Abstract
The process of cortical expansion in the central nervous system is a key step of mammalian brain development to ensure its physiological function. Radial glial (RG) cells are a glial cell type contributing to this progress as intermediate neural progenitor cells responsible for an increase in the number of cortical neurons. In this review, we discuss the current understanding of RG cells during neurogenesis and provide further information on the mechanisms of neurodevelopmental diseases and stem cell-related brain tumorigenesis. Knowledge of neuronal stem cell and relative diseases will bridge benchmark research through translational studies to clinical therapeutic treatments of these diseases.
Keywords: radial glial cell, neuronal stem cell, tumorigenesis, glioma
Contributor Information
Qian Wu, Email: qianwu@moon.ibp.ac.cn.
Xiaoqun Wang, Email: xiaoqunwang@ibp.ac.cn.
References
- Alkuraya F.S., Cai X., Emery C., Mochida G.H., Al-Dosari M.S., Felie J.M., Hill R.S., Barry B.J., Partlow J.N., Gascon G.G., et al. Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected] Am J Hum Genet. 2011;88:536–547. doi: 10.1016/j.ajhg.2011.04.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J Neurosci. 2002;22:629–634. doi: 10.1523/JNEUROSCI.22-03-00629.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alvarez-Buylla A., Kirn J.R., Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science. 1990;249:1444–1446. doi: 10.1126/science.1698312. [DOI] [PubMed] [Google Scholar]
- Anderson S.A., Eisenstat D.D., Shi L., Rubenstein J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 1997;278:474–476. doi: 10.1126/science.278.5337.474. [DOI] [PubMed] [Google Scholar]
- Assanah M., Lochhead R., Ogden A., Bruce J., Goldman J., Canoll P. Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci. 2006;26:6781–6790. doi: 10.1523/JNEUROSCI.0514-06.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bachoo R.M., Maher E.A., Ligon K.L., Sharpless N.E., Chan S.S., You M.J., Tang Y., DeFrances J., Stover E., Weissleder R., et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell. 2002;1:269–277. doi: 10.1016/s1535-6108(02)00046-6. [DOI] [PubMed] [Google Scholar]
- Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760. doi: 10.1038/nature05236. [DOI] [PubMed] [Google Scholar]
- Bao S., Wu Q., Sathornsumetee S., Hao Y., Li Z., Hjelmeland A.B., Shi Q., McLendon R.E., Bigner D.D., Rich J.N. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006;66:7843–7848. doi: 10.1158/0008-5472.CAN-06-1010. [DOI] [PubMed] [Google Scholar]
- Barrera J.A., Kao L.R., Hammer R.E., Seemann J., Fuchs J.L., Megraw T.L. CDK5RAP2 regulates centriole engagement and cohesion in mice. Dev Cell. 2010;18:913–926. doi: 10.1016/j.devcel.2010.05.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bauman M.L. Neuroembryology-clinical aspects. Semin Perinatol. 1987;11:74–84. [PubMed] [Google Scholar]
- Ben-Porath I., Thomson M.W., Carey V.J., Ge R., Bell G.W., Regev A., Weinberg R.A. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40:499–507. doi: 10.1038/ng.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benedito R., Duarte A. Expression of Dll4 during mouse embryogenesis suggests multiple developmental roles. Gene Expr Patterns. 2005;5:750–755. doi: 10.1016/j.modgep.2005.04.004. [DOI] [PubMed] [Google Scholar]
- Birnbaum T., Roider J., Schankin C.J., Padovan C.S., Schichor C., Goldbrunner R., Straube A. Malignant gliomas actively recruit bone marrow stromal cells by secreting angiogenic cytokines. J Neurooncol. 2007;83:241–247. doi: 10.1007/s11060-007-9332-4. [DOI] [PubMed] [Google Scholar]
- Bond J., Roberts E., Springell K., Lizarraga S.B., Scott S., Higgins J., Hampshire D.J., Morrison E.E., Leal G.F., Silva E.O., et al. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet. 2005;37:353–355. doi: 10.1038/ng1539. [DOI] [PubMed] [Google Scholar]
- Buchman J.J., Tseng H.C., Zhou Y., Frank C.L., Xie Z., Tsai L.H. Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron. 2010;66:386–402. doi: 10.1016/j.neuron.2010.03.036. [DOI] [PubMed] [Google Scholar]
- Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., Oh E.Y., Gaber M.W., Finklestein D., Allen M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69–82. doi: 10.1016/j.ccr.2006.11.020. [DOI] [PubMed] [Google Scholar]
- Chen R., Nishimura M.C., Bumbaca S.M., Kharbanda S., Forrest W.F., Kasman I.M., Greve J.M., Soriano R.H., Gilmour L.L., Rivers C.S., et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell. 2010;17:362–375. doi: 10.1016/j.ccr.2009.12.049. [DOI] [PubMed] [Google Scholar]
- Cheng L., Wu Q., Huang Z., Guryanova O.A., Huang Q., Shou W., Rich J.N., Bao S. L1CAM regulates DNA damage checkpoint response of glioblastoma stem cells through NBS1. EMBO J. 2011;30:800–813. doi: 10.1038/emboj.2011.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Choi Y.K., Liu P., Sze S.K., Dai C., Qi R.Z. CDK5RAP2 stimulates microtubule nucleation by the gammatubulin ring complex. J Cell Biol. 2010;191:1089–1095. doi: 10.1083/jcb.201007030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper J.A. A mechanism for inside-out lamination in the neocortex. Trends Neurosci. 2008;31:113–119. doi: 10.1016/j.tins.2007.12.003. [DOI] [PubMed] [Google Scholar]
- Corbin J.G., Gaiano N., Juliano S.L., Poluch S., Stancik E., Haydar T.F. Regulation of neural progenitor cell development in the nervous system. J Neurochem. 2008;106:2272–2287. doi: 10.1111/j.1471-4159.2008.05522.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dai C., Celestino J.C., Okada Y., Louis D.N., Fuller G.N., Holland E.C. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 2001;15:1913–1925. doi: 10.1101/gad.903001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dobyns W.B. Developmental aspects of lissencephaly and the lissencephaly syndromes. Birth Defects Orig Artic Ser. 1987;23:225–241. [PubMed] [Google Scholar]
- Elias L.A.B., Wang D.D., Kriegstein A.R. Gap junction adhesion is necessary for radial migration in the neocortex. Nature. 2007;448:901–907. doi: 10.1038/nature06063. [DOI] [PubMed] [Google Scholar]
- Eyler C.E., Foo W.C., LaFiura K.M., McLendon R.E., Hjelmeland A.B., Rich J.N. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells. 2008;26:3027–3036. doi: 10.1634/stemcells.2007-1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Facchino S., Abdouh M., Chatoo W., Bernier G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci. 2010;30:10096–10111. doi: 10.1523/JNEUROSCI.1634-10.2010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fan X., Khaki L., Zhu T.S., Soules M.E., Talsma C.E., Gul N., Koh C., Zhang J., Li Y.M., Maciaczyk J., et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells. 2010;28:5–16. doi: 10.1002/stem.254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581–611. doi: 10.1210/er.2003-0027. [DOI] [PubMed] [Google Scholar]
- Gal J.S., Morozov Y.M., Ayoub A.E., Chatterjee M., Rakic P., Haydar T.F. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci. 2006;26:1045–1056. doi: 10.1523/JNEUROSCI.4499-05.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghannad M. The essential role of NDE1 in extreme microcephaly. Clin Genet. 2011;80:241–242. doi: 10.1111/j.1399-0004.2011.01753.x. [DOI] [PubMed] [Google Scholar]
- Glass R., Synowitz M., Kronenberg G., Walzlein J.H., Markovic D.S., Wang L.P., Gast D., Kiwit J., Kempermann G., Kettenmann H. Glioblastoma-induced attraction of endogenous neural precursor cells is associated with improved survival. J Neurosci. 2005;25:2637–2646. doi: 10.1523/JNEUROSCI.5118-04.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gordon W.R., Arnett K.L., Blacklow S.C. The molecular logic of Notch signaling-a structural and biochemical perspective. J Cell Sci. 2008;121:3109–3119. doi: 10.1242/jcs.035683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray G.E., Sanes J.R. Lineage of radial glia in the chicken optic tectum. Development. 1992;114:271–283. doi: 10.1242/dev.114.1.271. [DOI] [PubMed] [Google Scholar]
- Griffero F., Daga A., Marubbi D., Capra M.C., Melotti A., Pattarozzi A., Gatti M., Bajetto A., Porcile C., Barbieri F., et al. Different response of human glioma tumor-initiating cells to epidermal growth factor receptor kinase inhibitors. J Biol Chem. 2009;284:7138–7148. doi: 10.1074/jbc.M807111200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halliday A.L., Cepko C.L. Generation and migration of cells in the developing striatum. Neuron. 1992;9:15–26. doi: 10.1016/0896-6273(92)90216-z. [DOI] [PubMed] [Google Scholar]
- Haubensak W., Attardo A., Denk W., Huttner W.B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A. 2004;101:3196–3201. doi: 10.1073/pnas.0308600100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hegi M.E., Diserens A.C., Gorlia T., Hamou M.F., de Tribolet N., Weller M., Kros J.M., Hainfellner J.A., Mason W., Mariani L., et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997–1003. doi: 10.1056/NEJMoa043331. [DOI] [PubMed] [Google Scholar]
- Higgins J., Midgley C., Bergh A.M., Bell S.M., Askham J.M., Roberts E., Binns R.K., Sharif S.M., Bennett C., Glover D.M., et al. Human ASPM participates in spindle organisation, spindle orientation and cytokinesis. BMC Cell Biol. 2010;11:85. doi: 10.1186/1471-2121-11-85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holmberg J., He X., Peredo I., Orrego A., Hesselager G., Ericsson C., Hovatta O., Oba-Shinjo S.M., Marie S.K., Nistér M., et al. Activation of neural and pluripotent stem cell signatures correlates with increased malignancy in human glioma. PLoS One. 2011;6:e18454. doi: 10.1371/journal.pone.0018454. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hopewell J.W. The subependymal plate and the genesis of gliomas. J Pathol. 1975;117:101–103. doi: 10.1002/path.1711170208. [DOI] [PubMed] [Google Scholar]
- Ignatova T.N., Kukekov V.G., Laywell E.D., Suslov O.N., Vrionis F.D., Steindler D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia. 2002;39:193–206. doi: 10.1002/glia.10094. [DOI] [PubMed] [Google Scholar]
- Jackson A.P., Eastwood H., Bell S.M., Adu J., Toomes C., Carr I.M., Roberts E., Hampshire D.J., Crow Y.J., Mighell A.J., et al. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am J Hum Genet. 2002;71:136–142. doi: 10.1086/341283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson A.P., McHale D.P., Campbell D.A., Jafri H., Rashid Y., Mannan J., Karbani G., Corry P., Levene M.I., Mueller R.F., et al. Primary autosomal recessive microcephaly (MCPH1) maps to chromosome 8p22-pter. Am J Hum Genet. 1998;63:541–546. doi: 10.1086/301966. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaindl A.M., Passemard S., Kumar P., Kraemer N., Issa L., Zwirner A., Gerard B., Verloes A., Mani S., Gressens P. Many roads lead to primary autosomal recessive microcephaly. Prog Neurobiol. 2010;90:363–383. doi: 10.1016/j.pneurobio.2009.11.002. [DOI] [PubMed] [Google Scholar]
- Kornblum H.I., Hussain R., Wiesen J., Miettinen P., Zurcher S.D., Chow K., Derynck R., Werb Z. Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res. 1998;53:697–717. doi: 10.1002/(SICI)1097-4547(19980915)53:6<697::AID-JNR8>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]
- Kouprina N., Pavlicek A., Collins N.K., Nakano M., Noskov V.N., Ohzeki J., Mochida G.H., Risinger J.I., Goldsmith P., Gunsior M., et al. The microcephaly ASPM gene is expressed in proliferating tissues and encodes for a mitotic spindle protein. Hum Mol Genet. 2005;14:2155–2165. doi: 10.1093/hmg/ddi220. [DOI] [PubMed] [Google Scholar]
- Kovall R.A. More complicated than it looks: assembly of Notch pathway transcription complexes. Oncogene. 2008;27:5099–5109. doi: 10.1038/onc.2008.223. [DOI] [PubMed] [Google Scholar]
- Kriegstein A., Noctor S., Martínez-Cerdeño V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci. 2006;7:883–890. doi: 10.1038/nrn2008. [DOI] [PubMed] [Google Scholar]
- Kriegstein A.R., Götz M. Radial glia diversity: a matter of cell fate. Glia. 2003;43:37–43. doi: 10.1002/glia.10250. [DOI] [PubMed] [Google Scholar]
- Kumar A., Girimaji S.C., Duvvari M.R., Blanton S.H. Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly. Am J Hum Genet. 2009;84:286–290. doi: 10.1016/j.ajhg.2009.01.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lendahl U., Zimmerman L.B., McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell. 1990;60:585–595. doi: 10.1016/0092-8674(90)90662-x. [DOI] [PubMed] [Google Scholar]
- Levitt P., Rakic P. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol. 1980;193:815–840. doi: 10.1002/cne.901930316. [DOI] [PubMed] [Google Scholar]
- Lin J., Zhang X.M., Yang J.C., Ye Y.B., Luo S.Q. g-secretase inhibitor-I enhances radiosensitivity of glioblastoma cell lines by depleting CD133+ tumor cells. Arch Med Res. 2010;41:519–529. doi: 10.1016/j.arcmed.2010.10.006. [DOI] [PubMed] [Google Scholar]
- Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., Lu L., Irvin D., Black K.L., Yu J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67. doi: 10.1186/1476-4598-5-67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LoTurco J.J., Blanton M.G., Kriegstein A.R. Initial expression and endogenous activation of NMDA channels in early neocortical development. J Neurosci. 1991;11:792–799. doi: 10.1523/JNEUROSCI.11-03-00792.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luskin M.B., Parnavelas J.G., Barfield J.A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J Neurosci. 1993;13:1730–1750. doi: 10.1523/JNEUROSCI.13-04-01730.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maher E.A., Furnari F.B., Bachoo R.M., Rowitch D.H., Louis D.N., Cavenee W.K., DePinho R.A. Malignant glioma: genetics and biology of a grave matter. Genes Dev. 2001;15:1311–1333. doi: 10.1101/gad.891601. [DOI] [PubMed] [Google Scholar]
- Malatesta P., Hartfuss E., Götz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development. 2000;127:5253–5263. doi: 10.1242/dev.127.24.5253. [DOI] [PubMed] [Google Scholar]
- Mapara K.Y., Stevenson C.B., Thompson R.C., Ehtesham M. Stem cells as vehicles for the treatment of brain cancer. [ix.] Neurosurg Clin N Am. 2007;18:71–80. doi: 10.1016/j.nec.2006.10.001. [DOI] [PubMed] [Google Scholar]
- Martínez-Cerdeño V., Noctor S.C., Kriegstein A.R. The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex. 2006;16:i152–i161. doi: 10.1093/cercor/bhk017. [DOI] [PubMed] [Google Scholar]
- Masui K., Suzuki S.O., Torisu R., Goldman J.E., Canoll P., Iwaki T. Glial progenitors in the brainstem give rise to malignant gliomas by platelet-derived growth factor stimulation. Glia. 2010;58:1050–1065. doi: 10.1002/glia.20986. [DOI] [PubMed] [Google Scholar]
- Megraw T.L., Sharkey J.T., Nowakowski R.S. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 2011;21:470–480. doi: 10.1016/j.tcb.2011.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miele L., Miao H., Nickoloff B.J. NOTCH signaling as a novel cancer therapeutic target. Curr Cancer Drug Targets. 2006;6:313–323. doi: 10.2174/156800906777441771. [DOI] [PubMed] [Google Scholar]
- Mione M.C., Danevic C., Boardman P., Harris B., Parnavelas J.G. Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons. J Neurosci. 1994;14:107–123. doi: 10.1523/JNEUROSCI.14-01-00107.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miyata T., Kawaguchi A., Okano H., Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron. 2001;31:727–741. doi: 10.1016/s0896-6273(01)00420-2. [DOI] [PubMed] [Google Scholar]
- Miyata T., Kawaguchi A., Saito K., Kawano M., Muto T., Ogawa M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development. 2004;131:3133–3145. doi: 10.1242/dev.01173. [DOI] [PubMed] [Google Scholar]
- Mizukami Y., Kohgo Y., Chung D.C. Hypoxia inducible factor-1 independent pathways in tumor angiogenesis. Clin Cancer Res. 2007;13:5670–5674. doi: 10.1158/1078-0432.CCR-07-0111. [DOI] [PubMed] [Google Scholar]
- Mizutani K., Yoon K., Dang L., Tokunaga A., Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature. 2007;449:351–355. doi: 10.1038/nature06090. [DOI] [PubMed] [Google Scholar]
- Niethammer M., Smith D.S., Ayala R., Peng J.M., Ko J., Lee M.S., Morabito M., Tsai L.H. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron. 2000;28:697–711. doi: 10.1016/s0896-6273(00)00147-1. [DOI] [PubMed] [Google Scholar]
- Nieto M., Monuki E.S., Tang H., Imitola J., Haubst N., Khoury S.J., Cunningham J., Gotz M., Walsh C.A. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol. 2004;479:168–180. doi: 10.1002/cne.20322. [DOI] [PubMed] [Google Scholar]
- Nishide K., Nakatani Y., Kiyonari H., Kondo T. Glioblastoma formation from cell population depleted of Prominin1-expressing cells. PLoS One. 2009;4:e6869. doi: 10.1371/journal.pone.0006869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niu C.S., Li D.X., Liu Y.H., Fu X.M., Tang S.F., Li J. Expression of NANOG in human gliomas and its relationship with undifferentiated glioma cells. Oncol Rep. 2011;26:593–601. doi: 10.3892/or.2011.1308. [DOI] [PubMed] [Google Scholar]
- Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 2001;409:714–720. doi: 10.1038/35055553. [DOI] [PubMed] [Google Scholar]
- Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci. 2002;22:3161–3173. doi: 10.1523/JNEUROSCI.22-08-03161.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noctor S.C., Martínez-Cerdeño V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 2004;7:136–144. doi: 10.1038/nn1172. [DOI] [PubMed] [Google Scholar]
- Noctor S.C., Martínez-Cerdeño V., Kriegstein A.R. Contribution of intermediate progenitor cells to cortical histogenesis. Arch Neurol. 2007;64:639–642. doi: 10.1001/archneur.64.5.639. [DOI] [PubMed] [Google Scholar]
- Noctor S.C., Martinez-Cerdeno V., Kriegstein A.R. Neural stem and progenitor cells in cortical development. Novartis Found Symp. 2007;288:59–73. [PubMed] [Google Scholar]
- Noguera-Troise I., Daly C., Papadopoulos N.J., Coetzee S., Boland P., Gale N.W., Lin H.C., Yancopoulos G.D., Thurston G. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature. 2006;444:1032–1037. doi: 10.1038/nature05355. [DOI] [PubMed] [Google Scholar]
- Pattison L., Crow Y.J., Deeble V.J., Jackson A.P., Jafri H., Rashid Y., Roberts E., Woods C.G. A fifth locus for primary autosomal recessive microcephaly maps to chromosome 1q31. Am J Hum Genet. 2000;67:1578–1580. doi: 10.1086/316910. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plate K.H., Breier G., Weich H.A., Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature. 1992;359:845–848. doi: 10.1038/359845a0. [DOI] [PubMed] [Google Scholar]
- Price J., Thurlow L. Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development. 1988;104:473–482. doi: 10.1242/dev.104.3.473. [DOI] [PubMed] [Google Scholar]
- Purow B.W., Haque R.M., Noel M.W., Su Q., Burdick M.J., Lee J., Sundaresan T., Pastorino S., Park J.K., Mikolaenko I., et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res. 2005;65:2353–2363. doi: 10.1158/0008-5472.CAN-04-1890. [DOI] [PubMed] [Google Scholar]
- Rakic P. Neuronal migration and contact guidance in the primate telencephalon. Postgrad Med J. 1978;54:25–40. [PubMed] [Google Scholar]
- Reardon D.A., Egorin M.J., Desjardins A., Vredenburgh J.J., Beumer J.H., Lagattuta T.F., Gururangan S., Herndon J.E., 2nd, Salvado A.J., Friedman H.S. Phase I pharmacokinetic study of the vascular endothelial growth factor receptor tyrosine kinase inhibitor vatalanib (PTK787) plus imatinib and hydroxyurea for malignant glioma. Cancer. 2009;115:2188–2198. doi: 10.1002/cncr.24213. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reynolds B.A., Tetzlaff W., Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci. 1992;12:4565–4574. doi: 10.1523/JNEUROSCI.12-11-04565.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ridgway J., Zhang G., Wu Y., Stawicki S., Liang W.C., Chanthery Y., Kowalski J., Watts R.J., Callahan C., Kasman I., et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature. 2006;444:1083–1087. doi: 10.1038/nature05313. [DOI] [PubMed] [Google Scholar]
- Seidman K.J., Teng A.L., Rosenkopf R., Spilotro P., Weyhenmeyer J.A. Isolation, cloning and characterization of a putative type-1 astrocyte cell line. Brain Res. 1997;753:18–26. doi: 10.1016/s0006-8993(96)01481-3. [DOI] [PubMed] [Google Scholar]
- Shats I., Gatza M.L., Chang J.T., Mori S., Wang J., Rich J., Nevins J.R. Using a stem cell-based signature to guide therapeutic selection in cancer. Cancer Res. 2011;71:1772–1780. doi: 10.1158/0008-5472.CAN-10-1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siebzehnrubl F.A., Jeske I., Müller D., Buslei R., Coras R., Hahnen E., Huttner H.B., Corbeil D., Kaesbauer J., Appl T., et al. Spontaneous in vitro transformation of adult neural precursors into stem-like cancer cells. Brain Pathol. 2009;19:399–408. doi: 10.1111/j.1750-3639.2008.00189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–5828. [PubMed] [Google Scholar]
- Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401. doi: 10.1038/nature03128. [DOI] [PubMed] [Google Scholar]
- Smart I.H., Dehay C., Giroud P., Berland M., Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex. 2002;12:37–53. doi: 10.1093/cercor/12.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Soeda A., Inagaki A., Oka N., Ikegame Y., Aoki H., Yoshimura S., Nakashima S., Kunisada T., Iwama T. Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem. 2008;283:10958–10966. doi: 10.1074/jbc.M704205200. [DOI] [PubMed] [Google Scholar]
- Sutton L.N., Phillips P., Lange B. Midline supratentorial tumors. Neurosurg Clin N Am. 1992;3:821–837. [PubMed] [Google Scholar]
- Tamamaki N., Nakamura K., Okamoto K., Kaneko T. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res. 2001;41:51–60. doi: 10.1016/s0168-0102(01)00259-0. [DOI] [PubMed] [Google Scholar]
- Tamura K., Aoyagi M., Wakimoto H., Ando N., Nariai T., Yamamoto M., Ohno K. Accumulation of CD133-positive glioma cells after high-dose irradiation by Gamma Knife surgery plus external beam radiation. J Neurosurg. 2010;113:310–318. doi: 10.3171/2010.2.JNS091607. [DOI] [PubMed] [Google Scholar]
- Tarabykin V., Stoykova A., Usman N., Gruss P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development. 2001;128:1983–1993. doi: 10.1242/dev.128.11.1983. [DOI] [PubMed] [Google Scholar]
- Tischfield M.A., Cederquist G.Y., Gupta M.L., Jr, Engle E.C. Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr Opin Genet Dev. 2011;21:286–294. doi: 10.1016/j.gde.2011.01.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tohyama T., Lee V.M., Rorke L.B., Marvin M., McKay R.D., Trojanowski J.Q. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab Invest. 1992;66:303–313. [PubMed] [Google Scholar]
- Uhrbom L., Dai C., Celestino J.C., Rosenblum M.K., Fuller G.N., Holland E.C. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res. 2002;62:5551–5558. [PubMed] [Google Scholar]
- Uhrbom L., Hesselager G., Nistér M., Westermark B. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res. 1998;58:5275–5279. [PubMed] [Google Scholar]
- Umeshima H., Hirano T., Kengaku M. Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc Natl Acad Sci U S A. 2007;104:16182–16187. doi: 10.1073/pnas.0708047104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vick N.A., Lin M.J., Bigner D.D. The role of the subependymal plate in glial tumorigenesis. Acta Neuropathol. 1977;40:63–71. doi: 10.1007/BF00688574. [DOI] [PubMed] [Google Scholar]
- Wechsler-Reya R., Scott M.P. The developmental biology of brain tumors. Annu Rev Neurosci. 2001;24:385–428. doi: 10.1146/annurev.neuro.24.1.385. [DOI] [PubMed] [Google Scholar]
- Weissman T.A., Riquelme P.A., Ivic L., Flint A.C., Kriegstein A.R. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron. 2004;43:647–661. doi: 10.1016/j.neuron.2004.08.015. [DOI] [PubMed] [Google Scholar]
- Wells A., Kassis J., Solava J., Turner T., Lauffenburger D.A. Growth factor-induced cell motility in tumor invasion. Acta Oncol. 2002;41:124–130. doi: 10.1080/028418602753669481. [DOI] [PubMed] [Google Scholar]
- Wu D.K., Cepko C.L. Development of dopaminergic neurons is insensitive to optic nerve section in the neonatal rat retina. Brain Res Dev Brain Res. 1993;74:253–260. doi: 10.1016/0165-3806(93)90011-x. [DOI] [PubMed] [Google Scholar]
- Yoon K.J., Koo B.K., Im S.K., Jeong H.W., Ghim J., Kwon M.C., Moon J.S., Miyata T., Kong Y.Y. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron. 2008;58:519–531. doi: 10.1016/j.neuron.2008.03.018. [DOI] [PubMed] [Google Scholar]
- Yuan X., Curtin J., Xiong Y., Liu G., Waschsmann-Hogiu S., Farkas D.L., Black K.L., Yu J.S. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene. 2004;23:9392–9400. doi: 10.1038/sj.onc.1208311. [DOI] [PubMed] [Google Scholar]
- Zbinden M., Duquet A., Lorente-Trigos A., Ngwabyt S.N., Borges I., Ruiz i Altaba A. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 2010;29:2659–2674. doi: 10.1038/emboj.2010.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang M., Song T., Yang L., Chen R., Wu L., Yang Z., Fang J. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res. 2008;27:85. doi: 10.1186/1756-9966-27-85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu H., Acquaviva J., Ramachandran P., Boskovitz A., Woolfenden S., Pfannl R., Bronson R.T., Chen J.W., Weissleder R., Housman D.E., et al. Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci U S A. 2009;106:2712–2716. doi: 10.1073/pnas.0813314106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zimmer C., Tiveron M.C., Bodmer R., Cremer H. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex. 2004;14:1408–1420. doi: 10.1093/cercor/bhh102. [DOI] [PubMed] [Google Scholar]
