Stem cells in gliomas

Handbook of Clinical Neurology

Volumn 104, Issue , 2012, Pages 63-73

  Guerrero Cazares, Hugo ^a   Attenello, Frank J ^a   Noiman, Liron ^a   Quiñones Hinojosa, Alfredo ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84855521726     PISSN: 00729752     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-52138-5.00006-2     Document Type: Chapter

References (132)

1. Aaku-Saraste E., Oback B., Hellwig A., et al. Neuroepithelial cells downregulate their plasma membrane polarity prior to neural tube closure and neurogenesis. Mech Dev 1997, 69:71-81.
2. Achanta P., Sedora Roman N.I., Quinones-Hinojosa A. Gliomagenesis and the use of neural stem cells in brain tumor treatment. Anticancer Agents Med Chem 2010, 10:121-130.
3. Al-Hajj M., Wicha M.S., Benito-Hernandez A., et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988.
4. Altman J. Proliferation and migration of undifferentiated precursor cells in the rat during postnatal gliogenesis. Exp Neurol 1966, 16:263-278.
5. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 1969, 137:433-457.
6. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965, 124:319-335.
7. Altman J., Das G.D. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 1966, 126:337-389.
8. Beier D., Hau P., Proescholdt M., et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007, 67:4010-4015.
9. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
10. Breunig J.J., Sarkisian M.R., Arellano J.I., et al. Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci U S A 2008, 105:13127-13132.
11. Brustle O., McKay R.D. The neuroepithelial stem cell concept: implications for neuro-oncology. J Neurooncol 1995, 24:57-59.
12. Bystron I., Blakemore C., Rakic P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 2008, 9:110-122.
13. Cameron H.A., Woolley C.S., McEwen B.S., et al. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56:337-344.
14. Casper K.B., McCarthy K.D. GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol Cell Neurosci 2006, 31:676-684.
15. Cattaneo E., McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 1990, 347:762-765.
16. Chaichana K.L., McGirt M.J., Frazier J., et al. Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol 2008, 89:219-224.
17. Chaichana K.L., Guerrero-Cazares H., Capilla-Gonzalez V., et al. Intra-operatively obtained human tissue: protocols and techniques for the study of neural stem cells. J Neurosci Methods 2009, 180:116-125.
18. Choi B.H., Lapham L.W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res 1978, 148:295-311.
19. Curtis M.A., Kam M., Nannmark U., et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
20. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997, 17:5046-5061.
21. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A 1999, 96:11619-11624.
22. Doetsch F., Caille I., Lim D.A., et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
23. Eberhart C.G. In search of the medulloblast: neural stem cells and embryonal brain tumors. Neurosurg Clin N Am 2007, 18:59-69. viii-ix.
24. Eckenhoff M.F., Rakic P. Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 1984, 223:1-21.
25. Esposito I., Kleeff J., Bischoff S.C., et al. The stem cell factor-c-kit system and mast cells in human pancreatic cancer. Lab Invest 2002, 82:1481-1492.
26. Farkas L.M., Huttner W.B. The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr Opin Cell Biol 2008, 20:707-715.
27. Fogarty M., Richardson W.D., Kessaris N. A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 2005, 132:1951-1959.
28. Gadisseux J.F., Evrard P. Glial-neuronal relationship in the developing central nervous system. A histochemical-electron microscope study of radial glial cell particulate glycogen in normal and reeler mice and the human fetus. Dev Neurosci 1985, 7:12-32.
29. Galli R., Binda E., Orfanelli U., et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004, 64:7011-7021.
30. Garcia-Verdugo J.M., Doetsch F., Wichterle H., et al. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 1998, 36:234-248.
31. Gonzalez-Perez O., Quinones-Hinojosa A. Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 2010, 58:975-983.
32. Gonzalez-Perez O., Romero-Rodriguez R., Soriano-Navarro M., et al. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 2009, 27:2032-2043.
33. Gotz M. Glial cells generate neurons-master control within CNS regions: developmental perspectives on neural stem cells. Neuroscientist 2003, 9:379-397.
34. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005, 6:777-788.
35. Gould E., Cameron H.A. Regulation of neuronal birth, migration and death in the rat dentate gyrus. Dev Neurosci 1996, 18:22-35.
36. Gould E., Gross C.G. Neurogenesis in adult mammals: some progress and problems. J Neurosci 2002, 22:619-623.
37. Guerrero-Cazares H., Chaichana K.L., Quinones-Hinojosa A. Neurosphere culture and human organotypic model to evaluate brain tumor stem cells. Methods Mol Biol 2009, 568:73-83.
38. Hallahan A.R., Pritchard J.I., Hansen S., et al. The smoa1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer Res 2004, 64:7794-7800.
39. Han Y.G., Spassky N., Romaguera-Ros M., et al. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 2008, 11:277-284.
40. Hansen D.V., Lui J.H., Parker P.R., et al. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
41. Hartfuss E., Galli R., Heins N., et al. Characterization of CNS precursor subtypes and radial glia. Dev Biol 2001, 229:15-30.
42. Haubensak W., Attardo A., Denk W., et al. 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.
43. Hermansson M., Nister M., Betsholtz C., et al. Endothelial cell hyperplasia in human glioblastoma: coexpression of mrna for platelet-derived growth factor (PDGF) B chain and PDGF receptor suggests autocrine growth stimulation. Proc Natl Acad Sci U S A 1988, 85:7748-7752.
44. Huntly B.J., Gilliland D.G. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer 2005, 5:311-321.
45. Imura T., Kornblum H.I., Sofroniew M.V. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 2003, 23:2824-2832.
46. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
47. Kam M., Curtis M.A., McGlashan S.R., et al. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 2009, 37:196-205.
48. Kaplan M.S., Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977, 197:1092-1094.
49. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
50. Kenney A.M., Rowitch D.H. Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 2000, 20:9055-9067.
51. Kilpatrick T.J., Bartlett P.F. Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 1993, 10:255-265.
52. Kirschenbaum B., Nedergaard M., Preuss A., et al. In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cereb Cortex 1994, 4:576-589.
53. Kleihues P., Soylemezoglu F., Schauble B., et al. Histopathology, classification, and grading of gliomas. Glia 1995, 15:211-221.
54. Koul D. PTEN signaling pathways in glioblastoma. Cancer Biol Ther 2008, 7:1321-1325.
55. Kraus J.A., Koopmann J., Kaskel P., et al. Shared allelic losses on chromosomes 1p and 19q suggest a common origin of oligodendroglioma and oligoastrocytoma. J Neuropathol Exp Neurol 1995, 54:91-95.
56. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009, 32:149-184.
57. Kriegstein A., Noctor S., Martinez-Cerdeno V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006, 7:883-890.
58. Kuhn H.G., Winkler J., Kempermann G., et al. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997, 17:5820-5829.
59. Kukekov V.G., Laywell E.D., Suslov O., et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999, 156:333-344.
60. Lachapelle F., Avellana-Adalid V., Nait-Oumesmar B., et al. Fibroblast growth factor-2 (FGF-2) and platelet-derived growth factor AB (PDGF AB) promote adult SVZ-derived oligodendrogenesis in vivo. Mol Cell Neurosci 2002, 20:390-403.
61. Lapidot T., Sirard C., Vormoor J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
62. Li J., Yen C., Liaw D., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275:1943-1947.
63. Li L., Liu F., Salmonsen R.A., et al. PTEN in neural precursor cells: regulation of migration, apoptosis, and proliferation. Mol Cell Neurosci 2002, 20:21-29.
64. Lim D.A., Cha S., Mayo M.C., et al. Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol 2007, 9:424-429.
65. Lois C., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 1993, 90:2074-2077.
66. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
67. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
68. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
69. Malatesta P., Hack M.A., Hartfuss E., et al. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 2003, 37:751-764.
70. McCarthy M., Turnbull D.H., Walsh C.A., et al. Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci 2001, 21:6772-6781.
71. Menn B., Garcia-Verdugo J.M., Yaschine C., et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006, 26:7907-7918.
72. Merkle F.T., Alvarez-Buylla A. Neural stem cells in mammalian development. Curr Opin Cell Biol 2006, 18:704-709.
73. Merkle F.T., Tramontin A.D., Garcia-Verdugo J.M., et al. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 2004, 101:17528-17532.
74. Miller M.W., Nowakowski R.S. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 1988, 457:44-52.
75. Mirzadeh Z., Merkle F.T., Soriano-Navarro M., et al. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008, 3:265-278.
76. Miyata T., Kawaguchi A., Saito K., et al. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004, 131:3133-3145.
77. Molofsky A.V., Pardal R., Iwashita T., et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425:962-967.
78. Morshead C.M., Reynolds B.A., Craig C.G., et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994, 13:1071-1082.
79. Morshead C.M., Garcia A.D., Sofroniew M.V., et al. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci 2003, 18:76-84.
80. Noctor S.C., Martinez-Cerdeno V., Ivic L., et al. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004, 7:136-144.
81. Noctor S.C., Martinez-Cerdeno V., Kriegstein A.R. Neural stem and progenitor cells in cortical development. Novartis Found Symp 2007, 288:59-73.
82. Noctor S.C., Martinez-Cerdeno V., Kriegstein A.R. Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 2008, 508:28-44.
83. Noushmehr H., Weisenberger D.J., Diefes K., et al. Identification of a cpg island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
84. Palmer T.D., Ray J., Gage F.H. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 1995, 6:474-486.
85. Palmer T.D., Takahashi J., Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 1997, 8:389-404.
86. Palmer T.D., Markakis E.A., Willhoite A.R., et al. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 1999, 19:8487-8497.
87. Park D.M., Rich J.N. Biology of glioma cancer stem cells. Mol Cells 2009, 28:7-12.
88. Parnavelas J.G., Anderson S.A., Lavdas A.A., et al. The contribution of the ganglionic eminence to the neuronal cell types of the cerebral cortex. Novartis Found Symp 2000, 228:129-139.
89. Parsa A.T., Wachhorst S., Lamborn K.R., et al. Prognostic significance of intracranial dissemination of glioblastoma multiforme in adults. J Neurosurg 2005, 102:622-628.
90. Parsons D.W., Jones S., Zhang X., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
91. Phillips H.S., Kharbanda S., Chen R., et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006, 9:157-173.
92. Piccirillo S.G., Vescovi A.L. Brain tumour stem cells: possibilities of new therapeutic strategies. Expert Opin Biol Ther 2007, 7:1129-1135.
93. Platel J.C., Gordon V., Heintz T., et al. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 2009, 57:66-78.
94. Prince M.E., Sivanandan R., Kaczorowski A., et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 2007, 104:973-978.
95. Quinones-Hinojosa A., Chaichana K. The human subventricular zone: a source of new cells and a potential source of brain tumors. Exp Neurol 2007, 205:313-324.
96. Quinones-Hinojosa A., Sanai N., Soriano-Navarro M., et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 2006, 494:415-434.
97. Raizer J.J., Abrey L.E., Lassman A.B., et al. A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro Oncol 2010, 12:95-103.
98. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 1971, 33:471-476.
99. Rakic P. DNA synthesis and cell division in the adult primate brain. Ann N Y Acad Sci 1985, 457:193-211.
100. Razis E., Selviaridis P., Labropoulos S., et al. Phase II study of neoadjuvant imatinib in glioblastoma: evaluation of clinical and molecular effects of the treatment. Clin Cancer Res 2009, 15:6258-6266.
101. Reardon D.A., Dresemann G., Taillibert S., et al. Multicentre phase II studies evaluating imatinib plus hydroxyurea in patients with progressive glioblastoma. Br J Cancer 2009, 101:1995-2004.
102. Reardon D.A., Desjardins A., Vredenburgh J.J., et al. Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J Neurooncol 2010, 96:219-230.
103. Reya T., Morrison S.J., Clarke M.F., et al. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
104. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
105. 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.
106. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
107. Roy N.S., Wang S., Jiang L., et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 2000, 6:271-277.
108. Sanai N., Berger M.S. Biology of brain tumor stem cells. Neurosurg Focus 2008, 24:E26.
109. Sanai N., Tramontin A.D., Quinones-Hinojosa A., et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
110. Sanai N., Alvarez-Buylla A., Berger M.S. Neural stem cells and the origin of gliomas. N Engl J Med 2005, 353:811-822.
111. Sanai N., Berger M.S., Garcia-Verdugo J.M., et al. Comment on Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 318:393.
112. Seri B., Garcia-Verdugo J.M., McEwen B.S., et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001, 21:7153-7160.
113. Seri B., Manuel J., Garcia V., et al. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004, 478:359-378.
114. Singh S.K., Clarke I.D., Terasaki M., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003, 63:5821-5828.
115. Singh S.K., Hawkins C., Clarke I.D., et al. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
116. Song D., Wang Z., Berger T.W. Contribution of T-type VDCC to TEA-induced long-term synaptic modification in hippocampal CA1 and dentate gyrus. Hippocampus 2002, 12:689-697.
117. Steiner B., Klempin F., Wang L., et al. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 2006, 54:805-814.
118. Stupp R., van den Bent M.J., Hegi M.E. Optimal role of temozolomide in the treatment of malignant gliomas. Curr Neurol Neurosci Rep 2005, 5:198-206.
119. Suh Y., Obernier K., Holzl-Wenig G., et al. Interaction between DLX2 and EGFR regulates proliferation and neurogenesis of SVZ precursors. Mol Cell Neurosci 2009, 42:308-314.
120. Temple S. Division and differentiation of isolated CNS blast cells in microculture. Nature 1989, 340:471-473.
121. Thurnher M.M. 2007 World Health Organization classification of tumours of the central nervous system. Cancer Imaging 2009, 9:S1-S3.
122. Tramontin A.D., Garcia-Verdugo J.M., Lim D.A., et al. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 2003, 13:580-587.
123. Verhaak R.G., Hoadley K.A., Purdom E., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
124. Voelzke W.R., Petty W.J., Lesser G.J. Targeting the epidermal growth factor receptor in high-grade astrocytomas. Curr Treat Options Oncol 2008, 9:23-31.
125. Wechsler-Reya R.J., Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 1999, 22:103-114.
126. Weigmann A., Corbeil D., Hellwig A., et al. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci U S A 1997, 94:12425-12430.
127. Wichterle H., Garcia-Verdugo J.M., Herrera D.G., et al. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 1999, 2:461-466.
128. Wichterle H., Turnbull D.H., Nery S., et al. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 2001, 128:3759-3771.
129. Wodarz A., Huttner W.B. Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech Dev 2003, 120:1297-1309.
130. Wong A.J., Bigner S.H., Bigner D.D., et al. Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invariably associated with gene amplification. Proc Natl Acad Sci U S A 1987, 84:6899-6903.
131. Zaidi H.A., Kosztowski T., DiMeco F., et al. Origins and clinical implications of the brain tumor stem cell hypothesis. J Neurooncol 2009, 93:49-60.
132. Zhadanov A.B., Provance D.W., Speer D.C., et al. Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr Biol 1999, 9:880-888.