Adult periventricular neural stem cells: Outstanding progress and outstanding issues

Developmental Neurobiology

Volumn 72, Issue 7, 2012, Pages 972-989

  Chojnacki, Andrew ^a   Cusulin, Carlo ^a   Weiss, Samuel ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Adult periventricular neural stem cells; Interkinetic nuclear migration; Notch signaling; Self renewal; Subventricular zone

Indexed keywords

EPITHELIUM DERIVED INHIBITORY FACTOR; NOTCH INTRACELLULAR DOMAIN PROTEIN; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ADULT PERIVENTRICULAR NEURAL STEM CELL; ARTICLE; BRAIN INJURY; CELL MIGRATION; CELL POPULATION; GLIA CELL; HUMAN; INTERKINETIC NUCLEAR MIGRATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIAL GLIAL CELL; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; UPREGULATION;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CEREBRAL VENTRICLES; NEURAL STEM CELLS; NEURONS;

EID: 84862142149     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22029     Document Type: Article

References (133)

1. Ables JL, Breunig JJ, Eisch AJ, Rakic P. 2011. Not(ch) just development: Notch signalling in the adult brain. Nat Rev Neurosci 12: 269-283.
2. Aguirre A, Rubio ME, Gallo V. 2010. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467: 323-327.
3. Ahn S, Joyner AL. 2005. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894-897.
4. Alexson TO, Hitoshi S, Coles BL, Bernstein A, van der Kooy D. 2006. Notch signaling is required to maintain all neural stem cell populations-Irrespective of spatial or temporal niche. Dev Neurosci 28: 34-48.
5. Allen E. 1912. The cessation of mitosis in the central nervous system of the albino rat. J Comp Neurol 22: 547-568.
6. Altman J. 1963. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145: 573-591.
7. Altman J. 1969. 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 137: 433-457.
8. Altman J, Das GD. 1965a. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335.
9. Altman J, Das GD. 1965b. Post-natal origin of microneurones in the rat brain. Nature 207: 953-956.
10. Andreu-Agullo C, Morante-Redolat JM, Delgado AC, Farinas I. 2009. Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci 12: 1514-1523.
11. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963-970.
12. Barnabe-Heider F, Goritz C, Sabelstrom H, Takebayashi H, Pfrieger FW, Meletis K, Frisen J. 2010. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7: 470-482.
13. Bayer SA. 1983. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50: 329-340.
14. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, et al. 2010. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7: 744-758.
15. Bedard A, Parent A. 2004. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151: 159-168.
16. Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H. 2011. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145: 1142-1155.
17. Bouab M, Paliouras GN, Aumont A, Forest-Berard K, Fernandes KJ. 2011. Aging of the subventricular zone neural stem cell niche: Evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 173: 135-149.
18. Boulder Committee. 1970. Embryonic vertebrate central nervous system: Revised terminology. Anat Rec 166: 257-261.
19. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, et al. 2008. Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci USA 105: 3581-3586.
20. Burrows RC, Wancio D, Levitt P, Lillien L. 1997. Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19: 251-267.
21. Campbell K, Gotz M. 2002. Radial glia: Multi-purpose cells for vertebrate brain development. Trends Neurosci 25: 235-238.
22. Capela A, Temple S. 2002. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35: 865-875.
23. Cappello S, Monzo P, Vallee RB. 2011. NudC is required for interkinetic nuclear migration and neuronal migration during neocortical development. Dev Biol 357: 326-335.
24. Caric D, Raphael H, Viti J, Feathers A, Wancio D, Lillien L. 2001. EGFRs mediate chemotactic migration in the developing telencephalon. Development 128: 4203-4216.
25. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, et al. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12: 259-267.
26. Chapouton P, Skupien P, Hesl B, Coolen M, Moore JC, Madelaine R, Kremmer E, et al. 2010. Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells. J Neurosci 30: 7961-7974.
27. Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D. 1999. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 19: 4462-4471.
28. Chojnacki A, Mak G, Weiss S. 2011. PDGFRalpha expression distinguishes GFAP-expressing neural stem cells from PDGF-responsive neural precursors in the adult periventricular area. J Neurosci 31: 9503-9512.
29. Chojnacki A, Weiss S. 2004. Isolation of a novel platelet-derived growth factor-responsive precursor from the embryonic ventral forebrain. J Neurosci 24: 10888-10899.
30. Chojnacki AK, Mak GK, Weiss S. 2009. Identity crisis for adult periventricular neural stem cells: Subventricular zone astrocytes, ependymal cells or both? Nat Rev Neurosci 10: 153-163.
31. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, et al. 2008. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28: 434-446.
32. Corbin JG, Gaiano N, Machold RP, Langston A, Fishell G. 2000. The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development 127: 5007-5020.
33. Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, et al. 2008. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA 105: 1026-1031.
34. Costa MR, Bucholz O, Schroeder T, Gotz M. 2009. Late origin of glia-restricted progenitors in the developing mouse cerebral cortex. Cereb Cortex 19 ( Suppl 1): i135-i143.
35. Costa MR, Gotz M, Berninger B. 2010. What determines neurogenic competence in glia? Brain Res Rev 63: 47-59.
36. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, et al. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249.
37. Darsalia V, Heldmann U, Lindvall O, Kokaia Z. 2005. Stroke-induced neurogenesis in aged brain. Stroke 36: 1790-1795.
38. Davis AA, Temple S. 1994. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372: 263-266.
39. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999a. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
40. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1999b. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 96: 11619-11624.
41. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. 2002. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36: 1021-1034.
42. Farkas LM, Haffner C, Giger T, Khaitovich P, Nowick K, Birchmeier C, Paabo S, et al. 2008. Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron 60: 40-55.
43. Formstone CJ, Moxon C, Murdoch J, Little P, Mason I. 2010. Basal enrichment within neuroepithelia suggests novel function(s) for Celsr1 protein. Mol Cell Neurosci 44: 210-222.
44. Fukushima N, Yokouchi K, Kawagishi K, Moriizumi T. 2002. Differential neurogenesis and gliogenesis by local and migrating neural stem cells in the olfactory bulb. Neurosci Res 44: 467-473.
45. Gabay L, Lowell S, Rubin LL, Anderson DJ. 2003. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40: 485-499.
46. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. 2004. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7: 1233-1241.
47. Goldman SA, Chen Z. 2011. Perivascular instruction of cell genesis and fate in the adult brain. Nat Neurosci 14: 1382-1389.
48. Gritti A, Bonfanti L, Doetsch F, Caille I, Alvarez-Buylla A, Lim DA, Galli R, et al. 2002. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 22: 437-445.
49. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, et al. 1996. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16: 1091-1100.
50. Guentchev M, McKay RD. 2006. Notch controls proliferation and differentiation of stem cells in a dose-dependent manner. Eur J Neurosci 23: 2289-2296.
51. Guerrero-Cazares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, Garcia-Verdugo JM, Quinones-Hinojosa A. 2011. Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 519: 1165-1180.
52. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M. 2005. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8: 865-872.
53. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Gotz M. 2004. Regionalization and fate specification in neurospheres: The role of Olig2 and Pax6. Mol Cell Neurosci 25: 664-678.
54. Han YG, Alvarez-Buylla A. 2010. Role of primary cilia in brain development and cancer. Curr Opin Neurobiol 20: 58-67.
55. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229: 15-30.
56. Hinds JW. 1968. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J Comp Neurol 134: 287-304.
57. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, et al. 2002a. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16: 846-858.
58. Hitoshi S, Tropepe V, Ekker M, van der Kooy D. 2002b. Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development 129: 233-244.
59. Hugnot JP, Franzen R. 2011. The spinal cord ependymal region: A stem cell niche in the caudal central nervous system. Front Biosci 16: 1044-1059.
60. Huttner HB, Janich P, Kohrmann M, Jaszai J, Siebzehnrubl F, Blumcke I, Suttorp M, et al. 2008. The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying central nervous system disease. Stem Cells 26: 698-705.
61. 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.
62. Ihrie RA, Alvarez-Buylla A. 2011. Lake-front property: A unique germinal niche by the lateral ventricles of the adult brain. Neuron 70: 674-686.
63. Ihrie RA, Shah JK, Harwell CC, Levine JH, Guinto CD, Lezameta M, Kriegstein AR, et al. 2011. Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71: 250-262.
64. Imura T, Kornblum HI, Sofroniew MV. 2003. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 23: 2824-2832.
65. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, Ming GL, et al. 2010. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 13: 541-550.
66. Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, Adams AC, Sahin E, et al. 2011. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469: 102-106.
67. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34.
68. Kam M, Curtis MA, McGlashan SR, Connor B, Nannmark U, Faull RL. 2009. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 37: 196-205.
69. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197: 1092-1094.
70. Karpowicz P, Morshead C, Kam A, Jervis E, Ramunas J, Cheng V, van der Kooy D. 2005. Support for the immortal strand hypothesis: Neural stem cells partition DNA asymmetrically in vitro. J Cell Biol 170: 721-732.
71. Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, et al. 2010. Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30: 9771-9781.
72. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A. 2005. Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25: 6997-7003.
73. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, et al. 2007. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27: 6878-6891.
74. Kosodo Y, Suetsugu T, Suda M, Mimori-Kiyosue Y, Toida K, Baba SA, Kimura A, et al. 2011. Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain. EMBO J 30: 1690-1704.
75. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. 2008. The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18: 28-35.
76. Lewis PD. 1968. A quantitative study of cell proliferation in the subependymal layer of the adult rat brain. Exp Neurol 20: 203-207.
77. Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P. 2010. Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci 30: 4197-4209.
78. Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Gotz M, Haas CA, et al. 2010. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6: 445-456.
79. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173-189.
80. Malatesta P, Hartfuss E, Gotz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127: 5253-5263.
81. Marzesco AM, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB. 2005. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118: 2849-2858.
82. Matyash V, Kettenmann H. 2010. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 63: 2-10.
83. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26: 7907-7918.
84. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317: 381-384.
85. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. 2004. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101: 17528-17532.
86. Messier B, Leblond CP, Smart I. 1958. Presence of DNA synthesis and mitosis in the brain of young adult mice. Exp Cell Res 14: 224-226.
87. Migaud M, Batailler M, Segura S, Duittoz A, Franceschini I, Pillon D. 2010. Emerging new sites for adult neurogenesis in the mammalian brain: A comparative study between the hypothalamus and the classical neurogenic zones. Eur J Neurosci 32: 2042-2052.
88. Ming GL, Song H. 2011. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 70: 687-702.
89. Mira H, Andreu Z, Suh H, Lie DC, Jessberger S, Consiglio A, San Emeterio J, et al. 2010. Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7: 78-89.
90. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3: 265-278.
91. Mori T, Tanaka K, Buffo A, Wurst W, Kuhn R, Gotz M. 2006. Inducible gene deletion in astroglia and radial glia-A valuable tool for functional and lineage analysis. Glia 54: 21-34.
92. Morshead CM, Garcia AD, Sofroniew MV, van Der Kooy D. 2003. 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 18: 76-84.
93. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, et al. 1994. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071-1082.
94. Nakada D, Levi BP, Morrison SJ. 2011. Integrating physiological regulation with stem cell and tissue homeostasis. Neuron 70: 703-718.
95. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: 714-720.
96. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR. 2002. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22: 3161-3173.
97. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: 136-144.
98. Nottebohm F. 2004. The road we travelled: Discovery, choreography, and significance of brain replaceable neurons. Ann N Y Acad Sci 1016: 628-658.
99. Nyfeler Y, Kirch RD, Mantei N, Leone DP, Radtke F, Suter U, Taylor V. 2005. Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J 24: 3504-3515.
100. Pastrana E, Cheng LC, Doetsch F. 2009. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA 106: 6387-6392.
101. Rakic P. 1985. Limits of neurogenesis in primates. Science 227: 1054-1056.
102. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, et al. 2006. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9: 331-339.
103. Ravin R, Hoeppner DJ, Munno DM, Carmel L, Sullivan J, Levitt DL, Miller JL, et al. 2008. Potency and fate specification in CNS stem cell populations in vitro. Cell Stem Cell 3: 670-680.
104. Recht L, Jang T, Savarese T, Litofsky NS. 2003. Neural stem cells and neuro-oncology: Quo vadis? J Cell Biochem 88: 11-19.
105. Reynolds BA, Tetzlaff W, Weiss S. 1992. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12: 4565-4574.
106. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
107. Reynolds BA, Weiss S. 1996. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175: 1-13.
108. Richards LJ, Kilpatrick TJ, Bartlett PF. 1992. De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA 89: 8591-8595.
109. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. 2001. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412: 736-739.
110. Ruckh JM, Zhao JW, Shadrach JL, van Wijngaarden P, Rao TN, Wagers AJ, Franklin RJ. 2012. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 10: 96-103.
111. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, et al. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478: 382-386.
112. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, et al. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744.
113. Sauer FC. 1935. Mitosis in the neural tube. J Comp Neurol 62: 377-405.
114. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, et al. 2008. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3: 289-300.
115. Shihabuddin LS, Horner PJ, Ray J, Gage FH. 2000. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 20: 8727-8735.
116. Shimojo H, Ohtsuka T, Kageyama R. 2008. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58: 52-64.
117. Smart I. 1961. The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116: 325-347.
118. Stenman J, Toresson H, Campbell K. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: Implications for striatal and olfactory bulb neurogenesis. J Neurosci 23: 167-174.
119. Suhonen JO, Peterson DA, Ray J, Gage FH. 1996. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383: 624-627.
120. Sun Y, Goderie SK, Temple S. 2005. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45: 873-886.
121. Taverna E, Huttner WB. 2010. Neural progenitor nuclei IN motion. Neuron 67: 906-914.
122. Toresson H, Campbell K. 2001. A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128: 4769-4780.
123. Tsai JW, Chen Y, Kriegstein AR, Vallee RB. 2005. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J Cell Biol 170: 935-945.
124. Vukovic J, Blackmore DG, Jhaveri D, Bartlett PF. 2011. Activation of neural precursors in the adult neurogenic niches. Neurochem Int 59: 341-346.
125. Wang C, Liu F, Liu YY, Zhao CH, You Y, Wang L, Zhang J, et al. 2011. Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21: 1534-1550.
126. Weigmann A, Corbeil D, Hellwig A, Huttner WB. 1997. 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 USA 94: 12425-12430.
127. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. 1996. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599-7609.
128. Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A. 1999. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2: 461-466.
129. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. 2001. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128: 3759-3771.
130. Willaime-Morawek S, van der Kooy D. 2008. Cortex- and striatum- derived neural stem cells produce distinct progeny in the olfactory bulb and striatum. Eur J Neurosci 27: 2354-2362.
131. Wilsch-Brauninger M, Peters J, Paridaen JT, Huttner WB. 2012. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139: 95-105.
132. Xie Z, Moy LY, Sanada K, Zhou Y, Buchman JJ, Tsai LH. 2007. Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron 56: 79-93.
133. Yun K, Garel S, Fischman S, Rubenstein JL. 2003. Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia. J Comp Neurol 461: 151-165.