Plasticity of subventricular zone neuroprogenitors in MPTP (1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine) mouse model of Parkinson'S disease involves cross talk between inflammatory and Wnt/β-catenin signaling pathways: Functional consequences for neuroprotection and repair

Journal of Neuroscience

Volumn 32, Issue 6, 2012, Pages 2062-2085

  L'Episcopo, Francesca ^a   Tirolo, Cataldo ^a   Testa, Nunzio ^a   Caniglia, Salvatore ^a   Morale, Maria C ^a   Deleidi, Michela ^b   Serapide, Maria F ^c   Pluchino, Stefano ^b,d   Marchetti, Bianca ^a,c  

^a OASI RESEARCH INSTITUTE IRCCS   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF CATANIA   (Italy)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1, 2, 3, 6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BETA CATENIN; BROXURIDINE; CASPASE 3; DOPAMINE; GLYCOGEN SYNTHASE KINASE 3BETA; MICROTUBULE ASSOCIATED PROTEIN 2; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CELL REGENERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENE SILENCING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; WESTERN BLOTTING;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; BETA CATENIN; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; RECEPTOR CROSS-TALK; STEM CELLS; WNT SIGNALING PATHWAY;

EID: 84856981228     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5259-11.2012     Document Type: Article

References (126)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R (1997) Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804.
2. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, Gotoh Y, Peltz G, Gong L, Kawase T, Alvarez-Buylla A, Okano H, Sawamoto K (2007) α-Catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25:2827-2836.
3. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z (2009) Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 29:4408-4419.
4. Allaman I, Bélanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34:76-87.
5. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2:2287-2293.
6. Baker SA, Baker KA, Hagg T (2004) Dopaminergic nigrostriatal projections regulate neural precursor cell proliferation in the adult mouse subventricular zone. Eur J Neurosci 20:575-579.
7. Barkho BZ, Song H, Aimone JB, Smrt RD, Kuwabara T, Nakashima K, Gage FH, Zhao X (2006) Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev 15:407-421.
8. Beaulieu JM, Del'guidice T, Sotnikova TD, Lemasson M, Gainetdinov RR (2011) Beyond cAMP: the regulation of Akt and GSK3 by dopamine receptors. Front Mol Neurosci 4:38.
9. Bhat RV, Shanley J, Correll MP, Fieles WE, Keith RA, Scott CW, Lee CM (2000) Regulation and localization of tyrosine 216 phosphorylation of glycogen synthase kinase-3+ in cellular and animal models of neuronal degeneration. Proc Natl Acad Sci U S A 97:11074-11079.
10. Borta A, Hoglinger GU (2007) Dopamine and adult neurogenesis. J Neurochem 100:587-595.
11. Brazas RM, Hagstrom JE (2005) Delivery of small interfering RNA to mammalian cells in culture by using cationic lipid/polymer-based transfection reagents. Methods Enzymol 392:112-124.
12. Butovsky O, Ziv Y, Schwartz A, Gennady L, Talpalar AE, Pluchino S, Martino G, Schwartz M (2006) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149-160.
13. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Hrupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264-278.
14. Castelo-Branco G, Rawal N, Arenas E (2004) GSK-3+ inhibition/α-catenin stabilization in ventral midbrain precursors increases differentiation into dopamine neurons. J Cell Sci 117:5731-5737.
15. Castelo-Branco G, Sousa KM, Bryja V, Pinto L, Wagner J, Arenas E (2006) Ventral midbrain glia express region-specific transcription factors and regulate dopaminergic neurogenesis through Wnt-5a secretion. Mol Cell Neurosci 31:251-262.
16. Chen G, Bower KA, Ma C, Ma C, Fang S, Thiele CJ, Luo J (2004) Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxy dopamineinduced neuronal death. FASEB J 18:1162-1164.
17. Chen LW, Wie LC, Qiu Y, Liu HL, Rao ZR, Ju G, Chan YS (2002) Significant up-regulation of nestin protein in the neostriatum of MPTP-treated mice. Are the striatal astrocytes regionally activated after systemic MPTP administration? Brain Res 925:9-17.
18. Chen LW, Hu JJ, Liu HL, Yung KK, Chan YS (2004) Identification of brainderived neurotrophic factor in nestin-expressing astroglial cells in the neostriatum of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mice. Neuroscience 126:941-956.
19. Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, Kan YW, Johnson JA (2009) Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte. Proc Natl Acad Sci U S A 106:2933-2938.
20. Chong ZZ, Shang YC, Hou J, Maiese K (2010) Wnt1 neuroprotection translates into improved neurological function during oxidant stress and cere-bral ischemia through AKT1 and mitochondrial apoptotic pathways. Oxid Med Cell Longev 3:153-165.
21. 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.
22. Curtis MA, Faull RLM, Eriksson PS (2007) The effect of neurodegenerative diseases on the subventricular zone. Nat Rev Neurosci 8:712-723.
23. Deleidi M, Hargus G, Hallett P, Osborn T, Isacson O (2011) Development of histocompatible primate induced pluripotent stem cells for neural transplantation. Stem Cells 29:1052-1063.
24. 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.
25. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-711.
26. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021-1034.
27. Duka T, Duka V, Joyce JN, Sidhu A (2009) α-Synuclein contributes to GSK-3+-catalyzed Tau phosphorylation in Parkinson's disease models. FASEB J 23:2820-2830.
28. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, LindvallO (2003) Inflammation is detrimental for neurogenesis in the adult brain. Proc Natl Acad Sci U S A 100:13632-13637.
29. Ekdahl CT, Kokaia Z, LindvallO (2009) Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158:1021-1029.
30. Estrada C, Murillo-CarreteroM (2005) Nitric oxide and adult neurogenesis in health and disease. Neuroscientist 11:294-307.
31. Fernando CV, Moses D, Parish CL, Tomas D, Drago J, Horne MK (2010) Creating a ventral midbrain stem cell niche in an animal model for Parkinson's disease. Stem Cells Dev 19:1995-2007.
32. Fiorucci S, Santucci L, Distrutti E (2007) NSAIDs, coxibs, CINOD andH2SreleasingNSAIDs: what lies beyond the horizon. Digest Liv Dis 39:1043-1051.
33. Freundlieb N, François C, Tandé D, Ortel WH, Hirsh EC, Hoglinger GU (2006) Dopaminergic subtantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 26:2321-2325.
34. Gallo F, Morale MC, Spina-Purrello V, Tirolo C, Testa N, Farinella Z, Avola R, Beaudet A, Marchetti B (2000a) Basic fibroblast growth factor (bFGF) acts on both neurons and glia to mediate the neurotrophic effects of astrocytes on LHRH neurons in culture. Synapse 36:233-253.
35. Gallo F, Morale MC, Tirolo C, Testa N, Farinella Z Avola R, Beaudet A Marchetti B (2000b) Basic fibroblast growth factor priming increases the responsiveness of immortalized hypothalamic luteinizing hormone releasing hormone neurones to neutrophic factors. J Neuroendocrinol 12:941-959.
36. Gao HM, Hong JS (2008) Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 29:357-365.
37. Gao HM, Liu B, Zhang W, Hong JS (2003) Critical role of microglia NADPH-oxidase-derived free radicals in the in vitro MPTP model of Parkinson's disease. FASEB J 17:1954-1966.
38. Gao HM, Kotzbauer PT, Kunihiro U, Leight S, Trojanowsski JQ, Lee VMY (2008) Neuroinflammation and oxidation/nitration of α-synuclein linked to dopaminergic neurodegeneration. J Neurosci 28:7687-7698.
39. Gennuso F, Fernetti C, Tirolo C, Testa N, L'Episcopo F, Caniglia S, Morale MC, Ostrow JD, Pascolo L, Tiribelli C, Marchetti B (2004) Bilirubin protects astrocytes from its own toxicity inducing up-regulation and translocation of multidrug resistance-associated protein 1 (Mrp 1). Proc Natl Acad Sci U S A 101:2470-2475.
40. Gordon MD, Nusse R (2006) Wnt signaling: multiple pathways, multiple receptors and multiple transcription factors. J Biol Chem 281:22429-22433.
41. Grimes CA, Jope RS (2001) The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65:391-426.
42. Gritti A, Bonfanti L, Doetsch F, Caille I, Alvarez-Buylla A, Lim DA (2002) Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 22:437-445.
43. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
44. He P, Shen Y (2009) Interruption of α-catenin signaling reduces neurogenesis in Alzheimer's disease. J Neurosci 29:6545-6557.
45. He XJ, Nakayama H, Dong M, Yamauchi H, Ueno M, Uetsuka K, Doi K (2006) Evidence of apoptosis in the subventricular zone and rostral migratory stream in the MPTP mouse model of Parkinson disease. J Neuropathol Exp Neurol 65:873-882.
46. Hermann A, Storch A (2008) Endogenous regeneration in Parkinson's disease: do we need orthotopic dopaminergic neurogenesis? Stem Cells 26:2749-2752.
47. Hirsch EC, Hunot S (2009) Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol 8:382-397.
48. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch E (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726-735.
49. Hu X, Zhang D, Pang H, Caudle WM, Li Y, Gao H, Liu Y, Qian L, Wilson B, Di Monte DA, Ali SF, Zhang J, Block ML, Hong JS (2008) Macrophage antigen complex-1 mediates reactive microgliosis and progressive dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. J Immunol 181:7194-7204.
50. Inestrosa NC, Arenas E (2010) Emerging role of Wnts in the adult nervous system. Nat Rev Neurosci 11:77-86.
51. Jackson-Lewis V, Przedborski S (2007) Protocol for the MPTP model of Parkinson's disease. Nat Protoc 2:141-151.
52. Jakubs K, Bonde S, Iosif RE, Ekdahl CT, Kokaia Z, Kopkaia M, Lindvall O (2008) Inflammation regulates functional integration of neurons born in adult brain. J Neurosci 28:12477-12488.
53. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F (2002) Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172-1183.
54. Jiao J, Chen DF (2008) Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyteproduced signals. Stem Cells 26:1221-1230.
55. Jin T, Fantus IG, Sun J (2008) Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of α-catenin. Cell Signal 20:1697-1704.
56. Kalani MYS, Cheshir SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R (2008) Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci U S A 105:16970-16975.
57. Kazanis I (2009) 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 132:2909-2921.
58. Keeble JE, Moore PK (2002) Pharmacology and potential therapeutic applications of nitric oxide-releasing non-steroidal anti-inflammatory and related nitric oxide-donating drugs. Br J Pharmacol 137:295-340.
59. Kim H, Won S, Hwang DY, Lee J, Kim M, Kim R, Kim W, Cha B, Kim T, Kim D, Costantini F, Jho E (2010) Downregulation of Wnt/+-catenin signaling causes degeneration of hippocampal neurons in vivo. Neurobiol Aging 32:2316.
60. King TD, Bijur GN, Jope RS (2001) Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3+ and attenuated by lithium. Brain Res 919:106-114.
61. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
62. Kuwabara T, Hsieh J, Muotri A, Yeo G, Warashira M, Lie DC, Moore L, Nakashima K, Asashima M, Gage FH (2009) Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci 12:1097-1105.
63. Lennington JB, Pope S, Goodheart AE, Drozdowicz L, Daniels SB, Salamone JD, Conover JC (2011) Midbrain dopamine neurons associated with reward processing innervate the neurogenic subventricular zone. J Neurosci 31:13078-13087.
64. L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Marchetti B (2010a) Glia as a turning point in the therapeutic strategy of Parkinson's disease. CNS Neurol Disord 9:349-372.
65. L'Episcopo F, Tirolo C, Caniglia S, Testa N, Serra PA, Impagnatiello F, Morale MC, Marchetti B (2010b) Combining nitric oxide release with antiinflammatory activity preserves nigrostriatal dopaminergic innervation and prevents motor impairment in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J Neuroinflamm 7:83.
66. L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Cossetti C, D'Adamo P, Zardini E, Andreoni L. Ihekwaba AE, Serra PA, Franciotta D, Martino G, Pluchino S, Marchetti B (2011a) Reactive astrocytes and Wnt/betacatenin signaling link nigrostriatal injury to repair in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Neurobiol Dis 41:508-527.
67. L'Episcopo F, Serapide MF, Tirolo C, Testa N, Caniglia S, Morale MC, Pluchino S, Marchetti B (2011b) A Wnt1 regulated frizzled-1/β-catenin signaling pathway as a candidate regulatory circuit controlling mesencephalic dopaminergic neuron-astrocyte crosstalk: therapeutical relevance for neuron survival and neuroprotection. Mol Neurodegener 6:49.
68. L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Impagniatiello F, Marchetti B (2011c) Switching microglial harmful phenotype promotes life-long restoration of Substantia Nigra dopaminergic neurons from inflammatory neurodegeneration in aged mice. Rejuv Res 14:411-424.
69. Lie DC, Colamarino SA, Song HG, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Diarie AR, Gage FH (2005) Wnt signaling regulates adult hippocampal neurogenesis. Nature 473:1370-1375.
70. Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci U S A 96:7526-7531.
71. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810.
72. Magistretti PJ (2006) Neuron-glia metabolic coupling and plasticity. J Exp Biol 209:2304-2311.
73. Maiese K, Faqi L, Chong ZZ, Chen SY (2008) The Wnt signalling pathway: aging gracefully as a protectionist? Pharmacol Ther 118:58-81.
74. Mander P, BrownG (2005) Activation of microglialNADPHoxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual key mechanism of inflammatory degeneration. J Neuroinflamm 2:20-27.
75. Mao L, Lau YS, Petroske E, Wan JQ (2001) Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration. Dev Brain Res 131:57-65.
76. Marchetti B, AbbracchioMP (2005) To be or not to be (inflamed) is that the question in anti-inflammatory drug therapy of neurodegenerative diseases? Trends Pharmacol Sci 26:517-525.
77. Marchetti B, Morale MC, Brouwer J, Tirolo C, Testa N, Caniglia S, Barden N, Amor S, Smith PA, Dijkstra CD (2002) Exposure to a dysfunctional glucocorticoid receptor from early embryonic life programs the resistance to experimental autoimmune encephalomyelitis via nitric oxide-induced immunosuppression. J Immunol 168:5848-5859.
78. Marchetti B, Kettenmann H, Streit WJ (2005a) Glia-neuron crosstalk in neuroinflammation, neurodegeneration and neuroprotection. Brain Res Rev 48:129-132.
79. Marchetti B, Serra PA, Tirolo C, L'Episcopo F, Caniglia S, Gennuso F, Testa N, Miele E, Desole MS, Barden N, Morale MC (2005b) Glucocorticoid receptor-nitric oxide crosstalk and vulnerability to experimental Parkinsonism: pivotal role for glia-neuron interactions. Brain Res Rev 48:302-321.
80. Matarredona ER, Murillo-Carretero M, Moreno-Lopez B, Estrada C (2004) Nitric oxide synthesis inhibition increases proliferation of neural precursors isolated from the postnatal mouse subventricular zone. Brain Res 995:274-284.
81. Matarredona ER, Murillo-Carretero M, Moreno-López B, Estrada C (2005) Role of nitric oxide in subventricular zone neurogenesis. Brain Res Brain Res Rev 2005 49:355-366.
82. Mohapel P, Frielingsdorf H, Haggblad J, Zachrisson O, Brundin P (2005) Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience 132:767-776.
83. Moncada S, Bolanos JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97:1676-1689.
84. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
85. Morale MC, Serra P, Delogu MR, Migheli R, Rocchitta G, Tirolo C, Caniglia S, Testa N, L'Episcopo F, Gennuso F, Scoto GM, Barden N, Miele E, Desole MS, Marchetti B (2004) Glucocorticoid receptor deficiency increases vulnerability of the nigrostriatal dopaminergic system: critical role of glial nitric oxide. FASEB J 18:164-166.
86. Morale MC, Serra PA, L'Episcopo F, Tirolo C, Caniglia S, Testa N, Gennuso F, Giaquinta G, Rocchitta G, Desole MS, Miele E, Marchetti B (2006) Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 138:869-878.
87. Moreno-López 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.
88. Morshead CM, van der Kooy D (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249-256.
89. MorsheadCM, Reynolds BA, Craig CG, McBurneyMW, StainesWA, Morassutti D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
90. Munji RN, Choe Y, Li G, Siegenthaler JA, Pleasure SJ (2011) Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J Neurosci 31:1676-1687.
91. Nair VD, OlanowCW (2008) Differential modulation of Akt/glycogen synthase kinase-3beta pathway regulates apoptotic and cytoprotective signalling responses. J Biol Chem 283:15469-15478.
92. Oieda L, Gao J, Hooten KG, Wang E, Thonhoff JR, Dunn TJ, Gao T Wu P (2011) Critical role of Pl3K/Akt/GSK3+ in motoneuron specification from human neural stem cells in response to FGF2 and EGF. PLoS One 6:e23414.
93. O'Keeffe GO, Barker RA, Caldwell MA (2009a) Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 8:18.
94. O'Keeffe GO, Tyers P, Aarsland D, Dalley JW, Barker RA, Caldwell MA (2009b) Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proc Natl Acad Sci U S A U S A 106:8754-8759.
95. Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M (2007) Wnt signalling promotes regeneration in the retina of adult mammals. J Neurosci 27:4210-4219.
96. Ouredinik VC, Ourednik J, Xu Y, Zhang Y, Lynch WP, Snyder EY, Schachner M (2009) Cross-talk between stem cells and the dysfunctional brain is facilitated by manipulating the niche: evidence from an adhesion molecule. Stem cells 27:2846-2856.
97. 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 U S A 100:9566-9571.
98. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, Ed 3. San Diego: Academic.
99. Petit-Paitel A, Brau F, Cazareth J, Chabry J (2009) Involment of cytosolic and mitochondrial GSK-3beta in mitochondrial dysfunction and neuronal cell death of MPTP/MPPβ-treated neurons. PLoS One 4:e5491.
100. Phukan S, Babu VS, Kannoji A, Hariharan R, Balaji VN (2010) GSK3beta: role in therapeutic landscape and development of modulators. Br J Pharmacol 160:1-19.
101. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, MartinoG (2003) Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422:688-694.
102. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, Martinello M, Cattalini A, Bergami A, Furlan R, Comi G, Costantin G, Martino G (2005) Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436:266-271.
103. Pluchino S, Muzio L, Imitola J, Deleidi M, Alfaro-Cervello C, Salani G, Porcheri C, Brambilla E, Cavasinni F, Bergamaschi A, Garcia-Verdugo JM, Comi G, Khoury SJ, Martino G (2008) Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain 131:2564-2578.
104. Prakash N, Brodski C, Naserke T, Puelles E, Gogoi R, Hall A, Panhuysen M, Echevarria D, Sussel L, Vogt Weisenhorn DM, Martinez S, Arenas E, Simeone A, Wurst W (2006) A Wnt1-regulated genetic network controls the identity and fate of midbrain-dopaminergic progenitors in vivo. Development 133:89-98.
105. Rietze RL, Reynolds BA (2006) Neural stem cell isolation and characterization. Methods Enzymol 419:3-23.
106. Sandhu JK, Gardaneh M, Iwasiow R, Lanthier P, Gangaraju S, Ribecco-Lutkiewicz M, Tremblay R, Kiuchi K, Sikorska M (2009) Astrocytesecreted GDNF and glutathione antioxidant system protect neurons against 6OHDA cytotoxicity. Neurobiol Dis 33:405-414.
107. Schwartz M, London A, Shecter R (2009) Boosting T-cell immunity as a therapeutic approach for neurodegenerative conditions: the role of innate immunity. Neuroscience 158:1133-1142.
108. Semënov MV, Tamai K, Brott BK, Kühl M, Sokol S, He X (2001) Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr Biol 11:951-961.
109. Shibui Y, He XJ, Uchida K, Nakayama H (2009) MPTP-induced neuroblast apoptosis in the subventricular zone is not regulated by dopamine or other monoamine transporters. Neurotoxicology 30:1036-1044.
110. Shimogori T, VanSant J, Paik E, Grove EA (2004) Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. J Comp Neurol 473:496-510.
111. Shruster A, Eldar-Finkelman H, Melamed E, Offen D (2011) Wnt signaling pathway overcomes the disruption of neuronal differentiation of neural progenitor cells induced by oligomeric amyloid α-peptide. J Neurochem 116:522-529.
112. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44.
113. Spiegel A, Shivtiel S, Kalinkovich A, Ludin A, Netzer N, Goichberg P, Azaria Y, Resnick I, Hardan I, Ben-Hur H, Nagler A, Rubinstein m, Lapidot T (2007) Catecholaminergic neurotransmitters regulate migration and repopulation of immature human CD34+ cells through Wnt signaling. Nat Immunol 8:1123-1131.
114. Tandé D, Hoglinger GU, Debeir T, Freundlieb N, Hirsch EC, Francois C (2006) New striatal dopamine neurons in MPTP-treated macaques result from a phenotypic shift not neurogenesis. Brain 129:1194-1200.
115. Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J, Nygren JM, Jacobsen SE, Ekdahl CT, Kokaia Z, LindvallO (2009) Longterm accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57:835-849.
116. Toledo EM, Clombres M, Inestrosa NC (2008) Wnt signaling in neuroprotection and stem cell differentiation. Progr Neurobiol 88:281-296.
117. Torroglosa A, Murillo-Carretero M, Romero-Grimaldi C, Matarredona ER, Campos-Caro A, Estrada C (2007) Nitric oxide decreases subventricular zone stem cell proliferation by inhibition of epidermal growth factor receptor and phosphoinositide-3-kinase/Akt pathway. Stem Cells 25:88-97.
118. Trowbridge JJ, Xenocostas A, Moon RT, Bhatia M (2006) Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat Med 12:89-98.
119. van Kampen RM, Hagg T, Robertson HA (2004) Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D receptor stimulation. Eur J Neurosci 19:2377-2387.
120. Wang W, Yang Y, Ying C, Li W, Ruan H, Zhu X, You Y, Han Y, Chen R, Wang Y, Li M (2007) Inhibition of glycogen synthase kinase-3+ protects dopaminergic neurons from MPTP toxicity. Neuropharmacology 52:1678-1684.
121. Wexler EM, Geschwind DH, Palmer TD (2008) Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation Mol Psychiatry 13:285-292.
122. 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.
123. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulus H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771.
124. Zhang L, Yang X, Yang S, Zhang J (2011) The Wnt/β-catenin signaling pathway in the adult neurogenesis. Eur J Neurosci 33:1-8.
125. Zhang QG, Wang R, Khan M, Maesh V, Brann DW (2008) Role of Dikkopf-1 (Dkk1), an antagonist of the Wnt-β-catenin signaling pathway, in estrogen-induced neuroprotection and attenuation of Tau phosphorylation. J Neurosci 28:8430-8441.
126. Zhang YJ, Xu YF, Liu YH, Yin J, Wang JZ (2005) Nitric oxide induces tau hyperphosphorylation via glycogen synthase kinase-3beta activation. FEBS Lett 579:6230-6236.