, H. Ying, H. Yan, A.C. Kimmelman, D.J. Hiller, A.-J. Chen, S.R. Perry, G. Tonon, G.C. Chu, Z. Ding, J.M. Stommel, K.L. Dunn, R. Wiedemeyer, M.J. You, C. Brennan, Y.A. Wang, K.L. Ligon, W.H. Wong, L. Chin, and R.A. DePinho P53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation Nature 455 2008 1129 1133
246. B.-B.S. Zhou, H. Zhang, M. Damelin, K.G. Geles, J.C. Grindley, and P.B. Dirks Tumour-initiating cells: challenges and opportunities for anticancer drug discovery Nat. Rev. Drug Discov. 8 2009 806 823
247. Q. Zhou, and D.J. Anderson The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification Cell 109 2002 61 73
248. Z. Zhou, L. Sun, Y. Wang, Z. Wu, J. Geng, W. Miu, Y. Pu, Y. You, Z. Yang, and N. Liu Bone morphogenetic protein 4 inhibits cell proliferation and induces apoptosis in glioma stem cells Cancer Biother. Radiopharm. 26 2011 77 83
249. W. Zhuang, B. Li, L. Long, L. Chen, Q. Huang, and Z. Liang Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity Int. J. Cancer J. Int. Cancer 129 2011 2720 2731