Adult neurogenesis and the ischemic forebrain

Journal of Cerebral Blood Flow and Metabolism

Volumn 26, Issue 1, 2006, Pages 1-20

  Lichtenwalner, Robin J ^a   Parent, Jack M ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Brain repair; Cerebral ischemia; Neural stem cell; Neurogenesis

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; EPIDERMAL GROWTH FACTOR; ERYTHROPOIETIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NEUROTROPHIC FACTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SEROTONIN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR ALPHA; VASCULOTROPIN;

ADULT; AGING; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN NERVE CELL; BRAIN REGION; CELL MIGRATION; CELL PROLIFERATION; CELL TYPE; DENTATE GYRUS; ENVIRONMENTAL ENRICHMENT; EXERCISE; FOREBRAIN; GRANULE CELL; GROWTH; HIPPOCAMPUS; HUMAN; MAMMAL; NEOSTRIATUM; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; REVIEW; RISK FACTOR; STROKE;

ANIMALS; BRAIN ISCHEMIA; DENTATE GYRUS; HUMANS; LATERAL VENTRICLES; MODELS, NEUROLOGICAL; NEURONS; PROSENCEPHALON; REGENERATION;

EID: 29144435322     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600170     Document Type: Review

References (209)

1. Åberg MA, Åberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20:2896-903
2. Ahmed S, Reynolds BA, Weiss S (1995) BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci 15:5765-5778
3. Allen E (1912) The cessation of mitosis in the central nervous system of the albino rat. J Comp Neurol 22:547-68
4. Alonso G, Prieto M, Chauvet N (1999) Tangential migration of young neurons arising from the subventricular zone of adult rats is impaired by surgical lesions passing through their natural migratory pathway. J Comp Neurol 405:508-28
5. Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573-91
6. 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 137:433-57
7. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-35
8. Andsberg G, Kokaia Z, Klein RL, Muzyczka N, Lindvall O, Mandel RJ (2002) Neuropathological and behavioral consequences of adeno-associated viral vector-mediated continuous intrastriatal neurotrophin delivery in a focal ischemia model in rats. Neurobiol Dis 9:187-204
9. Arsenijevic Y, Weiss S (1998) Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J Neurosci 18:2118-28
10. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-70
11. Arvidsson A, Kirik D, Lundberg C, Mandel RJ, Andsberg G, Kokaia Z, Lindvall O (2003) Elevated GDNF levels following viral vector-mediated gene transfer can increase neuronal death after stroke in rats. Neurobiol Dis 14:542-56
12. Arvidsson A, Kokaia Z, Lindvall O (2001) N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 14:10-8
13. Badan I, Platt D, Kessler C, Popa-Wagner A (2003) Temporal dynamics of degenerative and regenerative events associated with cerebral ischemia in aged rats. Gerontology 49:356-65
14. Bedard A, Cossette M, Levesque M, Parent A (2002) Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci Lett 328:213-6
15. Bedard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159-68
16. Benraiss A, Chmielnicki E, Lerner K, Roh D, Goldman SA (2001) Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 21:6718-31
17. Bernabeu R, Sharp FR (2000) NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab 20:1669-80
18. Bernal GM, Peterson DA (2004) Neural stem cells as therapeutic agents for age-related brain repair. Aging Cell 3:345-51
19. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99:11464-9
20. Biernaskie J, Chernenko G, Corbett D (2004) Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci 24:1245-54
21. Biernaskie J, Corbett D (2001) Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 21:5272-80
22. Brazel CY, Rosti RT, Boyce S, Rothstein RP, Levison SW (2004) Perinatal hypoxia/ischemia damages and depletes progenitors from the mouse subventricular zone. Dev Neurosci 26:266-74
23. Brezun JM, Daszuta A (1999) Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 89: 999-1002
24. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042-6
25. Calzà L, Giardino L, Pozza M, Bettelli C, Micera A, Aloe L (1998) Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: in vivo evidence of a role for nerve growth factor. Proc Natl Acad Sci USA 95: 3209-14
26. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203-9
27. Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-92
28. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894-7
29. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-17
30. Cameron HA, Tanapat P, Gould E (1998) Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82:349-54
31. Cameron HA, Woolley CS, McEwen BS, Gould E (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-44
32. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36:827-35
33. Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them asnonependymal. Neuron 35:865-75
34. Carlén M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J (2002) Functional integration of adult-born neurons. Curr Biol 12:606-8
35. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-18
36. Chen J, Magavi SS, Macklis JD (2004) Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci USA 101:16357-62
37. Chen J, Zacharek A, Zhang C, Jiang H, Li Y, Roberts C, Lu M, Kapke A, Chopp M (2005) Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 25:2366-75
38. Cheng A, Wang S, Cai J, Rao MS, Mattson MP (2003) Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev Biol 258:319-33
39. Chirumamilla S, Sun D, Bullock MR, Colello RJ (2002) Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J. Neurotrauma 19:693-703
40. Chmielnicki E, Benraiss A, Economides AN, Goldman SA (2004) 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 24:2133-42
41. Choi YS, Lee MY, Sung KW, Jeong SW, Choi JS, Park HJ, Kim ON, Lee SB, Kim SY (2003) Regional differences in enhanced neurogenesis in the dentate gyrus of adult rats after transient forebrain ischemia. Mol Cells 16:232-8
42. Cooper O, Isacson O (2004) Intrastriatal transforming growth factor α delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 24:8924-8931
43. Corotto FS, Henegar JA, Maruniak JA (1993) Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci Lett 149:111-4
44. Corotto FS, Henegar JR, Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61:739-44
45. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-58
46. Dahlqvist P, Ronnback A, Bergstrom SA, Soderstrom I, Olsson T (2004) Environmental enrichment reverses learning impairment in the Morris water maze after focal cerebral ischemia in rats. Eur J Neurosci 19:2288-98
47. Davis M, Mendelow AD, Perry RH, Chambers IR, James OF (1995) Experimental stroke and neuroprotection in the aging rat brain. Stroke 26:1072-8
48. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168:415-27
49. Dempsey RJ, Sailor KA, Bowen KK, Tureyen K, Vemuganti R (2003) Stroke-induced progenitor cell proliferation in adult spontaneously hypertensive rat brain: effect of exogenous IGF-1 and GDNF. J Neurochem 87:586-97
50. Ding Y, Li J, Luan X, Ding YH, Lai Q, Rafols JA, Phillis JW, Clark JC, Diaz FG (2004) Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 124:583-91
51. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-16
52. 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 36:1021-34
53. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632-7
54. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354-65
55. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-7
56. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803-12
57. Fallon J, Reid S, Kinyamu R, Opole I, Opole R, Baratta J, Korc M, Endo TL, Duong A, Nguyen G, Karkehabadhi M, Twardzik D, Patel S, Loughlin S (2000) In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 97:14686-91
58. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P (2004) No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 101:10177-82
59. Gage FH, Ray J, Fisher LJ (1995) Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18:159-92,
60. 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 7:1233-41
61. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci USA 97:1823-8
62. Gobbo OL, O'Mara SM (2004) Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav Brain Res 152:231-41
63. Goldman SA (1998) Adult neurogenesis: from canaries to the clinic. J Neurobiol 36:267-86
64. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-50
65. Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548-52
66. Gould E, Tanapat P (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80:427-36
67. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-71
68. Gustafsson E, Andsberg G, Darsalia V, Mohapel P, Mandel RJ, Kirik D, Lindvall O, Kokaia Z (2003) Anterograde delivery of brain-derived neurotrophic factor to striatum via nigral transduction of recombinant adeno-associated virus increases neuronal death but promotes neurogenic response following stroke. Eur J Neurosci 17:2667-78
69. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146-54
70. Hermann DM, Kilic E, Kugler S, Isenmann S, Bahr M (2001) Adenovirus-mediated GDNF and CNTF pretreatment protects against striatal injury following transient middle cerebral artery occlusion in mice. Neurobiol Dis 8:655-66
71. Holmin S, Almqvist P, Lendahl U, Mathiesen T (1997) Adult nestin-expressing subependymal cells differentiate to astrocytes in response to brain injury. Eur J Neurosci 9:65-75
72. Jiang W, Gu W, Brannstrom T, Rosqvist R, Wester P (2001) Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32:1201-7
73. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-5
74. Jin K, Minami M, Xie L, Sun Y, Mao XO, Wang Y, Simon RP, Greenberg DA (2004a) Ischemia-induced neurogenesis is preserved but reduced in the aged rodent brain. Aging Cell 3:373-7
75. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003a) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175-83
76. Jin K, Sun Y, Xie L, Childs J, Mao XO, Greenberg DA (2004b) Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 24:399-408
77. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA (2003b) Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24:171-89
78. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99:11946-50
79. Kaplan MS (1981) Neurogenesis in the 3-month-old rat visual cortex. J Comp Neurol 195:323-38
80. Kaplan MS, Bell DH (1983) Neuronal proliferation in the 9-month-old rodent-radioautographic study of granule cells in the hippocampus. Exp Brain Res 52:1-5
81. Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-4
82. Kawai T, Takagi N, Miyake-Takagi K, Okuyama N, Mochizuki N, Takeo S (2004) Characterization of BrdU-positive neurons induced by transient global ischemia in adult hippocampus. J Cereb Blood Flow Metab 24:548-55
83. Kee NJ, Preston E, Wojtowicz JM (2001) Enhanced neurogenesis after transient global ischemia in the dentate gyrus of the rat. Exp Brain Res 136:313-20
84. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-43
85. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-52
86. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-5
87. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-12
88. Kempermann G, Neumann H (2003) Microglia: the enemy within? Science 302:1689-90
89. Kershman J (1938) The medulloblast and the medulloblastoma. Arch Neurol Psychiat 40:937-67
90. Kharlamov A, Kharlamov E, Armstrong DM (2000) Age-dependent increase in infarct volume following photochemically induced cerebral infarction: putative role of astroglia. J Gerontol A Biol Sci Med Sci 55:B135-41
91. Kirschenbaum B, Goldman SA (1995) Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc Natl Acad Sci USA 92:210-4
92. Kitagawa H, Hayashi T, Mitsumoto Y, Koga N, Itoyama Y, Abe K (1998) Reduction of ischemic brain injury by topical application of glial cell line-derived neurotrophic factor after permanent middle cerebral artery occlusion in rats. Stroke 29:1417-22
93. Kitagawa H, Sasaki C, Zhang WR, Sakai K, Shiro Y, Warita H, Mitsumoto Y, Mori T, Abe K (1999) Induction of glial cell line-derived neurotrophic factor receptor proteins in cerebral cortex and striatum after permanent middle cerebral artery occlusion in rats. Brain Res 834:190-5
94. Kokaia Z, Zhao Q, Kokaia M, Elmer E, Metsis M, Smith ML, Siesjo BK, Lindvall O (1995) Regulation of brain-derived neurotrophic factor gene expression after transient middle cerebral artery occlusion with and without brain damage. Exp Neurol 136:73-88
95. Koketsu D, Mikami A, Miyamoto Y, Hisatsune T (2003) Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 23:937-42
96. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB (2002) Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. J Cereb Blood Flow Metab 22:852-60
97. Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768-73
98. Kornack DR, Rakic P (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752-7
99. Krupinski J, Kaluza J, Kumar P, Kumar S, Wang JM (1994) Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 25:1794-8
100. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyms of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-33
101. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820-9
102. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA (1999) Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 13:450-64
103. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107:603-13
104. Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA 96:7526-31
105. Lin TN, Te J, Lee M, Sun GY, Hsu CY (1997) Induction of basic fibroblast growth factor (bFGF) expression following focal cerebral ischemia. Brain Res Mol Brain Res 49:255-65
106. Linnarsson S, Willson CA, Ernfors P (2000) Cell death in regenerating populations of neurons in BDNF mutant mice. Brain Res Mol Brain Res 75:61-9
107. Liu J, Bartels M, Lu A, Sharp FR (2001) Microglia/macrophages proliferate in striatum and neocortex but not in hippocampus after brief global ischemia that produces ischemic tolerance in gerbil brain. J Cereb Blood Flow Metab 21:361-73
108. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-78
109. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-8
110. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978-81
111. Louissaint A, Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34:945-60
112. Mabuchi T, Lucero J, Feng A, Koziol JA, del Zoppo GJ (2005) Focal cerebral ischemia preferentially affects neurons distant from their neighboring microvessels. J Cereb Blood Flow Metab 25:257-66
113. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-5
114. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-10
115. Markakis EA, Gage FH (1999) Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406:449-60
116. 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 101:17528-32
117. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955-62
118. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-5
119. Montaron MF, Petry KG, Rodriguez JJ, Marinelli M, Aurousseau C, Rougon G, Le Moal M, Abrous DN (1999) Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur J Neurosci 11:1479-85
120. Moreno-Lopez B, Romero-Grimaldi C, Noval JA, Murillo-Carretero M, Matarredona ER, Estrada C (2004) Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24:85-95
121. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB (1999) Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11:4357-66
122. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-41
123. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS (1999) Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39:569-78
124. Ohlsson AL, Johansson BB (1995) Environment influences functional outcome of cerebral infarction in rats. Stroke 26:644-9
125. Ong J, Plane JM, Parent JM, Silverstein FS. Hypoxic-ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr Res (in press)
126. Otsuka H, Nakase H, Nagata K, Ueda K, Kempski O, Sakaki T (2000) Effect of age on cerebral venous circulation disturbances in the rat. J Neurosurg 93:298-304
127. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, Enikolopov G (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566-71
128. Palmer TD, Ray J, Gage FH (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6:474-86
129. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-94
130. Parent JM, Valentin VV, Lowenstein DH (2002a) Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci 22:3174-88
131. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002b) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-13
132. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-38
133. Pencea V, Bingaman KD, Freedman LJ, Luskin MB (2001a) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1-16
134. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001b) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706-17
135. Peretto P, Merighi A, Fasolo A, Bonfanti L (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42:9-21
136. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-13
137. Pincus DW, Keyoung HM, Harrison-Restelli C, Goodman RR, Fraser RA, Edgar M, Sakakibara S, Okano H, Nedergaard M, Goldman SA (1998) Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells. Ann Neurol 43:576-85
138. Plane JM, Liu R, Wang TW, Silverstein FS, Parent JM (2004) Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol Dis 16:585-95
139. Raber J, Fan Y, Matsumori Y, Liu Z, Weinstein PR, Fike JR, Liu J (2004) Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann Neurol 55:381-9
140. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464-76
141. Ray J, Raymon HK, Gage FH (1995) Generation and culturing of precursor cells and neuroblasts from embryonic and adult central nervous system. Methods Enzymol 254:20-37
142. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the mammalian central nervous system. Science 255:1707-10
143. Rice AC, Khaldi A, Harvey HB, Salman NJ, White F, Fillmore H, Bullock MR (2003) Proliferation and neuronal differentiation of mitotically active cells following traumatic brain injury. Exp Neurol 183:406-417
144. Richards LJ, Kilpatrick TJ, Bartlett PF (1992) De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA 89:8591-5
145. Rochefort C, Gheusi G, Vincent JD, Lledo PM (2002) Enriched odor exposure increases the number of new-born neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679-89
146. Romanko MJ, Rothstein RP, Levison SW (2004) Neural stem cells in the subventricular zone are resilient to hypoxia/ischemia whereas progenitors are vulnerable. J Cereb Blood Flow Metab 24:814-25
147. Roy NS, Benraiss A, Wang S, Fraser RA, Goodman R, Couldwell WT, Nedergaard M, Kawaguchi A, Okano H, Goldman SA (2000a) Promoter-targeted selection and isolation of neural progenitor cells from the adult human ventricular zone. J Neurosci Res 59:321-31
148. Roy NS, Wang S, Jiang L, Kang J, Benraiss A, Harrison-Restelli C, Fraser RA, Couldwell WT, Kawaguchi A, Okano H, Nedergaard M, Goldman SA (2000b) In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 6:271-7
149. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740-4
150. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-9
151. Sapolsky RM (1992) Do glucocorticoid concentrations rise with age in the rat? Neurobiol Aging 13:171-4
152. Schänzer A, Wachs FP, Wilhelm D, Acker T, Cooper-Kuhn C, Beck H, Winkler J, Aigner L, Plate KH, Kuhn HG (2004) Direct stimulation of adult neural stem cells in vitro and neurogenesis in vivo by vascular endothelial growth factor. Brain Pathol 14:237-48
153. Scharfman HE, Goodman JH, Sollas AL (2000) Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 20:6144-58
154. Scharfman HE, Goodman JH, Sollas AL, Croll SD (2002) Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Exp Neurol 174:201-14
155. Schmidt W, Reymann KG (2002) Proliferating cells differentiate into neurons in the hippocampal CA1 region of gerbils after global cerebral ischemia. Neurosci Lett 334:153-6
156. Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. NeuroReport 6:2479-82
157. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160
158. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-40
159. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-20
160. Shingo T, Sorokan ST, Shimazaki T, Weiss S (2001) Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 21:9733-43
161. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-6
162. Sloviter RS (1999) Status epilepticus-induced neuronal injury and network reorganization. Epilepsia 40(Suppl 1):S34-9
163. Smart IH (1961) The subepyendymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116:325-48
164. Smith MT, Pencea V, Wang Z, Luskin MB, Insel TR (2001) Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39:11-21
165. Song H, Stevens CF, Gage FH (2002a) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44
166. Song HJ, Stevens CF, Gage FH (2002b) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5:438-45
167. Stanfield BB, Trice JE (1988) Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72:399-406
168. Sugiura S, Kitagawa K, Tanaka S, Todo K, Omura-Matsuoka E, Sasaki T, Mabuchi T, Matsushita K, Yagita Y, Hori M (2005) Adenovirus-mediated gene transfer of heparin-binding epidermal growth factor-like growth factor enhances neurogenesis and angiogenesis after focal cerebral ischemia in rats. Stroke 36:859-64
169. Suh SW, Fan Y, Hong SM, Liu Z, Matsumori Y, Weinstein PR, Swanson RA, Liu J (2005) Hypoglycemia induces transient neurogenesis and subsequent progenitor cell loss in the rat hippocampus. Diabetes 54:500-9
170. Sun Y, Jin K, Childs JT, Xie L, Mao XO, Greenberg DA (2005) Neuronal nitric oxide synthase and ischemia-induced neurogenesis. J Cereb Blood Flow Metab 25:485-92
171. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, Greenberg DA (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111:1843-51
172. Szele FG, Chesselet MF (1996) Cortical lesions induce an increase in cell number and PSA-NCAM expression in the subventricular zone of adult rats. J Comp Neurol 368:439-54
173. Takagi Y, Nozaki K, Takahashi J, Yodoi J, Ishikawa M, Hashimoto N (1999) Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice. Brain Res 831:283-7
174. Takami K, Iwane M, Kiyota Y, Miyamoto M, Tsukuda R, Shiosaka S (1992) Increase of basic fibroblast growth factor immunoreactivity and its mRNA level in rat brain following transient forebrain ischemia. Exp Brain Res 90:1-10
175. Takasawa K, Kitagawa K, Yagita Y, Sasaki T, Tanaka S, Matsushita K, Ohstuki T, Miyata T, Okano H, Hori M, Matsumoto M (2002) Increased proliferation of neural progenitor cells but reduced survival of new-born cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 22:299-307
176. Tanaka R, Yamashiro K, Mochizuki H, Cho N, Onodera M, Mizuno Y, Urabe T (2004) Neurogenesis after transient global ischemia in the adult hippocampus visualized by improved retroviral vector. Stroke 35:1454-9
177. Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-801
178. Tattersfield , Croon RJ, Liu YW, Kells AP, Faull RL, Connor B (2004) Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience 127:319-32
179. Teramoto T, Qiu J, Plumier JC, Moskowitz MA (2003) EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J Clin Invest 111:1125-32
180. Thomas LB, Gates MA, Steindler DA (1996) Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 17:1-14
181. Tonchev AB, Yamashima T, Zhao L, Okano HJ, Okano H (2003) Proliferation of neural and neuronal progenitors after global brain ischemia in young adult macaque monkeys. Mol Cell Neurosci 23:292-301
182. Trejo JL, Carro E, Torres-Aleman I (2001) Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21:1628-34
183. Tropepe V, Craig CG, Morshead CM, van der Kooy D (1997) Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17:7850-9
184. Tsai TH, Chen SL, Chiang YH, Lin SZ, Ma HI, Kuo SW, Tsao YP (2000) Recombinant adeno-associated virus vector expressing glial cell line-derived neurotrophic factor reduces ischemia-induced damage. Exp Neurol 166:266-75
185. Tureyen K, Vemuganti R, Sailor KA, Bowen KK, Dempsey RJ (2004) Transient focal cerebral ischemia-induced neurogenesis in the dentate gyrus of the adult mouse. J Neurosurg 101:799-805
186. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-70
187. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-4
188. Wagner JP, Black IB, DiCicco-Bloom E (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J Neurosci 19:6006-16
189. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M (2004) Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35:1732-7
190. Wang RY, Wang PS, Yang YR (2003) Effect of age in rats followingmiddle cerebral artery occlusion. Gerontology 49:27-32
191. Wang RY, Yang YR, Yu SM (2001) Protective effects of treadmill training on infarction in rats. Brain Res 922:140-3
192. Wang S, Scott BW, Wojtowicz JM (2000) Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-57
193. Wang TW, Zhang H, Parent JM (2005) Retinoic acid regulates postnatal neurogenesis in the murine subventricular zone-olfactory bulb pathway. Development May 18 [Epub ahead of print]
194. Weinstein DE, Burrola P, Kilpatrick TJ (1996) Increased proliferation of precursor cells in the adult rat brain after targeted lesioning. Brain Res 743:11-6
195. Willis P, Berry M, Riches AC (1976) Effects of trauma on cell proliferation in the subependymal layer of the rat neocortex. Neuropathol Appl Neurobiol 2:377-88
196. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16:1681-9
197. Wurmser AE, Palmer TD, Gage FH (2004) Cellular interactions in the stem cell niche. Science 304:1253-5
198. Yagita Y, Kitagawa K, Ohtsuki T, Takasawa Ki, Miyata T, Okano H, Hori M, Matsumoto M (2001) Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 32:1890-6
199. Yamashima T, Tonchev AB, Vachkov IH, Popivanova BK, Seki T, Sawamoto K, Okano H (2004) Vascular adventitia generates neuronal progenitors in the monkey hippocampus after ischemia. Hippocampus 14:861-75
200. Yang YR, Wang RY, Wang PS (2003) Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 339:91-4
201. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98:5874-9
202. Young D, Lawlor PA, Leone P, Dragunow M, During MJ (1999) Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 5:448-53
203. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M (2001a) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50:602-11
204. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M (2004) Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24:441-8
205. Zhang RL, Zhang ZG, Zhang L, Chopp M (2001b) Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105:33-41
206. Zhang ZG, Zhang L, Jiang Q, Zhang R, Davies K, Powers C, Bruggen N, Chopp M (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106:829-38
207. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisen J, Janson AM (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 100:7925-30
208. Zhu DY, Liu SH, Sun HS, Lu YM (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23:223-9
209. Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11:234-45