Table of Contents
International Journal of Brain Science
Volume 2014, Article ID 217503, 14 pages
http://dx.doi.org/10.1155/2014/217503
Review Article

On the Genesis of Neuroblastoma and Glioma

1Institut des Neurosciences de Montpellier, INSERM U1051, Hôpital St Eloi, 80 rue Augustin Fliche, 34091 Montpellier, France
2BetaInnov Research, Institut de Recherche en Biothérapie de Montpellier, Hôpital St Eloi, 80 rue Augustin Fliche, 34091 Montpellier, France

Received 20 September 2013; Accepted 29 December 2013; Published 26 March 2014

Academic Editor: João O. Malva

Copyright © 2014 Jan de Weille. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Schiffer, L. Annovazzi, V. Caldera, and M. Mellai, “On the origin and growth of gliomas,” Anticancer Research, vol. 30, no. 6, pp. 1977–1998, 2010. View at Google Scholar · View at Scopus
  2. N. Sanai, A. Alvarez-Buylla, and M. S. Berger, “Mechanisms of disease: neural stem cells and the origin of gliomas,” The New England Journal of Medicine, vol. 353, no. 8, pp. 811–822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. V. Melotte, X. Qu, M. Ongenaert et al., “The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications,” The FASEB Journal, vol. 24, no. 11, pp. 4153–4166, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Jiang, J. Stanke, and J. M. Lahti, “Chapter 4. The connections between neural crest development and neuroblastoma,” in Current Topics in Developmental Biology, vol. 94, pp. 77–127, Elsevier, New York, NY, USA, 2011. View at Publisher · View at Google Scholar
  5. E. C. Holland, “Progenitor cells and glioma formation,” Current Opinion in Neurology, vol. 14, no. 6, pp. 683–688, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. X. Fan, L. G. Salford, and B. Widegren, “Glioma stem cells: evidence and limitation,” Seminars in Cancer Biology, vol. 17, no. 3, pp. 214–218, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Dai and E. C. Holland, “Glioma models,” Biochimica et Biophysica Acta—Reviews on Cancer, vol. 1551, no. 1, pp. M19–M27, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. 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 and Development, vol. 12, no. 23, pp. 3675–3685, 1998. View at Google Scholar · View at Scopus
  9. W. A. Weiss, M. J. Burns, C. Hackett et al., “Genetic determinants of malignancy in a mouse model for oligodendroglioma,” Cancer Research, vol. 63, no. 7, pp. 1589–1595, 2003. View at Google Scholar · View at Scopus
  10. R. Galli, E. Binda, U. Orfanelli et al., “Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma,” Cancer Research, vol. 64, no. 19, pp. 7011–7021, 2004. View at Google Scholar · View at Scopus
  11. X. Yuan, J. Curtin, Y. Xiong et al., “Isolation of cancer stem cells from adult glioblastoma multiforme,” Oncogene, vol. 23, no. 58, pp. 9392–9400, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. S. K. Singh, C. Hawkins, I. D. Clarke et al., “Identification of human brain tumour initiating cells,” Nature, vol. 432, no. 7015, pp. 396–401, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. D. M. Park, J. Jung, J. Masjkur et al., “Hes3 regulates cell number in cultures from glioblastoma multiforme with stem cell characteristics,” Scientific Reports, vol. 3, article 1095, 2013. View at Publisher · View at Google Scholar
  14. T. Kondo and M. Raff, “Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells,” Science, vol. 289, no. 5485, pp. 1754–1757, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Dai, J. C. Celestino, Y. Okada, D. N. Louis, G. N. Fuller, and E. C. Holland, “PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas from and oligoastrocytomas neural progenitors and astrocytes in vivo,” Genes and Development, vol. 15, no. 15, pp. 1913–1925, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. B. A. Reynolds and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992. View at Google Scholar · View at Scopus
  17. C. S. Potten, G. Owen, and D. Booth, “Intestinal stem cells protect their genome by selective segregation of template DNA strands,” Journal of Cell Science, vol. 115, no. 11, pp. 2381–2388, 2002. View at Google Scholar · View at Scopus
  18. P. Karpowicz, C. Morshead, A. Kam et al., “Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro,” Journal of Cell Biology, vol. 170, no. 5, pp. 721–732, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Campisi, “Aging, cellular senescence, and cancer,” Annual Review of Physiology, vol. 75, pp. 685–705, 2013. View at Publisher · View at Google Scholar
  20. L. Li and W. B. Neaves, “Normal stem cells and cancer stem cells: the niche matters,” Cancer Research, vol. 66, no. 9, pp. 4553–4557, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. R. J. Gilbertson and J. N. Rich, “Making a tumour's bed: glioblastoma stem cells and the vascular niche,” Nature Reviews Cancer, vol. 7, no. 10, pp. 733–736, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature, vol. 414, no. 6859, pp. 105–111, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. S. J. Morrison and J. Kimble, “Asymmetric and symmetric stem-cell divisions in development and cancer,” Nature, vol. 441, no. 7097, pp. 1068–1074, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. H. J. Snippert and H. Clevers, “Tracking adult stem cells,” EMBO Reports, vol. 12, no. 2, pp. 113–122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. R. W. Miller, J. L. Young Jr., and B. Novakovic, “Childhood cancer,” Cancer, vol. 75, no. 1, pp. 395–405, 1995. View at Google Scholar · View at Scopus
  26. R. T. Greenlee, T. Murray, S. Bolden, and P. A. Wingo, “Cancer statistics, 2000,” Ca-A Cancer Journal for Clinicians, vol. 50, no. 1, pp. 7–33, 2000. View at Google Scholar · View at Scopus
  27. A. M. Linabery and J. A. Ross, “Trends in childhood cancer incidence in the U.S. (1992–2004),” Cancer, vol. 112, no. 2, pp. 416–432, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. F. A. Siebzehnrubl, B. A. Reynolds, A. Vescovi, D. A. Steindler, and L. P. Deleyrolle, “The origins of glioma: e pluribus unum?” Glia, vol. 59, no. 8, pp. 1135–1147, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. E. R. Fearon, S. R. Hamilton, and B. Vogelstein, “Clonal analysis of human colorectal tumors,” Science, vol. 238, no. 4824, pp. 193–197, 1987. View at Google Scholar · View at Scopus
  30. S. K. Nicolis, “Cancer stem cells and “stemness” genes in neuro-oncology,” Neurobiology of Disease, vol. 25, no. 2, pp. 217–229, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. F. A. Siebzehnrubl, I. Jeske, D. Müller et al., “Spontaneous in vitro transformation of adult neural precursors into stem-like cancer cells,” Brain Pathology, vol. 19, no. 3, pp. 399–408, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Hiyama, Y. Hirai, S. Kyoizumi et al., “Activation of telomerase in human lymphocytes and hematopoietic progenitor cells,” Journal of Immunology, vol. 155, no. 8, pp. 3711–3715, 1995. View at Google Scholar · View at Scopus
  33. H. A. Pickett, J. D. Henson, A. Y. M. Au, A. A. Neumann, and R. R. Reddel, “Normal mammalian cells negatively regulate telomere length by telomere trimming,” Human Molecular Genetics, vol. 20, no. 23, pp. 4684–4692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. L. A. Langford, M. A. Piatyszek, R. Xu, S. C. Schold Jr., and J. W. Shay, “Telomerase activity in human brain tumours,” The Lancet, vol. 346, no. 8985, pp. 1267–1268, 1995. View at Google Scholar · View at Scopus
  35. C. T. Jordan, M. L. Guzman, and M. Noble, “Cancer stem cells,” The New England Journal of Medicine, vol. 355, no. 12, pp. 1253–1261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. B. A. Emmenegger and R. J. Wechsler-Reya, “Stem cells and the origin and propagation of brain tumors,” Journal of Child Neurology, vol. 23, no. 10, pp. 1172–1178, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Laigle-Donadey, F. Doz, and J.-Y. Delattre, “Brainstem gliomas in children and adults,” Current Opinion in Oncology, vol. 20, no. 6, pp. 662–667, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. P. A. Leach, E. J. Estlin, D. J. Coope, J. A. Thorne, and I. D. Kamaly-Asl, “Diffuse brainstem gliomas in children: should we or shouldn't we biopsy?” British Journal of Neurosurgery, vol. 22, no. 5, pp. 619–624, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Grill, G. Bergthold, and C. Ferreira, “Pediatric ependymomas: will molecular biology change patient management?” Current Opinion in Oncology, vol. 23, no. 6, pp. 638–642, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. B. A. Kohler, E. Ward, B. J. McCarthy et al., “Annual report to the nation on the status of cancer, 1975–2007, featuring tumors of the brain and other nervous system,” Journal of the National Cancer Institute, vol. 103, no. 9, pp. 714–736, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. R. E. Bristol, “Low-grade glial tumors: are they all the same?” Seminars in Pediatric Neurology, vol. 16, no. 1, pp. 23–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Dorey and E. Amaya, “FGF signalling: diverse roles during early vertebrate embryogenesis,” Development, vol. 137, no. 22, pp. 3731–3742, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Piccolo, Y. Sasai, B. Lu, and E. M. De Robertis, “Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4,” Cell, vol. 86, no. 4, pp. 589–598, 1996. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Kerosuo and M. Bronner-Fraser, “What is bad in cancer is good in the embryo: importance of EMT in neural crest development,” Seminars in Cell and Developmental Biology, vol. 23, no. 3, pp. 320–332, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. S. A. Mani, W. Guo, M.-J. Liao et al., “The epithelial-mesenchymal transition generates cells with properties of stem cells,” Cell, vol. 133, no. 4, pp. 704–715, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. B. G. Hollier, K. Evans, and S. A. Mani, “The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies,” Journal of Mammary Gland Biology and Neoplasia, vol. 14, no. 1, pp. 29–43, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Albino, A. Brizzolara, S. Moretti et al., “Gene expression profiling identifies eleven DNA repair genes down-regulated during mouse neural crest cell migration,” International Journal of Developmental Biology, vol. 55, no. 1, pp. 65–72, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. F. Crane and P. A. Trainor, “Neural crest stem and progenitor cells,” Annual Review of Cell and Developmental Biology, vol. 22, pp. 267–286, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Axelson, “The Notch signaling cascade in neuroblastoma: role of the basic helix-loop-helix proteins HASH-1 and HES-1,” Cancer Letters, vol. 204, no. 2, pp. 171–178, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. S. A. Mohlin, C. Wigerup, and S. Påhlman, “Neuroblastoma aggressiveness in relation to sympathetic neuronal differentiation stage,” Seminars in Cancer Biology, vol. 21, no. 4, pp. 276–282, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. S. C. Noctor, V. Martinez-Cerdeño, L. Ivic, and A. R. Kriegstein, “Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases,” Nature Neuroscience, vol. 7, no. 2, pp. 136–144, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. M. R. Costa, M. Götz, and B. Berninger, “What determines neurogenic competence in glia?” Brain Research Reviews, vol. 63, no. 1-2, pp. 47–59, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Kriegstein and A. Alvarez-Buylla, “The glial nature of embryonic and adult neural stem cells,” Annual Review of Neuroscience, vol. 32, pp. 149–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Ever and N. Gaiano, “Radial 'glial' progenitors: neurogenesis and signaling,” Current Opinion in Neurobiology, vol. 15, no. 1, pp. 29–33, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. K. E. Hunter and M. E. Hatten, “Radial glial cell transformation to astrocytes is bidirectional: regulation by a diffusible factor in embryonic forebrain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 6, pp. 2061–2065, 1995. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Keilani and K. Sugaya, “Reelin induces a radial glial phenotype in human neural progenitor cells by activation of Notch-1,” BMC Developmental Biology, vol. 8, article 69, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Gaiano and G. Fishell, “The role of Notch in promoting glial and neural stem cell fates,” Annual Review of Neuroscience, vol. 25, pp. 471–490, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Pierfelice, L. Alberi, and N. Gaiano, “Notch in the vertebrate nervous system: an old dog with new tricks,” Neuron, vol. 69, no. 5, pp. 840–855, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Zhou, J. B. Atkins, S. B. Rompani et al., “The mammalian golgi regulates numb signaling in asymmetric cell division by releasing ACBD3 during mitosis,” Cell, vol. 129, no. 1, pp. 163–178, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Cayre, P. Canoll, and J. E. Goldman, “Cell migration in the normal and pathological postnatal mammalian brain,” Progress in Neurobiology, vol. 88, no. 1, pp. 41–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. J. C. Lee, M. Mayer-Proschel, and M. S. Rao, “Gliogenesis in the central nervous system,” Glia, vol. 30, no. 2, pp. 105–121, 2000. View at Google Scholar
  62. Y. Liu and M. S. Rao, “Glial progenitors in the CNS and possible lineage relationships among them,” Biology of the Cell, vol. 96, no. 4, pp. 279–290, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Kakita and J. E. Goldman, “Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations,” Neuron, vol. 23, no. 3, pp. 461–472, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Zerlin, A. Milosevic, and J. E. Goldman, “Glial progenitors of the neonatal subventricular zone differentiate asynchronously, leading to spatial dispersion of glial clones and to the persistence of immature glia in the adult mammalian CNS,” Developmental Biology, vol. 270, no. 1, pp. 200–213, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. J. M. Gensert and J. E. Goldman, “Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter,” Journal of Neurobiology, vol. 48, no. 2, pp. 75–86, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Zerlin and J. E. Goldman, “Interactions between glial progenitors and blood vessels during early postnatal corticogenesis: blood vessel contact represents an early stage of astrocyte differentiation,” Journal of Comparative Neurology, vol. 387, no. 4, pp. 537–546, 1997. View at Google Scholar
  67. T. N. Phoenix, D. S. Currle, G. Robinson, and R. J. Gilbertson, “Review: developmental origins of neural tumours: old idea, new approaches,” Neuropathology and Applied Neurobiology, vol. 38, no. 3, pp. 222–227, 2012. View at Google Scholar
  68. N. M. Walton, G. E. Snyder, D. Park, F. Kobeissy, B. Scheffler, and D. A. Steindler, “Gliotypic neural stem cells transiently adopt tumorigenic properties during normal differentiation,” Stem Cells, vol. 27, no. 2, pp. 280–289, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. B. Scheffler, N. M. Walton, D. D. Lin et al., “Phenotypic and functional characterization of adult brain neuropoiesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 26, pp. 9353–9358, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. F. Doetsch, I. Caille, D. A. Lim, J. M. Garcia-Verdugo, and A. Alvarez-Buylla, “Subventricular zone astrocytes are neural stem cells in the adult mammalian brain,” Cell, vol. 97, no. 6, pp. 703–716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Seri, D. G. Herrera, A. Gritti et al., “Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain,” Cerebral Cortex, vol. 16, supplement 1, pp. i103–i111, 2006. View at Google Scholar · View at Scopus
  72. J. Jiao and F. C. Dong, “Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals,” Stem Cells, vol. 26, no. 5, pp. 1221–1230, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. L. de Filippis and E. Binda, “Concise review: self-renewal in the central nervous system: neural stem cells from embryo to adult,” Stem Cells Translational Medicine, vol. 1, no. 4, pp. 298–308, 2012. View at Google Scholar
  74. F. T. Merkle, A. D. Tramontin, J. M. García-Verdugo, and A. Alvarez-Buylla, “Radial glia give rise to adult neural stem cells in the subventricular zone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 50, pp. 17528–17532, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. C. V. Pfenninger, T. Roschupkina, F. Hertwig et al., “CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells,” Cancer Research, vol. 67, no. 12, pp. 5727–5736, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Corbeil, A. Joester, C. A. Fargeas et al., “Expression of distinct splice variants of the stem cell marker prominin-1 (CD133) in glial cells,” Glia, vol. 57, no. 8, pp. 860–874, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. E. L. Jackson and A. Alvarez-Buylla, “Characterization of adult neural stem cells and their relation to brain tumors,” Cells Tissues Organs, vol. 188, no. 1-2, pp. 212–224, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. Q. Shen, S. K. Goderie, L. Jin et al., “Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells,” Science, vol. 304, no. 5675, pp. 1338–1340, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. A. E. Wurmser, T. D. Palmer, and F. H. Gage, “Cellular interactions in the stem cell niche,” Science, vol. 304, no. 5675, pp. 1253–1255, 2004. View at Google Scholar · View at Scopus
  80. Z. Mirzadeh, F. T. Merkle, M. Soriano-Navarro, J. M. Garcia-Verdugo, and A. Alvarez-Buylla, “Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain,” Cell Stem Cell, vol. 3, no. 3, pp. 265–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. D. A. Lim, A. D. Tramontin, J. M. Trevejo, D. G. Herrera, J. M. García-Verdugo, and A. Alvarez-Buylla, “Noggin antagonizes BMP signaling to create a niche for adult neurogenesis,” Neuron, vol. 28, no. 3, pp. 713–726, 2000. View at Publisher · View at Google Scholar · View at Scopus
  82. G. Mudò, N. Belluardo, A. Mauro, and K. Fuxe, “Acute intermittent nicotine treatment induces fibroblast growth factor-2 in the subventricular zone of the adult rat brain and enhances neuronal precursor cell proliferation,” Neuroscience, vol. 145, no. 2, pp. 470–483, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Belluardo, G. Mudo', A. Bonomo, V. Di Liberto, M. Frinchi, and K. Fuxe, “Nicotine-induced fibroblast growth factor-2 restores the age-related decline of precursor cell proliferation in the subventricular zone of rat brain,” Brain Research, vol. 1193, pp. 12–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Carlén, K. Meletis, C. Göritz et al., “Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke,” Nature Neuroscience, vol. 12, no. 3, pp. 259–267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Garzón-Muvdi and A. Quiñones-Hinojosa, “Neural stem cell niches and homing: recruitment and integration into functional tissues,” ILAR Journal, vol. 51, no. 1, pp. 3–23, 2010. View at Google Scholar · View at Scopus
  86. A. Aguirre, M. E. Rubio, and V. Gallo, “Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal,” Nature, vol. 467, no. 7313, pp. 323–327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. O. J. Becher, D. Hambardzumyan, E. I. Fomchenko et al., “Gli activity correlates with tumor grade in platelet-derived growth factor-induced gliomas,” Cancer Research, vol. 68, no. 7, pp. 2241–2249, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. E. E. Bar, A. Chaudhry, A. Lin et al., “Cyclopamine-mediated Hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma,” Stem Cells, vol. 25, no. 10, pp. 2524–2533, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. E. Angot, K. Loulier, K. T. Nguyen-Ba-Charvet, A.-P. Gadeau, M. Ruat, and E. Traiffort, “Chemoattractive activity of Sonic Hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb,” Stem Cells, vol. 26, no. 9, pp. 2311–2320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. Y.-G. Han, N. Spassky, M. Romaguera-Ros et al., “Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells,” Nature Neuroscience, vol. 11, no. 3, pp. 277–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. K. Lai, B. K. Kaspar, F. H. Gage, and D. V. Schaffer, “Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo,” Nature Neuroscience, vol. 6, no. 1, pp. 21–27, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. P. J. Horner and T. D. Palmer, “New roles for astrocytes: the nightlife of an 'astrocyte'. La vida loca!,” Trends in Neurosciences, vol. 26, no. 11, pp. 597–603, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Robel, B. Berninger, and M. Götz, “The stem cell potential of glia: lessons from reactive gliosis,” Nature Reviews Neuroscience, vol. 12, no. 2, pp. 88–104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. C. Simon, M. Götz, and L. Dimou, “Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury,” Glia, vol. 59, no. 6, pp. 869–881, 2011. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Buffo, I. Rite, P. Tripathi et al., “Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 9, pp. 3581–3586, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. M. C. Nunes, N. S. Roy, H. M. Keyoung et al., “Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain,” Nature Medicine, vol. 9, no. 4, pp. 439–447, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall, “Neuronal replacement from endogenous precursors in the adult brain after stroke,” Nature Medicine, vol. 8, no. 9, pp. 963–970, 2002. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Courtès, J. Vernerey, L. Pujadas et al., “Reelin controls progenitor cell migration in the healthy and pathological adult mouse brain,” PLoS ONE, vol. 6, no. 5, Article ID e20430, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Sun, J. Lee, and H. A. Fine, “Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury,” Journal of Clinical Investigation, vol. 113, no. 9, pp. 1364–1374, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Yang, G. D. Feng, C. Olivera, X. Y. Jiao, A. Vitale et al., “Sonic hedgehog released from scratch-injured astrocytes is a key signal necessary but not sufficient for the astrocyte de-differentiation,” Stem Cell Research, vol. 9, no. 2, pp. 156–166, 2012. View at Publisher · View at Google Scholar
  101. A. L. Vescovi, E. A. Parati, A. Gritti et al., “Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation,” Experimental Neurology, vol. 156, no. 1, pp. 71–83, 1999. View at Publisher · View at Google Scholar · View at Scopus
  102. G. Tabatabai and M. Weller, “Glioblastoma stem cells,” Cell and Tissue Research, vol. 343, no. 3, pp. 459–465, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. L. P. Deleyrolle and B. A. Reynolds, “Identifying and enumerating neural stem cells: application to aging and cancer,” Progress in Brain Research, vol. 175, pp. 43–51, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Armando, A. Lebrun, J.-P. Hugnot, C. Ripoll, M. Saunier, and L. Simonneau, “Neurosphere-derived neural cells show region-specific behaviour in vitro,” NeuroReport, vol. 18, no. 15, pp. 1539–1542, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. S. A. Louis, R. L. Rietze, L. Deleyrolle et al., “Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay,” Stem Cells, vol. 26, no. 4, pp. 988–996, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. N. D. Bull and P. F. Bartlett, “The adult mouse hippocampal progenitor is neurogenic but not a stem cell,” Journal of Neuroscience, vol. 25, no. 47, pp. 10815–10821, 2005. View at Publisher · View at Google Scholar · View at Scopus
  107. D. Beier, P. Hau, M. Proescholdt et al., “CD133+ and CD133- glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles,” Cancer Research, vol. 67, no. 9, pp. 4010–4015, 2007. View at Publisher · View at Google Scholar · View at Scopus
  108. M. Ehtesham, A. Sarangi, J. G. Valadez et al., “Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells,” Oncogene, vol. 26, no. 39, pp. 5752–5761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. J. G. Valadez, V. K. Grover, M. D. Carter et al., “Identification of Hedgehog pathway responsive glioblastomas by isocitrate dehydrogenase mutation,” Cancer Letters, vol. 328, no. 2, pp. 297–306, 2013. View at Publisher · View at Google Scholar
  110. L. Gabay, S. Lowell, L. L. Rubin, and D. J. Anderson, “Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro,” Neuron, vol. 40, no. 3, pp. 485–499, 2003. View at Publisher · View at Google Scholar · View at Scopus
  111. C. M. Morshead, P. Benveniste, N. N. Iscove, and D. Van Der Kooy, “Hematopoietic competence is a rare property of neural stem cells that may depend on genetic and epigenetic alterations,” Nature Medicine, vol. 8, no. 3, pp. 268–273, 2002. View at Publisher · View at Google Scholar · View at Scopus
  112. S.-P. Han, J.-H. Kim, M.-E. Han et al., “SNAI1 is involved in the proliferation and migration of glioblastoma cells,” Cellular and Molecular Neurobiology, vol. 31, no. 3, pp. 489–496, 2011. View at Publisher · View at Google Scholar · View at Scopus
  113. C. Foroni, R. Galli, B. Cipelletti et al., “Resilience to transformation and inherent genetic and functional stability of adult neural stem cells ex vivo,” Cancer Research, vol. 67, no. 8, pp. 3725–3733, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. D. Ferrari, E. Binda, L. de Filippis, and A. L. Vescovi, “UNIT 2D.6. Isolation of neural stem cells from neural tissues using the neurosphere technique,” in Current Protocols in Stem Cell Biology, John Wiley & Sons, Hoboken, NJ, USA, 2010. View at Publisher · View at Google Scholar
  115. A. W. Craft and L. Parker, “Poor prognosis neuroblastoma: is screening the answer?” British Journal of Cancer, vol. 66, no. 18, pp. S96–S101, 1992. View at Google Scholar · View at Scopus
  116. T. Sawada, “Past and future of neuroblastoma screening in Japan,” The American Society of Pediatric Hematology/Oncology, vol. 14, no. 4, pp. 320–326, 1992. View at Google Scholar · View at Scopus
  117. S. J. Morrison, S. E. Perez, Z. Qiao et al., “Transient notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells,” Cell, vol. 101, no. 5, pp. 499–510, 2000. View at Google Scholar · View at Scopus
  118. D. Han, J. S. Zager, G. Han et al., “The unique clinical characteristics of melanoma diagnosed in children,” Annals of Surgical Oncology, vol. 19, no. 12, pp. 3888–3895, 2012. View at Publisher · View at Google Scholar
  119. K. K. Matthay, R. E. George, and A. L. Yu, “Promising therapeutic targets in neuroblastoma,” Clinical Cancer Research, vol. 18, no. 10, pp. 2740–2753, 2012. View at Publisher · View at Google Scholar
  120. N. R. Nichols, “Ndrg2, a novel gene regulated by adrenal steroids and antidepressants, is highly expressed in astrocytes,” Annals of the New York Academy of Sciences, vol. 1007, pp. 349–356, 2003. View at Publisher · View at Google Scholar · View at Scopus
  121. R. A. Ross and B. A. Spengler, “Human neuroblastoma stem cells,” Seminars in Cancer Biology, vol. 17, no. 3, pp. 241–247, 2007. View at Publisher · View at Google Scholar · View at Scopus
  122. J. D. Walton, D. R. Kattan, S. K. Thomas et al., “Characteristics of stem cells from human neuroblastoma cell lines and in tumors,” Neoplasia, vol. 6, no. 6, pp. 838–845, 2004. View at Publisher · View at Google Scholar · View at Scopus
  123. N. J. S. Kehoe, R. P. Reid, and J. C. Semple, “Solitary benign peripheral-nerve tumours: review of 32 years'experience,” Journal of Bone and Joint Surgery B, vol. 77, no. 3, pp. 497–500, 1995. View at Google Scholar · View at Scopus
  124. D. N. Louis, H. Ohgaki, O. D. Wiestler et al., “The 2007 WHO classification of tumours of the central nervous system,” Acta Neuropathologica, vol. 114, no. 2, pp. 97–109, 2007. View at Publisher · View at Google Scholar · View at Scopus
  125. N. Sanai and M. S. Berger, “Operative techniques for gliomas and the value of extent of resection,” Neurotherapeutics, vol. 6, no. 3, pp. 478–486, 2009. View at Publisher · View at Google Scholar · View at Scopus
  126. D. A. Hardesty and N. Sanai, “The value of glioma extent of resection in the modern neurosurgical era,” Frontiers in Neurology, vol. 3, article 140, 2012. View at Google Scholar
  127. V. Barresi, F. R. Buttarelli, E. Vitarelli E, A. Arcella, M. Antonelli, and F. Giangaspero, “Caveolin-1 expression in diffuse gliomas: correlation with the proliferation index, epidermal growth factor receptor, p53, and 1p/19q status,” Human Pathology, vol. 40, no. 12, pp. 1738–1746, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. K. Watanabe, K. Sato, W. Biernat et al., “Incidence and timing of p53 mutations during astrocytoma progression in patients with multiple biopsies,” Clinical Cancer Research, vol. 3, no. 4, pp. 523–530, 1997. View at Google Scholar · View at Scopus
  129. T. D. Bourne and D. Schiff, “Update on molecular findings, management and outcome in low-grade gliomas,” Nature Reviews Neurology, vol. 6, no. 12, pp. 695–701, 2010. View at Publisher · View at Google Scholar · View at Scopus
  130. H. Ohgaki and P. Kleihues, “The definition of primary and secondary glioblastoma,” Clinical Cancer Research, vol. 19, no. 4, pp. 764–772, 2013. View at Publisher · View at Google Scholar
  131. A. Lai, S. Kharbanda, W. B. Pope et al., “Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin,” Journal of Clinical Oncology, vol. 29, no. 34, pp. 4482–4490, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. Y. Jiao, P. J. Killela, Z. J. Reitman et al., “Frequent ATRX, CIC, and FUBP1 mutations refine the classification of malignant gliomas,” Oncotarget, vol. 3, no. 7, pp. 709–722, 2012. View at Google Scholar
  133. K. E. Yen, M. A. Bittinger, S. M. Su, and V. R. Fantin, “Cancer-associated IDH mutations: biomarker and therapeutic opportunities,” Oncogene, vol. 29, no. 49, pp. 6409–6417, 2010. View at Publisher · View at Google Scholar · View at Scopus
  134. P. Kleihues and H. Ohgaki, “Primary and secondary glioblastomas: from concept to clinical diagnosis,” Neuro-Oncology, vol. 1, no. 1, pp. 44–51, 1999. View at Google Scholar · View at Scopus
  135. D. Basanta, J. G. Scott, R. Rockne, K. R. Swanson, and A. R. A. Anderson, “The role of IDH1 mutated tumour cells in secondary glioblastomas: an evolutionary game theoretical view,” Physical Biology, vol. 8, no. 1, Article ID 015016, 2011. View at Publisher · View at Google Scholar · View at Scopus
  136. S. Larjavaara, R. Mäntylä, T. Salminen et al., “Incidence of gliomas by anatomic location,” Neuro-Oncology, vol. 9, no. 3, pp. 319–325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. C. Xue, J. Wyckoff, F. Liang et al., “Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis,” Cancer Research, vol. 66, no. 1, pp. 192–197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  138. S. Giampieri, C. Manning, S. Hooper, L. Jones, C. S. Hill, and E. Sahai, “Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility,” Nature Cell Biology, vol. 11, no. 11, pp. 1287–1296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  139. S. Floor, W. C. G. Van Staveren, D. Larsimont, J. E. Dumont, and C. Maenhaut, “Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: Distinct, overlapping or same populations,” Oncogene, vol. 30, no. 46, pp. 4609–4621, 2011. View at Publisher · View at Google Scholar · View at Scopus
  140. R. I. Smee, K. Broadley, J. R. Williams, N. S. Meagher, and G. P. Bridger, “Retained role of surgery for olfactory neuroblastoma,” Head and Neck, vol. 33, no. 10, pp. 1486–1492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  141. D. Tural, O. Yildiz, F. Selcukbiricik et al., “Olfactory neuroblastomas: an experience of 24 years,” Oncology, vol. 2011, Article ID 451086, 7 pages, 2011. View at Publisher · View at Google Scholar
  142. A. M. Zanation, A. Ferlito, A. Rinaldo et al., “When, how and why to treat the neck in patients with esthesioneuroblastoma: a review,” European Archives of Oto-Rhino-Laryngology, vol. 267, no. 11, pp. 1667–1671, 2010. View at Google Scholar · View at Scopus
  143. J. Kroonen, J. Nassen, Y.-G. Boulanger et al., “Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection,” International Journal of Cancer, vol. 129, no. 3, pp. 574–585, 2011. View at Publisher · View at Google Scholar · View at Scopus
  144. M. D. Taylor, H. Poppleton, C. Fuller et al., “Radial glia cells are candidate stem cells of ependymoma,” Cancer Cell, vol. 8, no. 4, pp. 323–335, 2005. View at Publisher · View at Google Scholar · View at Scopus
  145. J. Zhang, R. Babu, R. E. McLendon, A. H. Friedman, and C. Adamson, “A comprehensive analysis of 41 patients with rosette-forming glioneuronal tumors of the fourth ventricle,” Journal of Clinical Neuroscience, vol. 20, no. 3, pp. 335–341, 2013. View at Publisher · View at Google Scholar
  146. F. J. Sim, H. M. Keyoung, J. E. Goldman et al., “Neurocytoma is a tumor of adult neuronal progenitor cells,” Journal of Neuroscience, vol. 26, no. 48, pp. 12544–12555, 2006. View at Publisher · View at Google Scholar · View at Scopus
  147. A. Bertalanffy, K. Roessler, O. Koperek, E. Gelpi, D. Prayer, and E. Knosp, “Recurrent central neurocytomas,” Cancer, vol. 104, no. 1, pp. 135–142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  148. H. W. Yang, L. G. Menon, P. M. Black, R. S. Carroll, and M. D. Johnson, “SNAI2/Slug promotes growth and invasion in human gliomas,” BMC Cancer, vol. 10, article 301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  149. J. Myung, B.-K. Cho, Y.-S. Kim, and S.-H. Park, “Snail and Cox-2 expressions are associated with WHO tumor grade and survival rate of patients with gliomas,” Neuropathology, vol. 30, no. 3, pp. 224–231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  150. M. Salvati, E. Caroli, G. Rocchi, A. Frati, C. Brogna, and E. R. Orlando, “Post-traumatic glioma. Report of four cases and review of the literature,” Tumori, vol. 90, no. 4, pp. 416–419, 2004. View at Google Scholar · View at Scopus
  151. C. Yang, R. R. Iyer, A. C. Yu et al., “beta-Catenin signaling initiates the activation of astrocytes and its dysregulation contributes to the pathogenesis of astrocytomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 18, pp. 6963–6968, 2012. View at Publisher · View at Google Scholar
  152. X. Liu, L. Wang, S. Zhao, X. Ji, Y. Luo, and F. Ling, “β-Catenin overexpression in malignant glioma and its role in proliferation and apoptosis in glioblastma cells,” Medical Oncology, vol. 28, no. 2, pp. 608–614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  153. A. Gong and S. Huang, “FoxM1 and Wnt/beta-catenin signaling in glioma stem cells,” Cancer Research, vol. 72, no. 22, pp. 5658–5662, 2012. View at Publisher · View at Google Scholar
  154. P. Pu, Z. Zhang, C. Kang et al., “Downregulation of Wnt2 and β-catenin by siRNA suppresses malignant glioma cell growth,” Cancer Gene Therapy, vol. 16, no. 4, pp. 351–361, 2009. View at Publisher · View at Google Scholar · View at Scopus
  155. C. Yang, S. Rahimpour, A. C. Yu, R. R. Lonser, and Z. Zhuang, “Regulation and dysregulation of astrocyte activation and implications in tumor formation,” Cellular and Molecular Life Sciences, vol. 70, no. 22, pp. 4201–4211, 2013. View at Publisher · View at Google Scholar
  156. M. C. Guadamillas, A. Cerezo, and M. A. del Pozo, “Overcoming anoikis—pathways to anchorageindependent growth in cancer,” Journal of Cell Science, vol. 124, no. 19, pp. 3189–3197, 2011. View at Publisher · View at Google Scholar · View at Scopus
  157. S. Belachew, R. Chittajallu, A. A. Aguirre et al., “Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons,” Journal of Cell Biology, vol. 161, no. 1, pp. 169–186, 2003. View at Publisher · View at Google Scholar · View at Scopus
  158. B. Lang, H. L. Liu, R. Liu, G. D. Feng, X. Y. Jiao, and G. Ju, “Astrocytes in injured adult rat spinal cord may acquire the potential of neural stem cells,” Neuroscience, vol. 128, no. 4, pp. 775–783, 2004. View at Publisher · View at Google Scholar · View at Scopus
  159. H. Ohgaki and P. Kleihues, “Epidemiology and etiology of gliomas,” Acta Neuropathologica, vol. 109, no. 1, pp. 93–108, 2005. View at Publisher · View at Google Scholar · View at Scopus
  160. M. P. W. A. Houben, J. W. W. Coebergh, J. M. Birch, C. C. Tijssen, C. M. Van Duijn, and R. J. Q. McNally, “Space-time clustering patterns of gliomas in the Netherlands suggest an infectious aetiology,” European Journal of Cancer, vol. 41, no. 18, pp. 2917–2923, 2005. View at Publisher · View at Google Scholar · View at Scopus
  161. G. T. R. Monteiro, R. A. Pereira, R. J. Koifman, and S. Koifman, “Head injury and brain tumours in adults: a case-control study in Rio de Janeiro, Brazil,” European Journal of Cancer, vol. 42, no. 7, pp. 917–921, 2006. View at Publisher · View at Google Scholar · View at Scopus
  162. Z.-C. Ye and H. Sontheimer, “Glioma cells release excitotoxic concentrations of glutamate,” Cancer Research, vol. 59, no. 17, pp. 4383–4391, 1999. View at Google Scholar · View at Scopus
  163. A. Rosati, S. Marconi, B. Pollo et al., “Epilepsy in glioblastoma multiforme: correlation with glutamine synthetase levels,” Journal of Neuro-Oncology, vol. 93, no. 3, pp. 319–324, 2009. View at Publisher · View at Google Scholar · View at Scopus
  164. E. Crocetti, A. Trama, C. Stiller et al., “Epidemiology of glial and non-glial brain tumours in Europe,” European Journal of Cancer, vol. 48, no. 10, pp. 1532–1542, 2012. View at Publisher · View at Google Scholar · View at Scopus