Acta Neuropathologica

, 116:465 | Cite as

The interface between glial progenitors and gliomas

Review

Abstract

The mammalian brain and spinal cord contain heterogeneous populations of cycling, immature cells. These include cells with stem cell-like properties as well as progenitors in various stages of early glial differentiation. This latter population is distributed widely throughout gray and white matter and numerically represents an extremely large cell pool. In this review, we discuss the possibility that the glial progenitors that populate the adult CNS are one source of gliomas. Indeed, the marker phenotypes, morphologies, and migratory properties of cells in gliomas strongly resemble glial progenitors in many ways. We review briefly some salient features of normal glial development and then examine the similarities and differences between normal progenitors and cells in gliomas, focusing on the phenotypic plasticity of glial progenitors and the responses to growth factors in promoting proliferation and migration of normal and glioma cells, and discussing known mutational changes in gliomas in the context of how these might affect the proliferative and migratory behaviors of progenitors. Finally, we will discuss the “cancer stem cell” hypothesis in light of the possibility that glial progenitors can generate gliomas.

Keywords

Glial development Gliomas Glial progenitors Oligodendrocytes Astrocytes Neural stem cells PDGF EGF Cell migration 

Notes

Acknowledgments

Supported in part by NIH Grants KO8-NS045070 (P.C.) and NS17125 (J.E.G.)

References

  1. 1.
    Aguirre A, Rizvi TA, Ratner N, Gallo V (2005) Overexpression of the epidermal growth factor receptor confers migratory properties to nonmigratory postnatal neural progenitors. J Neurosci 25:11092–11106. doi: 10.1523/JNEUROSCI.2981-05.2005 PubMedGoogle Scholar
  2. 2.
    Alonso G (2000) Prolonged corticosterone treatment of adult rats inhibits the proliferation of oligodendrocyte progenitors present throughout white and gray matter regions of the brain. Glia 31:219–231. doi :10.1002/1098-1136(200009)31:3<219::AID-GLIA30>3.0.CO;2-RPubMedGoogle Scholar
  3. 3.
    Assanah M, Lochhead R, Ogden A, Bruce J, Goldman J, Canoll P (2006) Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci 26:6781–6790. doi: 10.1523/JNEUROSCI.0514-06.2006 PubMedGoogle Scholar
  4. 4.
    Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ et al (2002) Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 1:269–277. doi: 10.1016/S1535-6108(02)00046-6 PubMedGoogle Scholar
  5. 5.
    Bailey P, Bucy PC (1929) Oligodendrogliomas of the brain. J Pathol Bacteriol 32:735–751. doi: 10.1002/path.1700320403 Google Scholar
  6. 6.
    Beadle C, Assanah MC, Monzo P, Vallee R, Rosenfeld SS, Canoll P (2008) The role of myosin II in glioma invasion of the brain. Mol Biol Cell 19:3357–3368. doi: 10.1091/mbc.E08-03-0319 PubMedGoogle Scholar
  7. 7.
    Berger F, Gay E, Pelletier L, Tropel P, Wion D (2004) Development of gliomas: potential role of asymmetrical cell division of neural stem cells. Lancet Oncol 5:511–514. doi: 10.1016/S1470-2045(04)01531-1 PubMedGoogle Scholar
  8. 8.
    Biernat W, Huang H, Yokoo H, Kleihues P, Ohgaki H (2004) Predominant expression of mutant EGFR (EGFRvIII) is rare in primary glioblastomas. Brain Pathol 14:131–136PubMedGoogle Scholar
  9. 9.
    Bogler O, Nagane M, Gillis J, Huang HJ, Cavenee WK (1999) Malignant transformation of p53-deficient astrocytes is modulated by environmental cues in vitro. Cell Growth Differ 10:73–86PubMedGoogle Scholar
  10. 10.
    Bogler O, Wren D, Barnett SC, Land H, Noble M (1990) Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci USA 87:6368–6372. doi: 10.1073/pnas.87.16.6368 PubMedGoogle Scholar
  11. 11.
    Borit A, McIntosh GC (1981) Myelin basic protein and glial fibrillary acidic protein in human fetal brain. Neuropathol Appl Neurobiol 7:279–287. doi: 10.1111/j.1365-2990.1981.tb00099.x PubMedGoogle Scholar
  12. 12.
    Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M (2005) Synantocytes: the fifth element. J Anat 207:695–706. doi: 10.1111/j.1469-7580.2005.00458.x PubMedGoogle Scholar
  13. 13.
    Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B et al (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11:69–82. doi: 10.1016/j.ccr.2006.11.020 PubMedGoogle Scholar
  14. 14.
    Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C et al (1998) Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20:869–882. doi: 10.1016/S0896-6273(00)80469-9 PubMedGoogle Scholar
  15. 15.
    Choi BH (1986) Glial fibrillary acidic protein in radial glia of early human fetal cerebrum: a light and electron microscopic immunoperoxidase study. J Neuropathol Exp Neurol 45:408–418. doi: 10.1097/00005072-198607000-00003 PubMedGoogle Scholar
  16. 16.
    Colin C, Baeza N, Tong S, Bouvier C, Quilichini B, Durbec P et al (2006) In vitro identification and functional characterization of glial precursor cells in human gliomas. Neuropathol Appl Neurobiol 32:189–202. doi: 10.1111/j.1365-2990.2006.00740.x PubMedGoogle Scholar
  17. 17.
    Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC (2001) PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 15:1913–1925. doi: 10.1101/gad.903001 PubMedGoogle Scholar
  18. 18.
    Dirks PB (2006) Cancer: stem cells and brain tumours. Nature 444:687–688. doi: 10.1038/444687a PubMedGoogle Scholar
  19. 19.
    Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127–1134. doi: 10.1038/nn1144 PubMedGoogle Scholar
  20. 20.
    Edgar MA, Rosenblum MK (2007) Mixed glioneuronal tumors: recently described entities. Arch Pathol Lab Med 131:228–233PubMedGoogle Scholar
  21. 21.
    Evans RJ, Wyllie FS, Wynford-Thomas D, Kipling D, Jones CJ (2003) A p53-dependent, telomere-independent proliferative life span barrier in astrocytes consistent with the molecular genetics of glioma development. Cancer Res 63:4854–4861PubMedGoogle Scholar
  22. 22.
    Farin A, Suzuki SO, Weiker M, Goldman JE, Bruce JN, Canoll P (2006) Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 53:799–808. doi: 10.1002/glia.20334 PubMedGoogle Scholar
  23. 23.
    Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A et al (2007) Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21:2683–2710. doi: 10.1101/gad.1596707 PubMedGoogle Scholar
  24. 24.
    Furuta A, Rothstein JD, Martin LJ (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363–8375PubMedGoogle Scholar
  25. 25.
    Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S et al (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021. doi: 10.1158/0008-5472.CAN-04-1364 PubMedGoogle Scholar
  26. 26.
    Gensert JM, Goldman JE (1996) In vivo characterization of endogenous proliferating cells in adult rat subcortical white matter. Glia 17:39–51. doi :10.1002/(SICI)1098-1136(199605)17:1<39::AID-GLIA4>3.0.CO;2-2PubMedGoogle Scholar
  27. 27.
    Gensert JM, Goldman JE (1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19:197–203. doi: 10.1016/S0896-6273(00)80359-1 PubMedGoogle Scholar
  28. 28.
    Gensert JM, Goldman JE (2001) Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. J Neurobiol 48:75–86. doi: 10.1002/neu.1043 PubMedGoogle Scholar
  29. 29.
    Gil-Perotin S, Marin-Husstege M, Li J, Soriano-Navarro M, Zindy F, Roussel MF et al (2006) Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J Neurosci 26:1107–1116. doi: 10.1523/JNEUROSCI.3970-05.2006 PubMedGoogle Scholar
  30. 30.
    Goldman JE (2005) Lineages of astrocytes and oligodendrocytes. In: Kettenmann H, Ransom BR (eds) Neuroglia, 2nd edn. Oxford University Press, New York, pp 72–84Google Scholar
  31. 31.
    Guillemot F (2007) Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83:37–52. doi: 10.1016/j.pneurobio.2007.02.009 PubMedGoogle Scholar
  32. 32.
    Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin CH, Westermark B et al (1992) Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52:3213–3219PubMedGoogle Scholar
  33. 33.
    Hermanson M, Funa K, Koopmann J, Maintz D, Waha A, Westermark B et al (1996) Association of loss of heterozygosity on chromosome 17p with high platelet-derived growth factor alpha receptor expression in human malignant gliomas. Cancer Res 56:164–171PubMedGoogle Scholar
  34. 34.
    Hesselager G, Uhrbom L, Westermark B, Nister M (2003) Complementary effects of platelet-derived growth factor autocrine stimulation and p53 or Ink4a-Arf deletion in a mouse glioma model. Cancer Res 63:4305–4309PubMedGoogle Scholar
  35. 35.
    Horky LL, Galimi F, Gage FH, Horner PJ (2006) Fate of endogenous stem/progenitor cells following spinal cord injury. J Comp Neurol 498:525–538. doi: 10.1002/cne.21065 PubMedGoogle Scholar
  36. 36.
    Huff KR, Schreier W (1990) Fibroblast growth factor inhibits epidermal growth factor-induced responses in rat astrocytes. Glia 3:193–204. doi: 10.1002/glia.440030306 PubMedGoogle Scholar
  37. 37.
    Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA (2002) Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39:193–206. doi: 10.1002/glia.10094 PubMedGoogle Scholar
  38. 38.
    Imamoto K, Paterson JA, Leblond CP (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. I. Sequential changes in oligodendrocytes. J Comp Neurol 180:115–128. doi: 10.1002/cne.901800108 PubMedGoogle Scholar
  39. 39.
    Ivkovic S, Canoll P, Goldman JE (2008) Constitutive EGFR signaling in oligodendrocyte progenitors leads to diffuse hyperplasia in postnatal white matter. J Neurosci 28:914–922. doi: 10.1523/JNEUROSCI.4327-07.2008 PubMedGoogle Scholar
  40. 40.
    Kakita A, Goldman JE (1999) Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron 23:461–472. doi: 10.1016/S0896-6273(00)80800-4 PubMedGoogle Scholar
  41. 41.
    Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD (2006) Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173–179. doi: 10.1038/nn1620 PubMedGoogle Scholar
  42. 42.
    Koguchi K, Nakatsuji Y, Nakayama K, Sakoda S (2002) Modulation of astrocyte proliferation by cyclin-dependent kinase inhibitor p27(Kip1). Glia 37:93–104. doi: 10.1002/glia.10017 PubMedGoogle Scholar
  43. 43.
    Kondo T, Raff M (2000) Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754–1757. doi: 10.1126/science.289.5485.1754 PubMedGoogle Scholar
  44. 44.
    Kwon CH, Zhao D, Chen J, Alcantara S, Li Y, Burns DK et al (2008) Pten haploinsufficiency accelerates formation of high-grade astrocytomas. Cancer Res 68:3286–3294. doi: 10.1158/0008-5472.CAN-07-6867 PubMedGoogle Scholar
  45. 45.
    Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815–840. doi: 10.1002/cne.901930316 PubMedGoogle Scholar
  46. 46.
    Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL et al (2004) The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63:499–509PubMedGoogle Scholar
  47. 47.
    Lillien LE, Raff MC (1990) Differentiation signals in the CNS: type-2 astrocyte development in vitro as a model system. Neuron 5:111–119. doi: 10.1016/0896-6273(90)90301-U PubMedGoogle Scholar
  48. 48.
    Lin G, Goldman JE (2008) An FGF-responsive astrocyte precursor isolated from the neonatal forebrain. Glia (in press)Google Scholar
  49. 49.
    Liu Y, Han SS, Wu Y, Tuohy TM, Xue H, Cai J et al (2004) CD44 expression identifies astrocyte-restricted precursor cells. Dev Biol 276(1):31–46. doi: 10.1016/j.ydbio.2004.08.018 PubMedGoogle Scholar
  50. 50.
    Liu Y, Rao MS (2004) Glial progenitors in the CNS and possible lineage relationships among them. Biol Cell 96:279–290. doi: 10.1016/j.biolcel.2004.02.001 PubMedGoogle Scholar
  51. 51.
    Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109. doi: 10.1007/s00401-007-0243-4 PubMedGoogle Scholar
  52. 52.
    Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD et al (2002) Common developmental requirement for olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75–86. doi: 10.1016/S0092-8674(02)00678-5 PubMedGoogle Scholar
  53. 53.
    Lund-Johansen M, Bjerkvig R, Humphrey PA, Bigner SH, Bigner DD, Laerum OD (1990) Effect of epidermal growth factor on glioma cell growth, migration, and invasion in vitro. Cancer Res 50:6039–6044PubMedGoogle Scholar
  54. 54.
    Lund-Johansen M, Forsberg K, Bjerkvig R, Laerum OD (1992) Effects of growth factors on a human glioma cell line during invasion into rat brain aggregates in culture. Acta Neuropathol 84:190–197. doi: 10.1007/BF00311394 PubMedGoogle Scholar
  55. 55.
    Maehama T, Dixon JE (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3, 4, 5-trisphosphate. J Biol Chem 273:13375–13378. doi: 10.1074/jbc.273.22.13375 PubMedGoogle Scholar
  56. 56.
    Mao X, Barfoot R, Hamoudi RA, Noble M (1998) Alleletyping of an oligodendrocyte-type-2 astrocyte lineage derive from a human glioblastoma multiforme. J Neurooncol 40:243–250. doi: 10.1023/A:1006158010388 PubMedGoogle Scholar
  57. 57.
    Marshall CA, Goldman JE (2002) Subpallial dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter. J Neurosci 22:9821–9830PubMedGoogle Scholar
  58. 58.
    Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, Furusho M et al (2006) Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 293:358–369. doi: 10.1016/j.ydbio.2006.02.029 PubMedGoogle Scholar
  59. 59.
    Mason JL, Goldman JE (2002) A2B5+ and O4+ cycling progenitors in the adult forebrain white matter respond differentially to PDGF-AA, FGF-2, and IGF-1. Mol Cell Neurosci 20:30–42. doi: 10.1006/mcne.2002.1114 PubMedGoogle Scholar
  60. 60.
    McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA (1990) FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5:603–614. doi: 10.1016/0896-6273(90)90215-2 PubMedGoogle Scholar
  61. 61.
    McKinnon RD, Waldron S, Kiel ME (2005) PDGF alpha-receptor signal strength controls an RTK rheostat that integrates phosphoinositol 3’-kinase and phospholipase Cgamma pathways during oligodendrocyte maturation. J Neurosci 25:3499–3508. doi: 10.1523/JNEUROSCI.5049-04.2005 PubMedGoogle Scholar
  62. 62.
    Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ et al (2005) Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012–2024. doi: 10.1056/NEJMoa051918 PubMedGoogle Scholar
  63. 63.
    Mi H, Barres BA (1999) Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 19:1049–1061PubMedGoogle Scholar
  64. 64.
    Mi H, Haeberle H, Barres BA (2001) Induction of astrocyte differentiation by endothelial cells. J Neurosci 21:1538–1547PubMedGoogle Scholar
  65. 65.
    Nakatsuji Y, Miller RH (2001) Density dependent modulation of cell cycle protein expression in astrocytes. J Neurosci Res 66:487–496. doi: 10.1002/jnr.1240 PubMedGoogle Scholar
  66. 66.
    Nicolay DJ, Doucette JR, Nazarali AJ (2007) Transcriptional control of oligodendrogenesis. Glia 55:1287–1299. doi: 10.1002/glia.20540 PubMedGoogle Scholar
  67. 67.
    Nishiyama A (2007) Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13:62–76. doi: 10.1177/1073858406295586 PubMedGoogle Scholar
  68. 68.
    Noble M, Mayer-Proschel M (1997) Growth factors, glia and gliomas. J Neurooncol 35:193–209. doi: 10.1023/A:1005898228116 PubMedGoogle Scholar
  69. 69.
    Noble M, Pröschel C, Mayer-Pröschel M (2004) Getting a GR(i)P on oligodendrocyte development. Dev Biol 265:33–52. doi: 10.1016/j.ydbio.2003.06.002 PubMedGoogle Scholar
  70. 70.
    Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G 2nd, Jiang L et al (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439–447. doi: 10.1038/nm837 PubMedGoogle Scholar
  71. 71.
    Ogden AT, Waziri AE, Lochhead RA, Fusco D, Lopez K, Ellis JA et al (2008) Identification of A2B5 + CD133- tumor-initiating cells in adult human gliomas. Neurosurg 62:505–514. doi: 10.1227/01.neu.0000316019.28421.95 Google Scholar
  72. 72.
    Ohgaki H, Kleihues P (2005) Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 64:479–489PubMedGoogle Scholar
  73. 73.
    Ohgaki H, Kleihues P (2007) Genetic pathways to primary and secondary glioblastoma. Am J Pathol 170:1445–1453. doi: 10.2353/ajpath.2007.070011 PubMedGoogle Scholar
  74. 74.
    Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494. doi :10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3PubMedGoogle Scholar
  75. 75.
    Paterson JA, Privat A, Ling EA, Leblond CP (1973) Investigation of glial cells in semithin sections. 3. Transformation of subependymal cells into glial cells, as shown by radioautography after 3 H-thymidine injection into the lateral ventricle of the brain of young rats. J Comp Neurol 149:83–102. doi: 10.1002/cne.901490106 PubMedGoogle Scholar
  76. 76.
    Paukert M, Bergles DE (2006) Synaptic communication between neurons and NG2+ cells. Curr Opin Neurobiol 16:515–521. doi: 10.1016/j.conb.2006.08.009 PubMedGoogle Scholar
  77. 77.
    Polito A, Reynolds R (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707–716. doi: 10.1111/j.1469-7580.2005.00454.x PubMedGoogle Scholar
  78. 78.
    Pollack IF, Randall MS, Kristofik MP, Kelly RH, Selker RG, Vertosick FT Jr (1991) Response of low-passage human malignant gliomas in vitro to stimulation and selective inhibition of growth factor-mediated pathways. J Neurosurg 75:284–293PubMedCrossRefGoogle Scholar
  79. 79.
    Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303:390–396. doi: 10.1038/303390a0 PubMedGoogle Scholar
  80. 80.
    Rebetz J, Tian D, Persson A, Widegren B, Salford LG, Englund E, Gisselsson D, Fan X (2008) Glial progenitor-like phenotype in low-grade glioma and enhanced CD133-expression and neuronal lineage differentiation potential in high-grade glioma. PLoS ONE 3:e1936PubMedGoogle Scholar
  81. 81.
    Rousselot P, Lois C, Alvarez-Buylla A (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 351:51–61. doi: 10.1002/cne.903510106 PubMedGoogle Scholar
  82. 82.
    Sanai N, Alvarez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353:811–822. doi: 10.1056/NEJMra043666 PubMedGoogle Scholar
  83. 83.
    Sarkaria JN, Yang L, Grogan PT, Kitange GJ, Carlson BL, Schroeder MA et al (2007) Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol Cancer Ther 6:1167–1174. doi: 10.1158/1535-7163.MCT-06-0691 PubMedGoogle Scholar
  84. 84.
    Schnitzer J, Schachner M (1982) Cell type specificity of a neural cell surface antigen recognized by the monoclonal antibody A2B5. Cell Tissue Res 224:625–636. doi: 10.1007/BF00213757 PubMedGoogle Scholar
  85. 85.
    Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N et al (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340. doi: 10.1126/science.1095505 PubMedGoogle Scholar
  86. 86.
    Shih AH, Dai C, Hu X, Rosenblum MK, Koutcher JA, Holland EC (2004) Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis. Cancer Res 64:4783–4789. doi: 10.1158/0008-5472.CAN-03-3831 PubMedGoogle Scholar
  87. 87.
    Shoshan Y, Nishiyama A, Chang A, Mork S, Barnett GH, Cowell JK et al (1999) Expression of oligodendrocyte progenitor cell antigens by gliomas: implications for the histogenesis of brain tumors. Proc Natl Acad Sci USA 96:10361–10366. doi: 10.1073/pnas.96.18.10361 PubMedGoogle Scholar
  88. 88.
    Simpson PB, Armstrong RC (1999) Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration. Glia 26:22–35. doi :10.1002/(SICI)1098-1136(199903)26:1<22::AID-GLIA3>3.0.CO;2-MPubMedGoogle Scholar
  89. 89.
    Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401. doi: 10.1038/nature03128 PubMedGoogle Scholar
  90. 90.
    Stambolic V, Suzuki A, De la Pompa JL, Brothers GM, Mirtsos C, Sasaki T et al (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95:29–39. doi: 10.1016/S0092-8674(00)81780-8 PubMedGoogle Scholar
  91. 91.
    Staugaitis SM, Zerlin M, Hawkes R, Levine JM, Goldman JE (2001) Aldolase C/zebrin II expression in the neonatal rat forebrain reveals cellular heterogeneity within the subventricular zone and early astrocyte differentiation. J Neurosci 21:6195–6205PubMedGoogle Scholar
  92. 92.
    Suzuki SO, Kitai R, Llena J, Lee SC, Goldman JE, Shafit-Zagardo B (2002) MAP-2e, a novel MAP-2 isoform, is expressed in gliomas and delineates tumor architecture and patterns of infiltration. J Neuropathol Exp Neurol 61:403–412PubMedGoogle Scholar
  93. 93.
    Suzuki SO, Goldman JE (2003) Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J Neurosci 23:4240–4250PubMedGoogle Scholar
  94. 94.
    Takahashi Y, Morales FC, Kreimann EL, Georgescu MM (2006) PTEN tumor suppressor associates with NHERF proteins to attenuate PDGF receptor signaling. EMBO J 25:910–920. doi: 10.1038/sj.emboj.7600979 PubMedGoogle Scholar
  95. 95.
    Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M et al (2000) 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 99:143–148. doi: 10.1016/S0925-4773(00)00466-4 PubMedGoogle Scholar
  96. 96.
    Uhrbom L, Hesselager G, Nister M, Westermark B (1998) Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res 58:5275–5279PubMedGoogle Scholar
  97. 97.
    van der Valk P, Lindeman J, Kamphorst W (1997) Growth factor profiles of human gliomas. Do non-tumour cells contribute to tumour growth in glioma? Ann Oncol 8:1023–1029. doi: 10.1023/A:1008265905505 PubMedGoogle Scholar
  98. 98.
    van Heyningen P, Calver AR, Richardson WD (2001) Control of progenitor cell number by mitogen supply and demand. Curr Biol 11:232–241. doi: 10.1016/S0960-9822(01)00075-6 PubMedGoogle Scholar
  99. 99.
    Vergeli M, Mazzanti B, Ballerini C, Gran B, Amaducci L, Massacesi L (1995) Transforming growth factor-beta 1 inhibits the proliferation of rat astrocytes induced by serum and growth factors. J Neurosci Res 40:127–133. doi: 10.1002/jnr.490400114 PubMedGoogle Scholar
  100. 100.
    Wegner M (2008) A matter of identity: transcriptional control in oligodendrocytes. J Mol Neurosci 35:3–12. doi: 10.1007/s12031-007-9008-8 PubMedGoogle Scholar
  101. 101.
    Wei Q, Clarke L, Scheidenhelm DK, Qian B, Tong A, Sabha N et al (2006) High-grade glioma formation results from postnatal pten loss or mutant epidermal growth factor receptor expression in a transgenic mouse glioma model. Cancer Res 66:7429–7437. doi: 10.1158/0008-5472.CAN-06-0712 PubMedGoogle Scholar
  102. 102.
    Wolswijk G, Noble M (1992) Cooperation between PDGF and FGF converts slowly dividing O-2Aadult progenitor cells to rapidly dividing cells with characteristics of O-2A perinatal progenitor cells. J Cell Biol 118:889–900. doi: 10.1083/jcb.118.4.889 PubMedGoogle Scholar
  103. 103.
    Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ (2004) Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 25:252–262. doi: 10.1016/j.mcn.2003.10.014 PubMedGoogle Scholar
  104. 104.
    Wu S, Wu Y, Capecchi MR (2006) Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 133:581–590. doi: 10.1242/dev.02236 PubMedGoogle Scholar
  105. 105.
    Xiao A, Yin C, Yang C, Di Cristofano A, Pandolfi PP, Van Dyke T (2005) Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res 65:5172–5180. doi: 10.1158/0008-5472.CAN-04-3902 PubMedGoogle Scholar
  106. 106.
    Zerlin M, Levison SW, Goldman JE (1995) Early patterns of migration, morphogenesis, and intermediate filament expression of subventricular zone cells in the postnatal rat forebrain. J Neurosci 15:7238–7249PubMedGoogle Scholar
  107. 107.
    Zerlin M, Milosevic A, Goldman JE (2004) 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. Dev Biol 270:200–213. doi: 10.1016/j.ydbio.2004.02.024 PubMedGoogle Scholar
  108. 108.
    Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61–73. doi: 10.1016/S0092-8674(02)00677-3 PubMedGoogle Scholar
  109. 109.
    Zhou Q, Choi G, Anderson DJ (2001) The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31:791–807. doi: 10.1016/S0896-6273(01)00414-7 PubMedGoogle Scholar
  110. 110.
    Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145–157. doi: 10.1242/dev.004895 PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Pathology, Division of NeuropathologyColumbia UniversityNew YorkUSA

Personalised recommendations