Can adult neural stem cells create New Brains? plasticity in the adult mammalian neurogenic niches: Realities and expectations in the Era of regenerative biology

Neuroscientist

Volumn 18, Issue 1, 2012, Pages 15-27

  Kazanis, Ilias ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

brain; neurogenesis; neuroplasticity; regeneration; stem cell niche; stem cells

Indexed keywords

4 AMINOBUTYRIC ACID; EPIDERMAL GROWTH FACTOR; GLYCOPROTEIN; TENASCIN;

ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL EXPANSION; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CEREBROSPINAL FLUID; EMBRYONIC STEM CELL; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MICROENVIRONMENT; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL TUBE; NEUROSCIENCE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REGENERATIVE ABILITY; STEM CELL; STEM CELL NICHE;

ADULT STEM CELLS; ANIMALS; BRAIN; CELL DIFFERENTIATION; HUMANS; MAMMALS; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; RATS; STEM CELL NICHE;

EID: 84856489247     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858410390379     Document Type: Article

References (123)

1. Akita K, von Holst A, Furukawa Y, Mikami T, Sugahara K, Faissner A. Expression of multiple chondroitin/dermatan sulfotransferases in the neurogenic regions of the embryonic and adult central nervous system implies that complex chondroitin sulfates have a role in neural stem cell maintenance. Stem Cells. 2008 ; 26: 798-809
2. Altman J, Das GD. Autoradiographic examination of the effects of enriched environment on the rate of glial multiplication in the adult rat brain. Nature. 1964 ; 204: 1161-3
3. Altman J, Das GD. Post-natal origin of microneurones in the rat brain. Nature. 1965a ; 207: 953-6
4. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965b ; 124: 319-35
5. Altman J, Das GD. 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: 337-89
6. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci. 2001 ; 2: 287-93 (Pubitemid 33673069)
7. Barnabe-Heider F, Goritz C, Sabelstrom H, Takebayashi H, Pfrieger FW, Meletis K. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell. 2010 ; 7: 470-82
8. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL. Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science. 1999 ; 283: 534-7
9. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci. 2009 ; 12: 1524-33
10. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest. 2009 ; 119: 182-92
11. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A. 2008 ; 105: 3581-6 (Pubitemid 351723595)
12. Cajigas IJ, Will T, Schuman EM. Protein homeostasis and synaptic plasticity. EMBO J. 2010 ; 29: 2746-52
13. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci. 2009 ; 12: 259-67
14. Chen K, Henry RA, Hughes SM, Connor B. Creating a neurogenic environment: the role of BDNF and FGF2. Mol Cell Neurosci. 2007 ; 36: 108-20 (Pubitemid 47379558)
15. Chmielnicki E, Benraiss A, Economides AN, Goldman SA. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci. 2004 ; 24: 2133-42 (Pubitemid 38314545)
16. Clarke DL, Johansson CB, Wilbertz J, Veress B, Nilsson E, Karlstrom H. Generalized potential of adult neural stem cells. Science. 2000 ; 288: 1660-3 (Pubitemid 30387435)
17. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci. 2008 ; 28: 434-46
18. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science. 2007 ; 315: 1243-9 (Pubitemid 46364256)
19. De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci. 2007 ; 27: 657-64 (Pubitemid 46143769)
20. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci. 2010 ; 11: 339-50
21. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A. 1999 ; 96: 11619-24 (Pubitemid 29487430)
22. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 2002 ; 36: 1021-34 (Pubitemid 36044505)
23. Ekonomou A, Ballard CG, Pathmanaban ON, Perry RH, Perry EK, Kalaria RN. Increased neural progenitors in vascular dementia. Neurobiol Aging. 2010 ;:
24. Epp JR, Spritzer MD, Galea LA. Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience. 2007 ; 149: 273-85 (Pubitemid 47576544)
25. Etxeberria A, Mangin JM, Aguirre A, Gallo V. Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci. 2010 ; 13: 287-9
26. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull. 1999 ; 49: 377-91 (Pubitemid 29385505)
27. Franklin RJ, ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci. 2008 ; 9: 839-55
28. Gajera CR, Emich H, Lioubinski O, Christ A, Beckervordersandforth-Bonk R, Yoshikawa K. LRP2 in ependymal cells regulates BMP signaling in the adult neurogenic niche. J Cell Sci. 2010 ; 123: 1922-30
29. Galli R, Borello U, Gritti A, Minasi MG, Bjornson C, Coletta M. Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci. 2000 ; 3: 986-91
30. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci. 2004 ; 7: 1233-41 (Pubitemid 39426243)
31. Gerrow K, Triller A. Synaptic stability and plasticity in a floating world. Curr Opin Neurobiol. 2010 ; 20: 631-9
32. Gil-Mohapel J, Simpson JM, Titterness AK, Christie BR. Characterization of the neurogenesis quiescent zone in the rodent brain: effects of age and exercise. Eur J Neurosci. 2010 ; 31: 797-807
33. Gil-Perotin S, Duran-Moreno M, Belzunegui S, Luquin MR, Garcia-Verdugo JM. Ultrastructure of the subventricular zone in Macaca fascicularis and evidence of a mouse-like migratory stream. J Comp Neurol. 2009 ; 514: 533-54
34. Gotts JE, Chesselet MF. Vascular changes in the subventricular zone after distal cortical lesions. Exp Neurol. 2005a ; 194: 139-50 (Pubitemid 40719750)
35. Gotts JE, Chesselet MF. Mechanisms of subventricular zone expansion after focal cortical ischemic injury. J Comp Neurol. 2005b ; 488: 201-14 (Pubitemid 40840463)
36. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci. 2005 ; 8: 865-72
37. Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci. 2008 ; 11: 277-84 (Pubitemid 351311806)
38. Havrda MC, Harris BT, Mantani A, Ward NM, Paolella BR, Cuzon VC. Id2 is required for specification of dopaminergic neurons during adult olfactory neurogenesis. J Neurosci. 2008 ; 28: 14074-86
39. Hendriks JJ, Teunissen CE, de Vries HE, Dijkstra CD. Macrophages and neurodegeneration. Brain Res Brain Res Rev. 2005 ; 48: 185-95 (Pubitemid 40585749)
40. Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A. Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol. 1999 ; 46: 867-77
41. Hotulainen P, Hoogenraad CC. Actin in dendritic spines: connecting dynamics to function. J Cell Biol. 2010 ; 189: 619-29
42. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA. Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci. 2010 ; 13: 541-50
43. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S. 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: 187-99 (Pubitemid 44063617)
44. Jessberger S, Toni N, Clemenson GD, Ray J, Gage FH. Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat Neurosci. 2008 ; 11: 888-93
45. Jessberger S, Nakashima K, Clemenson GD, Mejia E, Mathews E, Ure K. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci. 2007 ; 27: 5967-75 (Pubitemid 46849752)
46. Jones PH, Simons BD, Watt FM. Sic transit gloria: farewell to the epidermal transit amplifying cell?. Cell Stem Cell. 2007 ; 1: 371-81 (Pubitemid 47506546)
47. Jones RG, Li X, Gray PD, Kuang J, Clayton F, Samowitz WS. Conditional deletion of beta1 integrins in the intestinal epithelium causes a loss of Hedgehog expression, intestinal hyperplasia, and early postnatal lethality. J Cell Biol. 2006 ; 175: 505-14 (Pubitemid 44708073)
48. Karpowicz P, Morshead C, Kam A, Jervis E, Ramunas J, Cheng V. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. J Cell Biol. 2005 ; 170: 721-32 (Pubitemid 41242105)
49. Kazanis I. The subependymal zone neurogenic niche: a beating heart in the centre of the brain. How plastic is adult neurogenesis? Opportunities for therapy and questions to be addressed. Brain. 2009 ; 132: 2909-21
50. Kazanis I, Belhadi A, Faissner A, ffrench-Constant C. The adult mouse subependymal zone regenerates efficiently in the absence of tenascin-C. J Neurosci. 2007 ; 27: 13991-6 (Pubitemid 351377848)
51. KazanisILathiaJMossLffrench-ConstantC. 2008. The neural stem cell microenvironment. StemBook, ed. The Stem Cell Research Community, StemBook, doi/10.3824/stembook.1.15.1, http://www.stembook.org
52. Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR. 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. 2010 ; 30: 9771-81
53. Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells. 2007 ; 25: 2146-57 (Pubitemid 47480472)
54. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci. 2006 ; 9: 173-9 (Pubitemid 43164539)
55. Kiel MJ, He S, Ashkenazi R, Gentry SN, Teta M, Kushner JA. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature. 2007 ; 449: 238-42 (Pubitemid 47402371)
56. Kraus N, Chandrasekaran B. Music training for the development of auditory skills. Nat Rev Neurosci. 2010 ; 11: 599-605
57. Lee HS, Han J, Bai HJ, Kim KW. Brain angiogenesis in developmental and pathological processes: regulation, molecular and cellular communication at the neurovascular interface. Febs J. 2009 ; 276: 4622-35
58. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci. 2004 ; 24: 7477-81 (Pubitemid 39166738)
59. Liu C, Teng ZQ, Santistevan NJ, Szulwach KE, Guo W, Jin P. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell. 2010 ; 6: 433-44
60. Liu XS, Zhang ZG, Zhang RL, Gregg SR, Meng H, Chopp M. Comparison of in vivo and in vitro gene expression profiles in subventricular zone neural progenitor cells from the adult mouse after middle cerebral artery occlusion. Neuroscience. 2007 ; 146: 1053-61 (Pubitemid 46694148)
61. Liu Y, Namba T, Liu J, Suzuki R, Shioda S, Seki T. Glial fibrillary acidic protein-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both glial fibrillary acidic protein and neuronal markers in the adult hippocampus. Neuroscience. 2010 ; 166: 241-51
62. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 1994 ; 264: 1145-8 (Pubitemid 24210676)
63. Louissaint A, Rao S, Leventhal C, Goldman SA. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron. 2002 ; 34: 945-60 (Pubitemid 34722284)
64. Luo J, Shook BA, Daniels SB, Conover JC. Subventricular zone-mediated ependyma repair in the adult mammalian brain. J Neurosci. 2008 ; 28: 3804-13
65. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science. 2009 ; 323: 1074-7
66. Mavrakis KJ, Andrew RL, Lee KL, Petropoulou C, Dixon JE, Navaratnam N. Arkadia enhances Nodal/TGF-beta signaling by coupling phospho-Smad2/3 activity and turnover. PLoS Biol. 2007 ; 5: e67
67. Melvin NR, Spanswick SC, Lehmann H, Sutherland RJ. Differential neurogenesis in the adult rat dentate gyrus: an identifiable zone that consistently lacks neurogenesis. Eur J Neurosci. 2007 ; 25: 1023-9
68. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci. 2006 ; 26: 7907-18 (Pubitemid 44315160)
69. Mercier F, Kitasako JT, Hatton GI. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol. 2002 ; 451: 170-88 (Pubitemid 34920408)
70. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science. 2007 ; 317: 381-4 (Pubitemid 47106379)
71. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A. 2004 ; 101: 17528-32 (Pubitemid 39657437)
72. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. ; 2008 ; 2008. 265.
73. Modo M, Stroemer RP, Tang E, Patel S, Hodges H. Effects of implantation site of stem cell grafts on behavioral recovery from stroke damage. Stroke. 2002 ; 33: 2270-8 (Pubitemid 35014642)
74. Modo M, Beech JS, Meade TJ, Williams SC, Price J. A chronic 1 year assessment of MRI contrast agent-labelled neural stem cell transplants in stroke. Neuroimage. 2009 ; 47 (Suppl 2). T133-42
75. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron. 1994 ; 13: 1071-82 (Pubitemid 24372126)
76. Neumeister B, Grabosch A, Basak O, Kemler R, Taylor V. Neural progenitors of the postnatal and adult mouse forebrain retain the ability to self-replicate, form neurospheres, and undergo multipotent differentiation in vivo. Stem Cells. 2009 ; 27: 714-23
77. O'Reilly AM, Lee HH, Simon MA. Integrins control the positioning and proliferation of follicle stem cells in the Drosophila ovary. J Cell Biol. 2008 ; 182: 801-15
78. Ohab JJ, Carmichael ST. Poststroke neurogenesis: emerging principles of migration and localization of immature neurons. Neuroscientist. 2008 ; 14: 369-80 (Pubitemid 352010071)
79. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 2000 ; 425: 479-94
80. Panchision DM. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol. 2009 ; 220: 562-8
81. Parras CM, Galli R, Britz O, Soares S, Galichet C, Battiste J. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 2004 ; 23: 4495-505 (Pubitemid 39601974)
82. Pastrana E, Cheng LC, Doetsch F. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci U S A. 2009 ; 106: 6387-92
83. Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol. 2005 ; 487: 407-27 (Pubitemid 40756879)
84. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol. 2010 ; 6: 193-201
85. Petreanu L, Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci. 2002 ; 22: 6106-13 (Pubitemid 35387653)
86. Pollard SM, Conti L, Sun Y, Goffredo D, Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex. 2006 ; 16 (Suppl 1). I112-20
87. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol. 2006 ; 494: 415-34 (Pubitemid 41794059)
88. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci. 2006 ; 9: 331-9 (Pubitemid 43290962)
89. Reddy L, Quiroga RQ, Wilken P, Koch C, Fried I. A single-neuron correlate of change detection and change blindness in the human medial temporal lobe. Curr Biol. 2006 ; 16: 2066-72 (Pubitemid 44573817)
90. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992 ; 255: 1707-10
91. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature. 2001 ; 412: 736-9 (Pubitemid 32771996)
92. Rizzo MT, Leaver HA. Brain endothelial cell death: modes, signaling pathways, and relevance to neural development, homeostasis, and disease. Mol Neurobiol. 2010 ; 42: 52-63
93. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 2004 ; 427: 740-4 (Pubitemid 38294593)
94. Sanchez Alvarado A, Tsonis PA. Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet. 2006 ; 7: 873-84 (Pubitemid 44607103)
95. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science. 2006 ; 311: 629-32 (Pubitemid 43191300)
96. Scadden DT. The stem-cell niche as an entity of action. Nature. 2006 ; 441: 1075-9 (Pubitemid 43990719)
97. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978 ; 4: 7-25 (Pubitemid 8376317)
98. Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV. SOX9 induces and maintains neural stem cells. Nat Neurosci. 2010 ; 13: 1181-9
99. Seki T, Namba T, Mochizuki H, Onodera M. Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol. 2007 ; 502: 275-90 (Pubitemid 46595399)
100. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol. 2004 ; 478: 359-78 (Pubitemid 39305128)
101. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell. 2008 ; 3: 289-300
102. Shibuya M. Brain angiogenesis in developmental and pathological processes: therapeutic aspects of vascular endothelial growth factor. Febs J. 2009 ; 276: 4636-43
103. Sidiropoulou K, Lu FM, Fowler MA, Xiao R, Phillips C, Ozkan ED. Dopamine modulates an mGluR5-mediated depolarization underlying prefrontal persistent activity. Nat Neurosci. 2009 ; 12: 190-9
104. Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development. 2007 ; 134: 2727-38 (Pubitemid 47307229)
105. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci. 2005 ; 25: 10-8 (Pubitemid 40110761)
106. Suhonen JO, Peterson DA, Ray J, Gage FH. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature. 1996 ; 383: 624-7 (Pubitemid 26347584)
107. Szulwach KE, Li X, Smrt RD, Li Y, Luo Y, Lin L. Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J Cell Biol. 2010 ; 189: 127-41
108. Tabata Y. Biomaterial technology for tissue engineering applications. J R Soc Interface 6 Suppl. 2009 ; 3: S311-24
109. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008 ; 3: 279-88
110. Tureyen K, Vemuganti R, Sailor KA, Bowen KK, Dempsey RJ. Transient focal cerebral ischemia-induced neurogenesis in the dentate gyrus of the adult mouse. J Neurosurg. 2004 ; 101: 799-805 (Pubitemid 39430973)
111. Uda M, Ishido M, Kami K. Features and a possible role of Mash1-immunoreactive cells in the dentate gyrus of the hippocampus in the adult rat. Brain Res. 2007 ; 1171: 9-17 (Pubitemid 47404530)
112. Urbach A, Redecker C, Witte OW. Induction of neurogenesis in the adult dentate gyrus by cortical spreading depression. Stroke. 2008 ; 39: 3064-72
113. van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005 ; 25: 8680-5 (Pubitemid 41362045)
114. von Holst A, Sirko S, Faissner A. The unique 473HD-chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci. 2006 ; 26: 4082-94 (Pubitemid 44315429)
115. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP. Microglia instruct subventricular zone neurogenesis. Glia. 2006 ; 54: 815-25 (Pubitemid 44671987)
116. Willaime-Morawek S, van der Kooy D. Cortex- and striatum-derived neural stem cells produce distinct progeny in the olfactory bulb and striatum. Eur J Neurosci. 2008 ; 27: 2354-62 (Pubitemid 351590915)
117. Willaime-Morawek S, Seaberg RM, Batista C, Labbe E, Attisano L, Gorski JA. Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J Cell Biol. 2006 ; 175: 159-68 (Pubitemid 44537207)
118. Yang Z. Postnatal subventricular zone progenitors give rise not only to granular and periglomerular interneurons but also to interneurons in the external plexiform layer of the rat olfactory bulb. J Comp Neurol. 2008 ; 506: 347-58
119. Young KM, Fogarty M, Kessaris N, Richardson WD. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci. 2007 ; 27: 8286-96 (Pubitemid 47219615)
120. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell. 2010 ; 6: 578-90
121. Zhao JW, Raha-Chowdhury R, Fawcett JW, Watts C. Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur J Neurosci. 2009 ; 29: 1853-69
122. Zhao S, Chai X, Frotscher M. Balance between neurogenesis and gliogenesis in the adult hippocampus: role for reelin. Dev Neurosci. 2007 ; 29: 84-90 (Pubitemid 44934964)
123. Zhao X, Ueba T, Christie BR, Barkho B, McConnell MJ, Nakashima K. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc Natl Acad Sci U S A. 2003 ; 100: 6777-82 (Pubitemid 36666656)