Wnt/β-catenin signaling is required to rescue midbrain dopaminergic progenitors and promote neurorepair in ageing mouse model of Parkinson's disease

Stem Cells

Volumn 32, Issue 8, 2014, Pages 2147-2163

  L'Episcopo, Francesca ^a   Tirolo, Cataldo ^a   Testa, Nunzio ^a   Caniglia, Salvatore ^a   Morale, Maria Concetta ^a   Serapide, Maria Francesca ^b   Pluchino, Stefano ^c   Marchetti, Bianca ^a,b  

^a OASI RESEARCH INSTITUTE IRCCS   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adult stem neuroprogenitors; Aging; Dopaminergic plasticity; Neuroprotection; Neurorepair; Parkinson's disease; Wnt catenin signaling

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; NEURITE PROMOTING FACTOR; WNT PROTEIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONOGENESIS; COCULTURE; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MALE; MESENCEPHALON; MOUSE; MULTIPOTENT STEM CELL; NERVE FIBER REGENERATION; NERVE INJURY; NEURAL STEM CELL; NONHUMAN; PARKINSON DISEASE; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DOPAMINERGIC NERVE CELL; GLIA; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

AGING; ANIMALS; BLOTTING, WESTERN; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; PARKINSON DISEASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY;

EID: 84904438586     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1708     Document Type: Article

References (83)

1. Di Monte DA, Langston J.W,. Idiopathic and 1-methyl-4phenyl-1,2,3,6- tetrahydropyridine (MPTP)-induced Parkinsonism. In:, Kettenmann H, Ransom BR, eds. Neuroglia, Chapter 65. Oxford: Oxford University Press, 1995: 989-997.
2. Olanow CV, Schapira AH,. Therapeutic prospects for Parkinson disease. Ann Neurol 2013; 74: 337-347.
3. Politis M, Lindvall O,. Clinical application of stem cell therapy in Parkinson's disease. BMC Med 2012; 10: 1.
4. Hermann A, Storch A,. Induced neural stem cells (iNSCs) in neurodegenerative diseases. J Neural Transm 2013; 120 (suppl 1): S19-25.
5. Ali F, Stott SR, Barker RA,. Stem cells and the treatment of Parkinson's disease. Exp Neurol 2013, pii: S0014-4886 (13)00004-6.
6. Prakash N, Wurst W,. Wnt1-regulated genetic networks in midbrain dopaminergic neuron development. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 34-41.
7. Castelo-Branco G, Rawal N, Arenas E,. GSK-3β inhibition/β- catenin stabilization in ventral midbrain precursors increases differentiation into dopamine neurons. J Cell Sci 2004; 11: 5731-5737.
8. Castelo-Branco G, Sousa KM, Bryja V, et al. Ventral midbrain glia express region-specific transcription factors and regulate dopaminergic neurogenesis through Wnt-5a secretion. Mol Cell Neurosci 2006; 31: 251-262.
9. Parish CL, Lachlan H, Thompson LH,. Modulating Wnt signaling to improve cell replacement therapy for Parkinson's disease. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 54-63.
10. Joksimovic M, Awatramani R,. Wnt/β-catenin signaling in midbrain dopaminergic neuron specification and neurogenesis. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 27-33.
11. Kriks S, Shim JW, Piao J, et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011; 480: 547-551.
12. Kirkeby A, Grealish S, Wolf DA, et al. Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Rep 2012; 1: 703-714.
13. Arenas E,. Wnt signaling in midbrain dopamine neuron development and Regenerative medicine for Parkinson's disease. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 42-53.
14. Blakely BD, Bye CR, Fernando CV, et al. Ryk, a receptor regulating Wnt5a-mediated neurogenesis and axon morphogenesis of ventral midbrain dopaminergic neurons. Stem Cells Dev 2013; 22: 2132-2144.
15. Clevers H, Nusse R,. Wnt/beta-catenin signaling and disease. Cell 2012; 149: 1192-1205.
16. Inestrosa NC, Varela-Nallar L,. Wnt signalling in the nervous system and in Alzheimer's disease. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 64-74.
17. Purro SA, Galli S, Salinas PC,. Dysfunction of Wnt signaling and synaptic disassembly in neurodegenerative diseases. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 75-80.
18. Harvey K, Marchetti B,. Regulating Wnt signalling, a strategy to prevent neurodegeneration and induce regeneration. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 1-2.
19. Berwick DC, Harvey K,. The regulation and deregulation of Wnt signalling by PARK genes in health and disease. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 3-12.
20. L'Episcopo F, Tirolo C, Testa N, et al. Reactive astrocytes and Wnt/β-catenin signaling link nigrostriatal injury to repair in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Neurobiol Dis 2011; 41: 508-527.
21. L'Episcopo F, Serapide MF, Tirolo C, et al. 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 Neurodegen 2011; 13: 6-49.
22. L'Episcopo F, Tirolo C, Testa N, et al. Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model of Parkinson's disease involves crosstalk between inflammatory and Wnt/β-catenin signaling pathways: Functional consequences for neuroprotection and repair. J Neurosci 2012; 32: 2062-2085.
23. Berwick DC, Harvey K,. LRRK2 functions as a Wnt signaling scaffold, bridging cytosolic proteins and membrane-localized LRP6. Hum Mol Genet 2012; 21: 4966-4979.
24. Gollamudi S, Johri A, Calingasan NY, et al. Concordant signaling pathways produced by pesticide exposure in mice correspond to pathways identified in human Parkinson's disease. PLoS One 2012; 7: e36191.
25. Marchetti B, L'Episcopo F, Morale MC, et al. Uncovering novel actors in astrocyte-neuron crosstalk in Parkinson's disease: the Wnt/β-catenin signaling cascade as the common final pathway for neuroprotection and self-repair. Eur J Neurosci 2013; 37: 1550-1563.
26. Bezard E, Gross CE,. Compensatory mechanisms in experimental and human parkinsonism: Towards a dynamic approach. Prog Neurobiol 1998; 55: 93-116.
27. Hornykiewicz O,. Parkinson's disease and the adaptive capacity of the nigrostriatal dopamine system: Possible neurochemical mechanisms. Adv Neurol 1993; 60: 140-147.
28. Collier TJ, Lipton J, Daley BF, et al. Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: Diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol Dis 2007; 26: 56-65.
29. Borta A, Holinger GU,. Dopamine and adult neurogenesis. J Neurochem 2007; 100: 587-595.
30. O'Keeffe GO, Barker RA, Caldwell MA,. Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 2009; 8: 18.
31. Winner B, Desplats P, Hagl C, et al. Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp Neurol 2009; 219: 543-552.
32. Winner B, Vogt-Weisenhorn DM, Chichung D, et al. Cellular repair strategies in Parkinson's disease. Adv Neurol Disord 2009; 2: 51-60.
33. L'Episcopo F, Tirolo C, Testa N, et al. Aging-induced Nrf2-ARE pathway disruption in the subventricular zone (SVZ) drives neurogenic impairment in parkinsonian mice via PI3K-Wnt/β-catenin dysregulation. J Neurosci 2013; 33: 1462-1485.
34. Alvarez-Builla A, Garcia-Verdugo JM, Tramontin AD,. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2: 2287-2293.
35. Song H, Stevens CF, Gage FH,. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002; 417: 39-44.
36. Lim DA, Alvarez-Buylla A,. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. PNAS USA 1999; 96: 7526-7531.
37. Fuentealba LC, Obernier K, Alvarez-Buylla A,. Adult neural stem cells bridge their niche. Cell Stem Cell 2012; 10: 698-708.
38. Lie DC, Colamarino SA, Song HG, et al. Wnt signaling regulates adult hippocampal neurogenesis. Nature 2005; 473: 1370-1375.
39. Adachi K, Mirzadeh Z, Sakaguchi M, et al. β-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 2007; 25: 2827-2836.
40. Kuwabara T, Hsieh J, Muotri A, et al. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci 2009; 12: 1097-1105.
41. Okamoto M, Inoue K, Iwamura H, et al. Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis. Faseb J 2011; 25: 3570-3582.
42. Seib DRM, Corsini NS, Ellwanger K, et al. Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 2013; 12: 204-214.
43. Lie DC, Dziewczapolski G, Willhoite AR, et al. The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 2002; 22: 6639-6649.
44. Hermann A, Storch A,. Endogenous regeneration in Parkinson's disease: Do we need orthotopic dopaminergic neurogenesis? Stem Cells 2008; 26: 2749-2752.
45. Hermann A, Maisel M, Wegner F, et al. Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 2006; 24: 949-964.
46. Hermann A, Suess C, Fauser M, et al. Rostro-caudal loss of cellular diversity within the periventricular regions of the ventricular system. Stem Cells 2009; 27: 928-941.
47. Meyer AK, Maisel M, Hermann A, et al. Restorative approaches in Parkinson's disease: Which cell type wins the race? J Neurol Sci 2010; 289: 93-103.
48. Hokfelt T, Martensson R, Bjorklund A, et al. Distributional maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In:, Bjorklund A, Hokfelt T, eds. Classical Transmitters in the CNS, part I. Handbook of Chemical Neuroanatomy. Vol 2. Amsterdam: Elsevier, 1984: 277-379.
49. Kawano H, Ohyama K, Kawamura K, et al. Migration of dopaminergic neurons in the embryonic mesencephalon of mice. Brain Res Dev Brain Res 1995; 86: 101-113.
50. Maretto S, Cordenonsi M, Dupont S, et al. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. PNAS 2003; 100: 3299-3304.
51. Jackson-Lewis V, Przedborski S,. Protocol for the MPTP model of Parkinson's disease. Nat Prot 2007; 2: 141-151.
52. Pluchino S, Zanotti L, Rossi B, et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005; 436: 266-271.
53. Franklin KBJ, Paxinos G,. The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press, Inc., 1997.
54. Morale MC, Serra PA, Delogu MR, et al. Glucocorticoid receptor deficiency increases vulnerability of the nigrostriatal dopaminergic system: critical role of glial nitric oxide. FASEB J 2004; 18: 164-166.
55. Gordon MD, Nusse R,. Wnt signaling: Multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006; 281: 22429-22433.
56. Lustig B, Jerchow, B, Sachs, M, et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 2002; 22: 1184-1193.
57. Osakada F, Ooto S, Akagi T, et al. Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 2007; 27: 4210-4219.
58. Kalani MHS, Chschier SH, Cord BJ, et al. Wnt-mediated self-renewal of neural stem/progenitor cells. PNAS 2008; 105: 16070-16075.
59. Yoshimi K, Ren YR, Seki T, et al. Possibility for neurogenesis in substantia nigra of parkinsonian brain. Ann Neurol 2005; 58: 31-40.
60. White BD, Nathe RJ, Maris DO, et al. β-Catenin signaling increases in proliferating NG2+ progenitors and astrocytes during post-traumatic gliogenesis in the adult brain. Stem Cell 2010; 28: 297-307.
61. Tang M, Miyamoto Y, Huang EJ,. Multiple roles of β-catenin in controlling the neurogenic niche for midbrain dopamine neurons. Develop 2009; 136: 2027-2038.
62. Tang M, Villaescusa JC, Luo SX, et al. Interactions of Wnt/beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci 2010; 7: 9280-9291.
63. Kitagua H, Ray WJ, Glantsching H, et al. A regulatory circuit mediating convergence between Nurr1 transcriptional regulation and Wnt signalling. Mol Cell Biol 2007; 27: 7486-7496.
64. Wang S, Okun MS, Suslov O, et al. Neurogenic potential of progenitor cells isolated from postmortem human Parkinsonian brains. Brain Res 2012; 1464: 61-72.
65. Martens DJ, Seaberg RM, van der Kooy D,. In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur J Neurosci 2002; 16: 1045-1057.
66. Pluchino S, Muzio L, Imitola J, et al. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain 2008; 131: 2564-2578.
67. Ekdahl CT, Kokaia Z, Lindvall O,. Brain inflammation and adult neurogenesis: The dual role of microglia. Neuroscience 2009; 158: 1021-1029.
68. Marchetti B, Pluchino S,. Wnt your brain be inflamed? Yes, it Wnt! Trends Mol Med 2013; 19: 144-156.
69. L'Episcopo F, Tirolo C, Caniglia S, et al. Targeting Wnt signaling at the neuroimmune interface in dopaminergic neuroreprotection/repair in Parkinson's disease. In "Wnt signaling cascades in neurodevelopment, neurodegeneration and regeneration". J Mol Cell Biol 2014; 6: 13-26.
70. Bonilla S, Hall AC, Pinto L, et al. Identification of midbrain floor plate radial glia-like cells as dopaminergic progenitors. Glia 2008; 56: 809-820.
71. Kadkhodaei B, Ito T, Joodmardi E, et al. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J Neurosci 2009; 29: 15923-15932.
72. Duka T, Duka V, Joyce JN, et al. α-Synuclein contributes to GSK-3β-catalyzed Tau phosphorylation in Parkinson's disease models. Faseb J 2009; 23: 2820-2830.
73. Petit-Paitel A, Brau F, Cazareth J, et al. Involvement of cytosolic and mitochondrial GSK-3beta in mitochondrial dysfunction and neuronal cell death of MPTP/Mpp+-treated neurons. PLoS One 2009; 4: e5491.
74. Wang W, Yang Y, Ying C, et al. Inhibition of glycogen synthase kinase-3β protects dopaminergic neurons from MPTP toxicity. Neuropharmacology 2007; 52: 1678-1684.
75. Sirerol-Piquer M, Gomez-Ramos P, Hernández F, et al. GSK3β overexpression induces neuronal death and a depletion of the neurogenic niches in the dentate gyrus. Hippocampus 2011; 21: 910-922.
76. Diaz-Ruiz O, Zhang YJ, Shan F, et al. Attenuated response to methamphetamine sensitization and deficits in motor learning and memory after selective deletion of β-catenin in dopamine neurons. Learn Mem 2012; 19: 341-350.
77. Klaissle P, Lesemann A, Huehnchen P, et al. Physical activity and environmental enrichment regulate the generation of neural precursors in the adult mouse substantia nigra in a dopamine-dependent manner. BMC Neurosi 2012; 13: 132.
78. Esfandiari F, Fathi A, Gourabi H, et al. Glycogen synthase kinase-3 inhibition promotes proliferation and neuronal differentiation of human-induced pluripotent stem cell-derived neural progenitors. Stem Cells Dev 2012; 21: 3233-3243.
79. Kokaia Z, Martino G, Schwartz M, et al. Cross-talk between neural stem cells and immune cells: the key to better brain repair? Nat Neurosci 2012; 15: 1078-1087.
80. Srikanth M, Kessler JA,. Nanotechnology-novel therapeutics for CNS disorders. Nat Rev Neurol 2012; 8: 307-318.
81. Sundberg M, Bogetofte H, Lawson T, et al. Improved cell therapy protocols for Parkinson's disease based on differentiation efficiency and safety of hESC, hiPSC-, and non-human primate iPSC-derived dopaminergic neurons. Stem Cells 2013; 31: 1548-1562.
82. Lian X, Zhang J, Azarin SM, et al. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc 2013; 8: 162-175.
83. Zhao WN, Cheng C, Theriault KM, et al. A high-throughput screen for Wnt/β-catenin signaling pathway modulators in human iPSC-derived neural progenitors. J Biomol Screen 2012; 17: 1252-1263.