Endogenous neurogenesis induced by ischemic brain injury or neurodegenerative diseases in adults

Acta Neurobiologiae Experimentalis

Volumn 72, Issue 4, 2012, Pages 309-324

  Ziemka Nałecz, Małgorzata ^a   Zalewska, Teresa ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Adult brain disorders; Epigenetic agents; Neural progenitors; Neurogenic zones

Indexed keywords

ADULT STEM CELL; ANIMAL; BRAIN INJURY; BRAIN ISCHEMIA; DEGENERATIVE DISEASE; HUMAN; NERVOUS SYSTEM DEVELOPMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ADULT STEM CELLS; ANIMALS; BRAIN INJURIES; BRAIN ISCHEMIA; HUMANS; NEURODEGENERATIVE DISEASES; NEUROGENESIS;

EID: 84874548398     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Review

References (140)

1. Abel T, Zukin RS (2008) Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Curr Opin Pharmacol 8: 57-64.
2. Androutsellis-Theotokis A, Rueger MA, Park DM, Mkhikian H, Korb E, Poser SW, Walbridge S, Munasinge J, Koretsky AP, Lonser RR, McKay RD (2009) Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc Natl Acad Sci U S A 106: 13570-13575.
3. Arias-Carrión O, Drucker-Colín R (2007) Neurogenesis as a therapeutic strategy to regenerate central nervous system. Rev Neurol 45: 739-745.
4. 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: 10-18.
5. 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.
6. Baker SA, Baker KA, Hagg T (2004) Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur J Neurosci 20: 575-579.
7. Balu DT, Lucki I (2009) Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33: 232-252.
8. Bendel O, Bueters T, von Euler M, Ove Ogren S, Sandin J, von Euler G (2005) Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J Cereb Blood Flow Metab 25: 1586-1595.
9. 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: 1669-1680.
10. Bonfanti L, Ponti G (2008) title typecontributorAdult mammalian neurogenesis and the New Zealand white rabbit/title. Vet J 175: 310-331.
11. Bovetti S, Bovolin P, Perroteau I, Puche AC (2007) Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur J Neurosci 25: 2021-2033.
12. Burns TC, Verfaillie CM, Low WC (2009) Stem Cells for ischemic brain injury: a critical review. J Comp Neurol 515: 125-144.
13. Butt AM, Dinsdale J (2005a) Fibroblast growth factor 2 induces loss of adult oligodendrocytes and myelin in vivo. Exp Neurol 192: 125-133.
14. Butt AM, Dinsdale J (2005b) Fibroblast growth factor 2 mediated disruption of myelin-forming oligodendrocytes in vivo is associated with increased tau immunoreactivity. Neurosci Lett 375: 28-32.
15. Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyru. J Neurosci 15: 4687-4692.
16. Cantarella C, Cayre M, Magalon K, Durbec P (2008) Intranasal HB-EGF administration favors adult SVZ cell mobilization to demyelinated lesions in mouse corpus callosum. Dev Neurobiol 68: 223-236.
17. Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10: 295-304.
18. Cooper O, Isacson O (2004) Intrastriatal transforming growth factor alpha 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.
19. Couillard-Despres S, Finkl R, Winner B, Ploetz S, Wiedermann D, Aigner R, Bogdahn U, Winkler J, Hoehn M, Aigner L (2008) In vivo optical imaging of neurogenesis: watching new neurons in the intact brain. Mol Imaging 7: 28-34.
20. Cova L, Armentero MT, Zennaro E, Calzarossa C, Bossolasco P, Busca G, Lambertenghi Deliliers G, Polli E, Nappi G, Silani V, Blandini F (2010) Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson's disease. Brain Res 1311: 12-27.
21. Covic M, Karaca E, Lie DC (2010) Epigenetic regulation of neurogenesis in the adult hippocampus. Heredity (Edinb) 105: 122-134.
22. Crews L, Mizuno H, Desplats P, Rockenstein E, Adame A, Patrick C, Winner B, Winkler J, Masliah E (2008) Alpha-synuclein alters Notch-1 expression and neurogenesis in mouse embryonic stem cells and in the hippocampus of transgenic mice. J Neurosci 28: 4250-4260.
23. Curtis MA, Penney EB, Pearson AG, van Roon-Mom WM, Butterworth NJ, Dragunow M, Connor B, Faull RL (2003) Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci U S A 100: 9023-9027.
24. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtås S, van Roon-Mom WM, Björk-Eriksson T, Nordborg C, Frisén J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249.
25. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36: 1790-1795.
26. Dirnagl U (2006) Bench to bedside: the quest for quality in experimental stroke research. J Cereb Blood Flow Metab 26: 1465-1478.
27. Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-5061.
28. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ (2006) Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495: 70-83.
29. El Amki M, Lerouet D, Coqueran B, Curis E, Orset C, Vivien D, Plotkine M, Marchand-Leroux C, Margaill I (2012) Experimental modeling of recombinant tissue plasminogen activator effects after ischemic stroke. Exp Neurol 238: 138-144.
30. Emsley JG, Mitchell BD, Kempermann G, Macklis JD (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75: 321-341.
31. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317.
32. García-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36: 234-248.
33. Gibson CL, Murphy SP (2010) Benefits of histone deacetylase inhibitors for acute brain injury: a systematic review of animal studies. J Neurochem 115: 806-813.
34. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8: 481-488.
35. Graff J, Kim D, Dobbin MM, Tsai LH (2011) Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol Rev 91: 603-649.
36. Gray M, Shirasaki DI, Cepeda C, André VM, Wilburn B, Lu XH, Tao J, Yamazaki I, Li SH, Sun YE, Li XJ, Levine MS, Yang XW (2008) Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice. J Neurosci 28: 6182-6195.
37. Grote HE, Hannan AJ (2007) Regulators of adult neurogenesis in the healthy and diseased brain. Clin Exp Pharmacol Physiol 34: 533-545.
38. Gu WG, Brannstrom T, Wester P (2000) Cortical neurogenesis in adult rats after reversible phototrombotic stroke. J Cereb Blood Flow Metab 20: 1166-1173.
39. Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-42.
40. Hagg T (2005) Molecular regulation of adult CNS neurogenesis: an integrated view. Trends Neurosci 28: 589-595.
41. Heurteaux C, Gandin C, Borsotto M, Widmann C, Brau F, Lhuillier M, Onteniente B, Lazdunski M (2010) Neuroprotective and neuroproliferative activities of NeuroAid (MLC601, MLC901), a Chinese medicine, in vitro and in vivo. Neuropharmacology 58: 987-1001.
42. von Horsten S, Schmitt I, Nguyen HP, Holzmann C, Schmidt T, Walther T, Bader M, Pabst R, Kobbe P, Krotova J, Stiller D, Kask A, Vaarmann A, Rathke-Hartlieb S, Schulz JB, Grasshoff U, Bauer I, Vieira-Saecker AM, Paul M, Jones L, Lindenberg KS, Landwehrmeyer B, Bauer A, Li XJ, Riess O (2003) Transgenic rat model of Huntington's disease. Hum Mol Genet 12: 617-624.
43. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7: 726-735.
44. Huisman E, Uylings HB, Hoogland PV (2004) A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson's disease. Mov Disord 19: 687-692.
45. Ihunwo AO, Schliebs R (2010) Cell proliferation and total granule cell number in dentate gyrus of transgenic Tg2576 mouse. Acta Neurobiol Exp (Wars) 70: 362-369.
46. Jablonska A, Lukomska B (2011) Stroke induced brain changes: Implications for stem cell transplantation. Acta Neurobiol Exp (Wars) 71: 74-85. [Erratum in: Acta Neurobiol Exp (Wars) 71: 303.]
47. Jiang W, Gu WG, Brannstrom T, Rosquist R, Wester P (2001) Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32: 1201-1207.
48. 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 U S A 98: 4710-4715.
49. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA (2003a) Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24: 171-189
50. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003b) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2: 175-183.
51. 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: 373-377.
52. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA (2004b) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101: 343-347.
53. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA (2006) Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 103: 13198-13202.
54. Kadir A, Nordberg A (2010) Target-specific PET probes for neurodegenerative disorders related to dementia. J Nucl Med 51: 1418-1430.
55. Kandasamy M, Couillard-Despres S, Raber KA, Stephan M, Lehner B, Winner B, Kohl Z, Rivera FJ, Nguyen HP, Riess O, Bogdahn U, Winkler J, von Hörsten S, Aigner L (2010) Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J Neuropathol Exp Neurol 69: 717-728.
56. Kazantsev AG, Thompson LM (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 7: 854-868.
57. Kee NJ, Preston E, Wojtowicz JM (2001) Enhanced neurogenesis after transient global ischemia in the dentate gyrus of the rat. Exp Brain Res 136: 313-320.
58. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18: 3206-3212.
59. Kim HJ, Rowe M, Ren M, Hong JS, Chen PS, Chuang DM (2007) Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: multiple mechanisms of action. J Pharmacol Exp Ther 321: 892-901.
60. Kim HJ, Leeds P, Chuang DM (2009) The HDAC inhibitor, sodium butyrate, stimulates neurogenesis in the ischemic brain. J Neurochem 110: 1226-1240.
61. 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. Brain Res 834: 190-195.
62. Kohl Z, Kandasamy M, Winner B, Aigner R, Gross C, Couillard-Despres S, Bogdahn U, Aigner L, Winkler J (2007) Physical activity fails to rescue hippocampal neu-rogenesis deficits in the R6/2 mouse model of Huntington's disease. Brain Res 1155: 24-33.
63. Kohl Z, Regensburger M, Aigner R, Kandasamy M, Winner B, Aigner L, Winkler J (2010) Impaired adult olfactory bulb neurogenesis in the R6/2 mouse model of Huntington's disease. BMC Neurosci 11: 114.
64. Kokaia Z, Zhao Q, Kokaia M, Elmér E, Metsis M, Smith ML, Siesjö 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.
65. Kokaia Z, Lindvall O (2003) Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 13: 127-132.
66. Kokaia Z, Thored P, Arvidsson A, Lindvall O (2006) Regulation of stroke-induced neurogenesis in adult brain--recent scientific progress. Cereb Cortex 16 (Suppl 1): 162-167.
67. Komitova M, Mattsson B, Johansson BB, Eriksson PS (2005) Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 36: 1278-1282.
68. Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294: 2127-2130.
69. Krafft PR, Bailey EL, Lekic T, Rolland WB, Altay O, Tang J, Wardlaw JM, Zhang JH, Sudlow CL (2012) Etiology of stroke and choice of models. Int J Stroke 7: 398-406.
70. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
71. Kuhn HG, Palmer TD, Fuchs E (2001) Adult neurogenesis: a compensatory mechanism for neuronal damage. Eur Arch Psychiatry Clin Neurosci 251: 152-158.
72. Langley B, Brochier C, Rivieccio MA (2009) Targeting his-tone deacetylases as a multifaceted approach to treat the diverse outcomes of stroke. Stroke 40: 2899-2905.
73. Latham JA, Dent SY (2007) Cross-regulation of histone modifications. Nat Struct Mol Biol 14: 1017-1024.
74. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer's disease: at the crossroads. Exp Neurol 223: 267-281.
75. Lazic SE, Grote HE, Armstrong RJ, Blakemore C, Hannan AJ, van Dellen A, Barker RA (2004) Decreased hip-pocampal cell proliferation in R6/1 Huntington's mice. NeuroReport 15: 811-813.
76. Leker RR, Soldner F, Velasco I, Gavin DK, Androutsellis-Theotokis A, McKay RD (2007) Long-lasting regeneration after ischemia in the cerebral cortex. Stroke 38: 153-161.
77. 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: 603-613.
78. Lie DC, Song H, Colamarino SA, Ming GL, Gager FH (2004) Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44: 399-421
79. 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: 255-265.
80. Lindvall O, Kokaia Z (2010) Stem cells in human neurode-generative disorders--time for clinical translation? J Clin Invest 120: 29-40.
81. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18: 7768-7778.
82. ledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7: 179-193.
83. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148.
84. Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5: 139-152.
85. Macas J, Nern C, Plate KH, Momma S (2006) Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26: 13114-13119.
86. MacMillan KS, Naidoo J, Liang J, Melito L, Williams NS, Morlock L, Huntington PJ, Estill SJ, Longgood J, Becker GL, McKnight SL, Pieper AA, De Brabander JK, Ready JM (2011) Development of proneurogenic, neuroprotective small molecules. J Am Chem Soc 133: 1428-1437.
87. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405: 951-955.
88. Magavi SS, Mitchell BD, Szentirmai O, Carter BS, Macklis JD (2005) Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 25: 10729-10739.
89. Marlatt MW, Lucassen PJ (2010) Neurogenesis and Alzheimer's disease: Biology and pathophysiology in mice and men. Curr Alzheimer Res 7: 113-125.
90. Marxreiter F, Nuber S, Kandasamy M, Klucken J, Aigner R, Burgmayer R, Couillard-Despres S, Riess O, Winkler J, Winner B (2009) Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein. Eur J Neurosci 29: 879-890.
91. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24: 1726-1733.
92. Masuda T, Isobe Y, Aihara N, Furuyama F, Misumi S, Kim TS, Nishino H, Hida H (2007) Increase in neurogenesis and neuroblast migration after a small intrac-erebral hemorrhage in rats. Neurosci Lett 425: 114-119.
93. 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.
94. Minger SL, Ekonomou A, Carta EM, Chinoy A, Perry RH, Ballard CG (2007) Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med 2: 69-74.
95. Mino M, Kamii H, Fujimura M, Kondo T, Takasawa S, Okamoto H, Yoshimoto T (2003) Temporal Changes of neurogenesis in the mouse hippocampus after experimental subarachnoid hemorrhage. Neurol Res 25: 839-845.
96. Mirochnic S, Wolf S, Staufenbiel M, Kempermann G (2009) Age effects on the regulation of adult hippocampal neurogenesis by physical activity and environmental enrichment in the APP23 mouse model of Alzheimer disease. Hippocampus 19: 1008-1018.
97. Mu Y, Lee SW, Gage FH (2010) Signaling in adult neuro-genesis. Curr Opin Neurobiol 20: 416-423.
98. Nakashima T, Minematsu K (2009) Prospects in throm-bolytic therapy for acute ischemic stroke. Brain Nerve 61: 1003-1012.
99. 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: 429-441.
100. Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26: 13007-13016.
101. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, Miyakawa T, Kaneko T, Nakamura S (2010) Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci 13: 173-179.
102. Otero L, Zurita M, Bonilla C, Rico MA, Aguayo C, Rodriguez Z, Vaquero J (2012) Endogenous neurogenesis after intracerebral hemorrhage. Histol Histopathol 27: 303-315.
103. Ourednik J, Ourednik V, Lynch WP, Schachner M, Snyder EY (2002) Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol 20: 1103-1110.
104. Palmer TD, Markakis DA, Willhoite AR, Safar F, Gage FH (1999)Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19: 8487-8497.
105. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52: 802-813.
106. Parent JM (2003) Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9: 261-272.
107. Pearson AG, Curtis MA, Waldvogel HJ, Faull RL, Dragunow M (2005) Activating transcription factor 2 expression in the adult human brain: Association with both neurodegeneration and neurogenesis. Neuroscience 133: 437-451.
108. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113.
109. Phillips W, Morton AJ, Baker RA (2005) Abnormalities of neurogenesis in the R6/2 mouse model of Huntington's disease are attributable to the in vivo microenvironment. J. Neurosci 25: 11564-11576.
110. Pieper AA, Wu X, Han TW, Estill SJ, Dang Q, Wu LC, Reece-Fincanon S, Dudley CA, Richardson JA, Brat DJ, McKnight SL (2005) The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice. Proc Natl Acad Sci U S A 102: 14052-14057.
111. Rodriguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM, Oddo S, Verkhratsky A (2008) Impaired adult neurogenesis in the dentate gyrus of a triple transgenic nouse model of Alzheimer's disease. PLoS One 3: e2935.
112. Schinder AF, Gage FH (2004) A hypothesis about the role of adult neurogenesis in hippocampal function. Physiology 19: 253-261.
113. Sgubin D, Aztiria E, Perin A, Longatti P, Leanza G (2007) Activation of endogenous neural stem cells in the adult human brain following subarachnoid hemorrhage. J Neurosci Res 85: 1647-1655.
114. Shen J, Xie L, Mao X, Zhou Y, Zhan R, Greenberg DA, Jin K (2008) Neurogenesis after primary intracerebral hemorrhage in adult human brain. J Cereb Blood Flow Metab 28: 1460-1468.
115. Shetty AK, Hattiangady B, Shetty GA (2005) Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51: 173-186.
116. 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: 9733-9743.
117. 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: 372-376. Erratum in: Nature 2001, 414: 938
118. Sulzer D (2010) Clues to how alpha-synuclein damages neurons in Parkinson's disease. Mov Disord 25 (Suppl 1): S27-31.
119. 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: 283-287.
120. 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: 1454-1459.
121. Tattersfield AS, 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: 319-332.
122. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O (2006) Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24: 739-747.
123. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O (2007) Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38: 3032-3039.
124. Tonchev AB, Yamashima T, Zhao L, Okano HJ, Okano H (2003a) Proliferation of neural and neuronal progenitors after global brain ischemia in young adult macaque monkeys. Mol Cell Neurosci 23: 292-301.
125. Tonchev AB, Yamashima T, Zhao L, Okano H (2003b) Differential proliferative response in the postischemic hippocampus, temporal cortex, and olfactory bulb of young adult macaque monkeys. Glia 42: 209-224.
126. Tonchev AB, Yamashima T (2006) Differential neurogenic potential of progenitor cells in dentate gyrus and CA1 sector of the postischemic adult monkey hippocampus. Exp Neurol 198: 101-113.
127. Verret L, Jankowsky JL, Xu GM, Borchelt DR, Rampon C (2007) Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J Neurosci 27: 6771-6780.
128. Walker FO (2007) Huntington's disease. Lancet 369: 218-228.
129. Winner B, Rockenstein E, Lie DC, Aigner R, Mante M, Bogdahn U, Couillard-Despres S, Masliah E, Winkler J (2008) Mutant alpha-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol Aging 29: 913-925.
130. Winner B, Desplats P, Hagl C, Klucken J, Aigner R, Ploetz S, Laemke J, Karl A, Aigner L, Masliah E, Buerger E, Winkler J (2009) Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp Neurol 219: 543-552.
131. Winner B, Kohl Z, Gage FH (2011) Neurodegenerative disease and adult neurogenesis. Eur J Neurosci 33: 1139-1151.
132. Wojcik L, Sawicka A, Rivera S, Zalewska T (2009) Neurogenesis in gerbil hippocampus following brain ischemia: focus on the involvement of metalloproteinases. Acta Neurobiol Exp(Wars) 69: 52-61.
133. Wójcik-Stanaszek L, Sypecka J, Szymczak P, Ziemka-Nalecz M, Khrestchatisky M, Rivera S, Zalewska T (2011) The potential role of metalloproteinases in neurogenesis in the gerbil hippocampus following global fore-brain ischemia. PLoS One 6: e22465.
134. Xu X, Zhang J, Chen X, Liu J, Lu H, Yang P, Xiao X, Zhao L, Jiao Q, Zhao B, Zheng P, Liu Y (2012) The increased expression of metabotropic glutamate receptor in subven-tricular zone neural progenitor cells and enhanced neurogenesis in a rat model of intracerebral hemorrhage. Neurosci 202: 474-483.
135. 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: 1890-1896.
136. Yang S, Song S, Hua Y, Nakamura T, Keep RE, Xi G (2008) Effects of thrombin on neurogenesis after intracerebral hemorrhage. Stroke 39: 2079-2084.
137. Zaruba MM, Theiss HD, Vallaster M, Mehl U, Brunner S, David R, Fischer R, Krieg L, Hirsch E, Huber B, Nathan P, Israel L, Imhof A, Herbach N, Assmann G, Wanke R, Mueller-Hoecker J, Steinbeck G, Franz WM (2009) Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell 4: 313-323.
138. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M (2001) A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50: 602-611.
139. Zhang RL, Zhang Z, Zhang L, Wang Y, Zhang C, Chopp M (2006) Delayed treatment with sildenafil enhances neurogenesis and improves functional recovery in aged rats after focal cerebral ischemia. J Neurosci Res 83: 1213-1219.
140. Zhang C, McNeil E, Dressler L, Siman R (2007) Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp Neurol 204: 77-87