Canonical and noncanonical Wnt signaling in neural stem/progenitor cells

Cellular and Molecular Life Sciences

Volumn 72, Issue 21, 2015, Pages 4157-4172

  Bengoa Vergniory, Nora ^a,c   Kypta, Robert M ^a,b  

^a CIC BIOGUNE   (Spain)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

AP 1 family transcription factors; Beta catenin; Neural stem cells; Wnt signaling

Indexed keywords

BETA CATENIN; STRESS ACTIVATED PROTEIN KINASE; WNT3A PROTEIN; WNT PROTEIN;

AGING; BRAIN DEVELOPMENT; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HIPPOCAMPUS; HUMAN; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM CELL; NONHUMAN; PLURIPOTENT STEM CELL; REVIEW; STEM CELL CULTURE; STEM CELL TRANSPLANTATION; SUBVENTRICULAR ZONE; WNT SIGNALING PATHWAY; ANIMAL; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PHYSIOLOGY; STEM CELL;

ANIMALS; BRAIN; CELL DIFFERENTIATION; HUMANS; MICE; NEURAL STEM CELLS; NEUROGENESIS; STEM CELLS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84944147101     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-2028-6     Document Type: Review

References (182)

1. MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26. doi: 10.1016/j.devcel.2009.06.016
2. Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149:1192-1205. doi: 10.1016/j.cell.2012.05.012
3. Niehrs C (2012) The complex world of WNT receptor signalling. Nat Rev Mol Cell Biol 13:767-779. doi: 10.1038/nrm3470
4. Li VSW, Ng SS, Boersema PJ et al (2012) Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 149:1245-1256. doi: 10.1016/j.cell.2012.05.002
5. Kawano Y, Kypta R (2003) Secreted antagonists of the Wnt signalling pathway. J Cell Sci 116:2627-2634. doi: 10.1242/jcs.00623
6. Xavier CP, Melikova M, Chuman Y et al (2014) Secreted Frizzled-related protein potentiation versus inhibition of Wnt3a/β-catenin signaling. Cell Signal 26:94-101. doi: 10.1016/j.cellsig.2013.09.016
7. Satoh S, Daigo Y, Furukawa Y et al (2000) AXIN1 mutations in hepatocellular carcinomas, and growth suppression. Nat Genet 24:245-250
8. Lammi L, Arte S, Somer M et al (2004) Mutations in AXIN2 cause familial tooth agenesis and predispose to colorectal cancer. Am J Hum Genet 74:1043-1050. doi: 10.1086/386293
9. Nishisho I, Nakamura Y, Miyoshi Y et al (1991) Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 253:665-669. doi: 10.1126/science.1651563
10. Morin PJ, Sparks AB, Korinek V et al (1997) Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 275:1787-1790. doi: 10.1126/science.275.5307.1787
11. Takeda H, Lyle S, Lazar AJF et al (2006) Human sebaceous tumors harbor inactivating mutations in LEF1. Nat Med 12:395-397
12. Bass AJ, Lawrence MS, Brace LE et al (2011) Genomic sequencing of colorectal adenocarcinomas identifies a recurrent VTI1A-TCF7L2 fusion. Nat Genet 43:964-968
13. Chen B, Dodge ME, Tang W et al (2009) Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 5:100-107
14. Proffitt K, Madan B, Ke Z et al (2013) Pharmacological inhibition of the Wnt acyltransferase PORCN prevents growth of WNT-driven mammary cancer. Cancer Res 73:502-507
15. Huang S-M, Mishina YM, Liu S et al (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461:614-620. doi: 10.1038/nature08356
16. Sato N, Meijer L, Skaltsounis L et al (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10:55-63. doi: 10.1038/nm979
17. Gonsalves FC, Klein K, Carson BB et al (2011) An RNAi-based chemical genetic screen identifies three small-molecule inhibitors of the Wnt/wingless signaling pathway. Proc Natl Acad Sci 108:5954-5963
18. Van Amerongen R, Nusse R (2009) Towards an integrated view of Wnt signaling in development. Development 136:3205-3214
19. Gómez-Orte E, Sáenz-Narciso B, Moreno S, Cabello J (2013) Multiple functions of the noncanonical Wnt pathway. Trends Genet 29:545-553. doi: 10.1016/j.tig.2013.06.003
20. Lopez-Bergami P, Lau E, Ronai Z (2010) Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat Rev Cancer 10:65-76
21. Kohn AD, Moon RT (2005) Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38:439-446
22. Rao TP, Kühl M (2010) An updated overview on Wnt signaling pathways: a prelude for more. Circ Res 106:1798-1806. doi: 10.1161/CIRCRESAHA.110.219840
23. 2+ signaling pathway: a brief overview. Acta Biochim Biophys Sin 43:745-756. doi: 10.1093/abbs/gmr079
24. Clark CEJ, Nourse CC, Cooper HM (2012) The tangled web of non-canonical Wnt signalling in neural migration. Neurosignals 20:202-220. doi: 10.1159/000332153
25. Yu H, Ye X, Guo N, Nathans J (2012) Frizzled 2 and frizzled 7 function redundantly in convergent extension and closure of the ventricular septum and palate: evidence for a network of interacting genes. Development 139:4383-4394
26. Najdi R, Proffitt K, Sprowl S et al (2012) A uniform human Wnt expression library reveals a shared secretory pathway and unique signaling activities. Differ Res Biol Divers 84:203-213. doi: 10.1016/j.diff.2012.06.004
27. Schambony A, Wedlich D (2007) Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev Cell 12:779-792. doi: 10.1016/j.devcel.2007.02.016
28. Liu Y, Rubin B, Bodine PVN, Billiard J (2008) Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J Cell Biochem 105:497-502. doi: 10.1002/jcb.21848
29. Zhang S, Chen L, Cui B et al (2012) ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. PLoS ONE 7:e31127. doi: 10.1371/journal.pone.0031127
30. Acebron SP, Karaulanov E, Berger BS et al (2014) Mitotic wnt signaling promotes protein stabilization and regulates cell size. Mol Cell 54:663-674. doi: 10.1016/j.molcel.2014.04.014
31. Grumolato L, Liu G, Mong P et al (2010) Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev
32. Sato A, Yamamoto H, Sakane H et al (2010) Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J 29:41-54. doi: 10.1038/emboj.2009.322
33. Janda CY, Waghray D, Levin AM et al (2012) Structural basis of Wnt recognition by Frizzled. Science 337:59-64. doi: 10.1126/science.1222879
34. Aimone JB, Deng W, Gage FH (2010) Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci 14:325-337
35. Nusse R (2008) Wnt signaling and stem cell control. Cell Res 18:523-527. doi: 10.1038/cr.2008.47
36. Young F, Sloan A, Song B (2013) Dental pulp stem cells and their potential roles in central nervous system regeneration and repair. J Neurosci Res 91:1383-1393. doi: 10.1002/jnr.23250
37. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612-613
38. Florio M, Huttner WB (2014) Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141:2182-2194. doi: 10.1242/dev.090571
39. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788. doi: 10.1038/nrm1739
40. Bartolini G, Ciceri G, Marín O (2013) Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults. Neuron 79:849-864. doi: 10.1016/j.neuron.2013.08.014
41. Bielen H, Houart C (2014) The Wnt cries many: Wnt regulation of neurogenesis through tissue patterning, proliferation, and asymmetric cell division. Dev Neurobiol 74:772-780. doi: 10.1002/dneu.22168
42. Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457-467
43. Munji RN, Choe Y, Li G et al (2011) Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J Neurosci 31:1676-1687. doi: 10.1523/JNEUROSCI.5404-10.2011
44. Pino D, Choe Y, Pleasure SJ (2011) Wnt5a controls neurite development in olfactory bulb interneurons. Am Soc Neurochem 3:125-133. doi: 10.1042/AN20100038
45. Blakely BD, Bye CR, Fernando CV et al (2011) Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS ONE 6:e18373. doi: 10.1371/journal.pone.0018373
46. Hall AC, Lucas FR, Salinas PC et al (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535
47. Fernando CV, Kele J, Bye CR et al (2014) Diverse roles for Wnt7a in ventral midbrain neurogenesis and dopaminergic axon morphogenesis. Stem Cells Dev 23:1991-2003
48. 2+/calmodulin-dependent protein kinase II. Proc Natl Acad Sci. doi: 10.1073/pnas.1018132108
49. Many AM, Brown AMC (2014) Both canonical and non-canonical Wnt signaling independently promote stem cell growth in mammospheres. PLoS ONE 9:e101800. doi: 10.1371/journal.pone.0101800
50. Davis EK, Zou Y, Ghosh A (2008) Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocampal synapse formation. Neural Dev 3:32. doi: 10.1186/1749-8104-3-32
51. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC (2005) Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34-42. doi: 10.1038/nn1374
52. Andersson ER, Saltó C, Villaescusa JC et al (2012) Wnt5a cooperates with canonical Wnts to generate midbrain dopaminergic neurons in vivo and in stem cells. Proc Natl Acad Sci. doi: 10.1073/pnas.1208524110
53. Castelo-Branco G, Wagner J, Rodriguez FJ et al (2003) Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc Natl Acad Sci 100:12747-12752. doi: 10.1073/pnas.1534900100
54. Shimamura K, Hirano S, McMahon AP, Takeichi M (1994) Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development 120:2225-2234
55. - mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell 69:581-595. doi: 10.1016/0092-8674(92)90222-X
56. Lie D-C, Colamarino SA, Song H-J et al (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375. doi: 10.1038/nature04108
57. Jessberger S, Clark RE, Broadbent NJ et al (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154. doi: 10.1101/lm.1172609
58. Aubert J, Dunstan H, Chambers I, Smith A (2002) Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation. Nat Biotechnol 20:1240-1245. doi: 10.1038/nbt763
59. Cajánek L, Ribeiro D, Liste I et al (2009) Wnt/beta-catenin signaling blockade promotes neuronal induction and dopaminergic differentiation in embryonic stem cells. Stem Cells 27:2917-2927. doi: 10.1002/stem.210
60. Sousa KM, Carlos Villaescusa J, Cajanek L et al (2010) Wnt2 regulates progenitor proliferation in the developing ventral midbrain. J Biol Chem 285:7246-7253. doi: 10.1074/jbc.M109.079822
61. Wayman GA, Impey S, Marks D et al (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50:897-909. doi: 10.1016/j.neuron.2006.05.008
62. Lyu J, Yamamoto V, Lu W (2008) Cleavage of the Wnt receptor Ryk regulates neuronal differentiation during cortical neurogenesis. Dev Cell 15:773-780. doi: 10.1016/j.devcel.2008.10.004
63. Zhong J, Kim H-T, Lyu J et al (2011) The Wnt receptor Ryk controls specification of GABAergic neurons versus oligodendrocytes during telencephalon development. Development 138:409-419. doi: 10.1242/dev.061051
64. Davidson KC, Adams AM, Goodson JM et al (2012) Wnt/β-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc Natl Acad Sci 109:4485-4490. doi: 10.1073/pnas.1118777109
65. Davidson KC, Jamshidi P, Daly R et al (2007) Wnt3a regulates survival, expansion, and maintenance of neural progenitors derived from human embryonic stem cells. Mol Cell Neurosci 36:408-415
66. Kalani MYS, Cheshier SH, Cord BJ et al (2008) Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci 105:16970-16975
67. Dravid G, Ye Z, Hammond H et al (2005) Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 23:1489-1501. doi: 10.1634/stemcells.2005-0034
68. Elizalde C, Campa VM, Caro M et al (2011) Distinct roles for Wnt-4 and Wnt-11 during retinoic acid-induced neuronal differentiation. Stem Cells 29:141-153. doi: 10.1002/stem.562
69. Farías GG, Alfaro IE, Cerpa W et al (2009) Wnt-5a/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons. J Biol Chem 284:15857-15866. doi: 10.1074/jbc.M808986200
70. Varela-Nallar L, Alfaro IE, Serrano FG et al (2010) Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses. Proc Natl Acad Sci 107:21164-21169. doi: 10.1073/pnas.1010011107/
71. Zhang X, Zhu J, Yang G-Y et al (2007) Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat Cell Biol 9:743-754. doi: 10.1038/ncb1603
72. Delaunay D, Cortay V, Patti D et al (2014) Mitotic spindle asymmetry: a Wnt/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell Rep 6:400-414. doi: 10.1016/j.celrep.2013.12.026
73. Wang Y, Thekdi N, Smallwood PM et al (2002) Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J Neurosci 22:8563-8573
74. Zhou C, Borello U, Rubenstein JLR (2006) Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience 142:1119-1131. doi: 10.1016/j.neuroscience.2006.07.007
75. L'episcopo F, Serapide MF, Tirolo C et al (2011) 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. doi: 10.1186/1750-1326-6-49
76. Lu W, Yamamoto V, Ortega B, Baltimore D (2004) Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119:97-108. doi: 10.1016/j.cell.2004.09.019
77. Ho H-YH, Susman MW, Bikoff JB et al (2012) Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc Natl Acad Sci 109:4044-4051. doi: 10.1073/pnas.1200421109
78. Torban E, Patenaude A-M, Leclerc S et al (2008) Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proc Natl Acad Sci 105:3449-3454. doi: 10.1073/pnas.0712126105
79. Lake BB, Sokol SY (2009) Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. J Cell Biol 185:59-66. doi: 10.1083/jcb.200807073
80. Marchetti B, L'Episcopo F, Morale MC et al (2013) 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 37:1550-1563. doi: 10.1111/ejn.12166
81. Inestrosa NC, Arenas E (2010) Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 11:77-86. doi: 10.1038/nrn2755
82. Zheng H, Ying H, Wiedemeyer R et al (2010) PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 17:497-509. doi: 10.1016/j.ccr.2010.03.020
83. Wang Y, Guo N, Nathans J (2006) The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J Neurosci 26:2147-2156. doi: 10.1523/JNEUROSCI.4698-05.2005
84. Stuebner S, Faus-Kessler T, Fischer T et al (2010) Fzd3 and Fzd6 deficiency results in a severe midbrain morphogenesis defect. Dev Dyn 239:246-260. doi: 10.1002/dvdy.22127
85. Bethea CL, Reddy AP, Pedersen D, Tokuyama Y (2009) Gene expression patterns expression profile of differentiating serotonin neurons derived from rhesus embryonic stem cells and comparison to adult serotonin neurons q. Gene Expr Patterns 9:94-108. doi: 10.1016/j.gep.2008.10.002
86. Jin X, Jeon H-Y, Joo KM et al (2011) Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res 71:3066-3075. doi: 10.1158/0008-5472.CAN-10-1495
87. Verani R, Cappuccio I, Spinsanti P et al (2007) Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid. J Neurochem 100:242-250. doi: 10.1111/j.1471-4159.2006.04207.x
88. Wu JQ, Habegger L, Noisa P et al (2010) Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc Natl Acad Sci 107:5254-5259. doi: 10.1073/pnas.0914114107
89. Lin M, Pedrosa E, Shah A et al (2011) RNA-Seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatric disorders. PLoS ONE 6:e23356. doi: 10.1371/journal.pone.0023356
90. Kemp CR, Willems E, Wawrzak D et al (2007) Expression of Frizzled5, Frizzled7, and Frizzled10 during early mouse development and interactions with canonical Wnt signaling. Dev Dyn 236:2011-2019. doi: 10.1002/dvdy.21198
91. Cantilena S, Pastorino F, Pezzolo A et al (2011) Frizzled receptor 6 marks rare, highly tumourigenic stem-like cells in mouse and human neuroblastomas. Oncotarget 2:976-983
92. De Calisto J, Araya C, Marchant L et al (2005) Essential role of non-canonical Wnt signalling in neural crest migration. Development 132:2587-2597. doi: 10.1242/dev.01857
93. Snow GE, Kasper AC, Busch AM et al (2009) Wnt pathway reprogramming during human embryonal carcinoma differentiation and potential for therapeutic targeting. BMC Cancer 9:383. doi: 10.1186/1471-2407-9-383
94. Katoh M, Katoh M (2007) Comparative integromics on FZD7 orthologs: conserved binding sites for PU.1, SP1, CCAAT-box and TCF/LEF/SOX transcription factors within 5′-promoter region of mammalian FZD7 orthologs. Int J Mol Med 19:529-533
95. Zhao C, Avilés C, Abel RA et al (2005) Hippocampal and visuospatial learning defects in mice with a deletion of frizzled 9, a gene in the Williams syndrome deletion interval. Development 132:2917-2927. doi: 10.1242/dev.01871
96. Kibar Z, Torban E, McDearmid JR et al (2007) Mutations in VANGL1 associated with neural-tube defects. N Engl J Med 356:1432-1437. doi: 10.1056/NEJMoa060651
97. Kibar Z, Vogan KJ, Groulx N et al (2001) Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28:251-255. doi: 10.1038/90081
98. Paganoni S, Ferreira A (2005) Neurite extension in central neurons: a novel role for the receptor tyrosine kinases Ror1 and Ror2. J Cell Sci 118:433-446. doi: 10.1242/jcs.01622
99. Paganoni S, Bernstein J, Ferreira A (2010) Ror1-Ror2 complexes modulate synapse formation in hippocampal neurons. Neuroscience 165:1261-1274. doi: 10.1016/j.neuroscience.2009.11.056
100. Endo M, Doi R, Nishita M, Minami Y (2011) Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J Cell Sci 125:2017-2029. doi: 10.1242/jcs.097782
101. Lu X, Borchers AGM, Jolicoeur C et al (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93-98. doi: 10.1038/nature02677
102. Pinson KI, Brennan J, Monkley S et al (2000) An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535-538. doi: 10.1038/35035124
103. Gomez AM, Burden SJ (2011) The extracellular region of Lrp4 is sufficient to mediate neuromuscular synapse formation. Dev Dyn 240:2626-2633. doi: 10.1002/dvdy.22772
104. Zhou C-J, Zhao C, Pleasure SJ (2004) Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci 24:121-126. doi: 10.1523/JNEUROSCI.4071-03.2004
105. Castelo-Branco G, Andersson ER, Minina E et al (2010) Delayed dopaminergic neuron differentiation in Lrp6 mutant mice. Dev Dyn 239:211-221. doi: 10.1002/dvdy.22094
106. Zechner D, Fujita Y, Hülsken J et al (2003) β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258:406-418. doi: 10.1016/S0012-1606(03)00123-4
107. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369. doi: 10.1126/science.1074192
108. Pöschl J, Grammel D, Dorostkar M et al (2013) Constitutive activation of β-catenin in neural progenitors results in disrupted proliferation and migration of neurons within the central nervous system. Dev Biol 374:319-332
109. Machon O, Backman M, Machonova O et al (2007) A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 311:223-237. doi: 10.1016/j.ydbio.2007.08.038
110. Chen B-Y, Wang X, Wang Z-Y et al (2013) Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/β-catenin signaling pathway. J Neurosci Res 91:30-41
111. Hirabayashi Y, Itoh Y, Tabata H et al (2004) The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791-2801. doi: 10.1242/dev.01165
112. Fang WQ, Chen WW, Fu AY, Ip N (2013) Axin directs the amplification and differentiation of intermediate progenitors in the developing cerebral cortex. Neuron 79:665-679. doi: 10.1016/j.neuron.2013.06.017
113. Pei Y, Brun SN, Markant SL et al (2012) WNT signaling increases proliferation and impairs differentiation of stem cells in the developing cerebellum. Development 139:1724-1733. doi: 10.1242/dev.050104
114. Israsena N, Hu M, Fu W et al (2004) The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev Biol 268:220-231. doi: 10.1016/j.ydbio.2003.12.024
115. Dhara SK, Stice SL (2008) Neural differentiation of human embryonic stem cells. J Cell Biochem 105:633-640
116. Vallier L, Alexander M, Pedersen RA (2005) Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118:4495-4509. doi: 10.1242/jcs.02553
117. Wang Q, Yang L, Alexander C, Temple S (2012) The niche factor syndecan-1 regulates the maintenance and proliferation of neural progenitor cells during mammalian cortical development. PLoS ONE. doi: 10.1371/journal.pone.0042883
118. Zhang J, Woodhead GJ, Swaminathan SK et al (2010) Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev Cell 18:472-479. doi: 10.1016/j.devcel.2009.12.025
119. Porlan E, Martí-Prado B, Morante-Redolat JM et al (2014) MT5-MMP regulates adult neural stem cell functional quiescence through the cleavage of N-cadherin. Nat Cell Biol 16:629-638. doi: 10.1038/ncb2993
120. Reimold AM, Grusby MJ, Kosaras B et al (1996) Chondrodysplasia and neurological abnormalities in ATF-2-deficient mice. Nature 379:262-265
121. Mantamadiotis T, Lemberger T, Bleckmann SC et al (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat Genet 31:47-54. doi: 10.1038/ng882
122. Ackermann J, Ashton G, Lyons S et al (2011) Loss of ATF2 function leads to cranial motoneuron degeneration during embryonic mouse development. PLoS ONE 6:e19090. doi: 10.1371/journal.pone.0019090
123. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660. doi: 10.1016/j.cell.2008.01.033
124. Miranda CJ, Braun L, Jiang Y et al (2013) Aging brain microenvironment decreases hippocampal neurogenesis through Wnt-mediated survivin signaling. Aging Cell 11:542-552. doi: 10.1111/j.1474-9726.2012.00816.x.Aging
125. Qu Q, Sun G, Murai K et al (2013) Wnt7a regulates multiple steps of neurogenesis. Mol Cell Biol 33:2551-2559. doi: 10.1128/MCB.00325-13
126. Encinas JM, Sierra A, Valcárcel-Martín R, Martín-Suárez S (2013) A developmental perspective on adult hippocampal neurogenesis. Int J Dev Neurosci 31:640-645. doi: 10.1016/j.ijdevneu.2013.04.001
127. Moreno-Estellés M, González-Gómez P, Hortigüela R et al (2012) Symmetric expansion of neural stem cells from the adult olfactory bulb is driven by astrocytes via WNT7A. Stem Cells 30:2796-2809. doi: 10.1002/stem.1243
128. Slater PG, Ramirez VT, Gonzalez-Billault C et al (2013) Frizzled-5 receptor is involved in neuronal polarity and morphogenesis of hippocampal neurons. PLoS ONE 8:e78892. doi: 10.1371/journal.pone.0078892
129. Seib D, Corsini N, Ellwanger K et al (2013) Loss of dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 12:204-214
130. Jang M-H, Bonaguidi MA, Kitabatake Y et al (2013) Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell 12:215-223. doi: 10.1016/j.stem.2012.11.021
131. Wexler EM, Paucer A, Kornblum HI et al (2009) Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells 27:1130-1141. doi: 10.1002/stem.36
132. Wexler EM, Geschwind DH, Palmer TD (2008) Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol Psychiatry 13:285-292. doi: 10.1038/sj.mp.4002093
133. Fiorentini A, Rosi MC, Grossi C et al (2010) Lithium improves hippocampal neurogenesis, neuropathology and cognitive functions in APP mutant mice. PLoS ONE 5:e14382. doi: 10.1371/journal.pone.0014382
134. Imura T, Wang X, Noda T et al (2010) Adenomatous polyposis coli is essential for both neuronal differentiation and maintenance of adult neural stem cells in subventricular zone and hippocampus. Stem Cells 28:2053-2064. doi: 10.1002/stem.524
135. Morgan-Smith M, Wu Y, Zhu X et al (2014) GSK-3 signaling in developing cortical neurons is essential for radial migration and dendritic orientation. Elife 2014:1-24. doi: 10.7554/eLife.02663.001
136. Orme M, Giannini A, Vivanco M, Kypta R (2003) Glycogen synthase kinase-3 and Axin function in a β-catenin-independent pathway that regulates neurite outgrowth in neuroblastoma cells. Mol Cell Neurosci 24:673-686. doi: 10.1016/S1044-7431(03)00229-X
137. Castaño Z, Gordon-Weeks PR, Kypta RM (2010) The neuron-specific isoform of glycogen synthase kinase-3beta is required for axon growth. J Neurochem 113:117-130. doi: 10.1111/j.1471-4159.2010.06581.x
138. Nelson S, Näthke IS (2013) Interactions and functions of the adenomatous polyposis coli (APC) protein at a glance. J Cell Sci 126:873-877. doi: 10.1242/jcs.100479
139. Preitner N, Quan J, Nowakowski DW et al (2014) APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 158:368-382. doi: 10.1016/j.cell.2014.05.042
140. Bowman AN, van Amerongen R, Palmer TD, Nusse R (2013) Lineage tracing with Axin2 reveals distinct developmental and adult populations of Wnt/β-catenin-responsive neural stem cells. Proc Natl Acad Sci 110:7324-7329. doi: 10.1073/pnas.1305411110
141. Adachi K, Mirzadeh Z, Sakaguchi M et al (2007) Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25:2827-2836. doi: 10.1634/stemcells.2007-0177
142. Ortega F, Gascón S, Masserdotti G et al (2013) Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling. Nat Cell Biol 15:602-613. doi: 10.1038/ncb2736
143. Azim K, Fisher B, Hurtado-chong A et al (2014) Persistent Wnt/beta-catenin signaling determines dorsalization of the postnatal subventricular zone and neural stem cell specification into oligodendrocytes and glutamatergic neurons. Stem Cells 32:1301-1312
144. Ye F, Chen Y, Hoang T et al (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829-838. doi: 10.1038/nn.2333
145. Reinecke K, Herdegen T, Eminel S et al (2013) Knockout of c-Jun N-terminal kinases 1, 2 or 3 isoforms induces behavioural changes. Behav Brain Res 245:88-95. doi: 10.1016/j.bbr.2013.02.013
146. Bevilaqua LRM, Kerr DS, Medina JH et al (2003) Inhibition of hippocampal Jun N-terminal kinase enhances short-term memory but blocks long-term memory formation and retrieval of an inhibitory avoidance task. Eur J Neurosci 17:897-902. doi: 10.1046/j.1460-9568.2003.02524.x
147. Pittenger C, Huang YY, Paletzki RF et al (2002) Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447-462
148. Nakagawa S, Kim J-E, Lee R et al (2002) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22:3673-3682
149. Raivich G, Bohatschek M, Da Costa C et al (2004) The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43:57-67. doi: 10.1016/j.neuron.2004.06.005
150. Wichterle H, Przedborski S (2010) What can pluripotent stem cells teach us about neurodegenerative diseases? Nat Neurosci 13:800-804. doi: 10.1038/nn.2577
151. Erceg S, Ronaghi M, Stojković M (2009) Human embryonic stem cell differentiation toward regional specific neural precursors. Stem Cells 27:78-87. doi: 10.1634/stemcells.2008-0543
152. Zhang SC, Wernig M, Duncan ID et al (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19:1129-1133. doi: 10.1038/nbt1201-1129
153. Broccoli V, Giannelli SG, Mazzara PG (2014) Modeling physiological and pathological human neurogenesis in the dish. Front Neurosci 8:183. doi: 10.3389/fnins.2014.00183
154. Kriks S, Shim J-W, Piao J et al (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480:547-551. doi: 10.1038/nature10648
155. Sundberg M, Bogetofte H, Lawson T et al (2013) 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 31:1548-1562
156. Du Z, Chen H, Liu H et al (2015) Generation and expansion of highly pure motor neuron progenitors from human pluripotent stem cells. Nat Commun 6:1-9. doi: 10.1038/ncomms7626
157. Reubinoff BE, Itsykson P, Turetsky T et al (2001) Neural progenitors from human embryonic stem cells. Nat Biotechnol 19:1134-1140
158. Menendez L, Yatskievych TA, Antin PB, Dalton S (2012) Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci 109:9220. doi: 10.1073/pnas.1207810109
159. Elkabetz Y, Panagiotakos G, Al Shamy G et al (2008) Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22:152-165. doi: 10.1101/gad.1616208
160. Uysal-Onganer P, Kypta RM (2012) Wnt11 in 2011 - the regulation and function of a non-canonical Wnt. Acta Physiol 204:52-64. doi: 10.1111/j.1748-1716.2011.02297.x
161. Vijayaragavan K, Szabo E, Bossé M et al (2009) Noncanonical Wnt signaling orchestrates early developmental events toward hematopoietic cell fate from human embryonic stem cells. Cell Stem Cell 4:248-262. doi: 10.1016/j.stem.2008.12.011
162. Terami H, Hidaka K, Katsumata T et al (2004) Wnt11 facilitates embryonic stem cell differentiation to Nkx2.5-positive cardiomyocytes. Biochem Biophys Res Commun 325:968-975. doi: 10.1016/j.bbrc.2004.10.103
163. Bengoa-Vergniory N, Gorroño-Etxebarria I, González Salazar I, Kypta RM (2014) A switch from canonical to noncanonical Wnt signaling mediates early differentiation of human neural stem cells. Stem Cells 32:3196-3208. doi: 10.1002/stem.1807
164. Nicoleau C, Varela C, Bonnefond C et al (2013) ES cells neural differentiation qualifies the role of Wnt/β-catenin signals in human telencephalic specification and regionalization. Stem Cells 31:1763-1774. doi: 10.1002/stem.1462
165. Ding VMY, Ling L, Natarajan S et al (2010) FGF-2 modulates Wnt signaling in undifferentiated hESC and iPS cells through activated PI3-K/GSK3beta signaling. J Cell Physiol 225:417-428
166. Muroyama Y, Kondoh H, Takada S (2004) Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem Biophys Res Commun 313:915-921
167. Slawny NA, O'Shea KS (2011) Dynamic changes in Wnt signaling are required for neuronal differentiation of mouse embryonic stem cells. Mol Cell Neurosci 48:205-216. doi: 10.1016/j.mcn.2011.07.010
168. Ten Berge D, Kurek D, Blauwkamp T et al (2011) Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 13:1070-1075. doi: 10.1038/ncb2314
169. Ying Q-L, Wray J, Nichols J et al (2008) The ground state of embryonic stem cell self-renewal. Nature 453:519-523. doi: 10.1038/nature06968
170. Atlasi Y, Noori R, Gaspar C et al (2013) Wnt signaling regulates the lineage differentiation potential of mouse embryonic stem cells through Tcf3 down-regulation. PLoS Genet 9:e1003424. doi: 10.1371/journal.pgen.1003424
171. Osei-Sarfo K, Gudas LJ (2014) Retinoic acid suppresses the canonical Wnt signaling pathway in embryonic stem cells and activates the noncanonical Wnt signaling pathway. Stem Cells 32:2061-2071. doi: 10.1002/stem.1706
172. Wu C-I, Hoffman JA, Shy BR et al (2012) Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 139:2118-2129. doi: 10.1242/dev.076067
173. Lee C-T, Bendriem RM, Kindberg AA et al (2015) Functional consequences of 17q21.31/WNT3-WNT9B amplification in hPSCs with respect to neural differentiation. Cell Rep 10:616-632. doi: 10.1016/j.celrep.2014.12.050
174. Li X-J, Zhang X, Johnson MA et al (2009) Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 136:4055-4063. doi: 10.1242/dev.036624
175. Lange C, Mix E, Frahm J et al (2011) Small molecule GSK-3 inhibitors increase neurogenesis of human neural progenitor cells. Neurosci Lett 488:36-40
176. Inestrosa NC, Montecinos-Oliva C, Fuenzalida M (2012) Wnt signaling: role in Alzheimer disease and schizophrenia. J Neuroimmune Pharmacol 7:788-807. doi: 10.1007/s11481-012-9417-5
177. Fancy SPJ, Baranzini SE, Zhao C et al (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23:1571-1585. doi: 10.1101/gad.1806309
178. Encinas JM, Michurina TV, Peunova N et al (2011) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:566-579
179. Sancho RM, Law BMH, Harvey K (2009) Mutations in the LRRK2 Roc-COR tandem domain link Parkinson's disease to Wnt signalling pathways. Hum Mol Genet 18:3955-3968. doi: 10.1093/hmg/ddp337
180. Marchetti B, Pluchino S (2013) Wnt your brain be inflamed? Yes, it Wnt! Trends Mol Med 19:144-156. doi: 10.1016/j.molmed.2012.12.001
181. Piccin D, Tufford A, Morshead CM (2015) Neural stem and progenitor cells in the aged subependyma are activated by the young niche. Neurobiol Aging 35:1669-1679. doi: 10.1016/j.neurobiolaging.2014.01.026
182. Aloia L, Di Stefano B, Sessa A et al (2014) Zrf1 is required to establish and maintain neural progenitor identity. Genes Dev 28:182-197. doi: 10.1101/gad.228510.113