Canonical Wnt signaling is necessary for object recognition memory consolidation

Journal of Neuroscience

Volumn 33, Issue 31, 2013, Pages 12619-12626

  Fortress, Ashley M ^a   Schram, Sarah L ^a   Tuscher, Jennifer J ^a   Frick, Karyn M ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3BETA; LYMPHOID ENHANCER FACTOR 1; MYC PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; TRANSCRIPTION FACTOR 7; WNT PROTEIN; WNT1 PROTEIN; WNT7A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HABITUATION; IMMUNOREACTIVITY; LEARNING; MALE; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECOGNITION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BETA CATENIN; CYCLIN D1; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; GUANYLATE KINASE; HIPPOCAMPUS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; RECOGNITION (PSYCHOLOGY); SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; WNT PROTEINS;

EID: 84880849552     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0659-13.2013     Document Type: Article

References (47)

1. Ahmad-Annuar A, Ciani L, Simeonidis I, Herreros J, Fredj NB, Rosso SB, Hall A, Brickley S, Salinas PC (2006) Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J Cell Biol 174:127-139. CrossRef Medline
2. Amendola D, De Salvo M, Marchese R, Verga Falzacappa C, Stigliano A, Carico E, Brunetti E, Moscarini M, Bucci B (2009) Myc downregulation affects cyclin D1/cdk4 activity and induces apoptosis via Smac/ Diablo pathway in an astrocytoma cell line. Cell Prolif 42:94-109. CrossRef Medline
3. Arrázola MS, Varela-Nallar L, Colombres M, Toledo EM, Cruzat F, Pavez L, Assar R, Aravena A, González M, Montecino M, Maass A, Martínez S, Inestrosa NC (2009) Calcium/calmodulin-dependent protein kinase type IV is a target gene of the Wnt/beta-catenin signaling pathway. J Cell Physiol 221:658-667. CrossRef Medline
4. Caraci F, Busceti C, Biagioni F, Aronica E, Mastroiacovo F, Cappuccio I, Battaglia G, Bruno V, Caricasole A, Copani A, Nicoletti F (2008) The Wnt antagonist, Dickkopf-1, as a target for the treatment of neurodegenerative disorders. Neurochem Res 33:2401-2406. CrossRef Medline
5. Cerpa W, Godoy JA, Alfaro I, Farías GG, Metcalfe MJ, Fuentealba R, Bonansco C, Inestrosa NC (2008) Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 283:5918-5927. CrossRef Medline
6. Cerpa W, Gambrill A, Inestrosa NC, Barria A (2011) Regulation of NMDAreceptor synaptic transmission by Wnt signaling. J Neurosci 31:9466-9471. CrossRef Medline
7. Chen J, Park CS, Tang SJ (2006) Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J Biol Chem 281: 11910-11916. CrossRef Medline
8. Chen Y, Bodles AM (2007) Amyloid precursor protein modulates betacatenin degradation. J Neuroinflammation 4:29. CrossRef Medline
9. Ciani L, Salinas PC (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6:351-362. CrossRef Medline
10. Ciani L, Boyle KA, Dickins E, Sahores M, Anane D, Lopes DM, Gibb AJ, Salinas PC (2011) Wnt7a signaling promotes dendritic spine growth and synaptic strength through Ca(2)(+)/Calmodulin-dependent protein kinase II. Proc Natl Acad Sci U S A 108:10732-10737. CrossRef Medline
11. Diep DB, Hoen N, Backman M, Machon O, Krauss S (2004) Characterisation of the Wnt antagonists and their response to conditionally activated Wnt signalling in the developing mouse forebrain. Brain Res Dev Brain Res 153:261-270. CrossRef Medline
12. Epp JR, Chow C, Galea LA (2013) Hippocampus-dependent learning influences hippocampal neurogenesis. Front Neurosci 7:57. CrossRef Medline
13. Farías GG, Alfaro IE, Cerpa W, Grabowski CP, Godoy JA, Bonansco C, Inestrosa NC (2009) Wnt-5a/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons. J Biol Chem 284:15857-15866. CrossRef Medline
14. Fortress AM, Fan L, Orr PT, Zhao Z, Frick KM (2013) Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in dorsal hippocampus. Learn Mem 20:147-155. CrossRef Medline
15. Frick KM, Fernandez SM, Harburger LL (2010) A new approach to understanding the molecular mechanisms through which estrogens affect cognition. Biochim Biophys Acta 1800:1045-1055. CrossRef Medline
16. Gogolla N, Galimberti I, Deguchi Y, Caroni P (2009) Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 62:510-525. CrossRef Medline
17. Gresack JE, Frick KM (2003) Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Res 982:98-107. CrossRef Medline
18. Hall AC, Lucas FR, Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535. CrossRef Medline
19. HuS, Begum AN, JonesMR, OhMS, BeechWK, Beech BH, Yang F, Chen P, Ubeda OJ, Kim PC, Davies P, Ma Q, Cole GM, Frautschy SA (2009) GSK3 inhibitors show benefits in an Alzheimer's disease (AD) model of neurodegeneration but adverse effects in control animals. Neurobiol Dis 33:193-206. CrossRef Medline
20. Inestrosa NC, Arenas E (2010) Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 11:77-86. CrossRef Medline
21. Killick R, Ribe EM, Al-Shawi R, Malik B, Hooper C, Fernandes C, Dobson R, Nolan PM, Lourdusamy A, Furney S, Lin K, Breen G, Wroe R, To AW, Leroy K, Causevic M, Usardi A, Robinson M, NobleW, Williamson R, et al. (2012) Clusterin regulates beta-amyloid toxicity via Dickkopf-1-driven induction of the wnt-PCP-JNK pathway. Mol Psychiatry. Advance online publication. Retrieved January 28, 2013. doi:10.1038/mp.2012.163. CrossRef Medline
22. Lie DC, Colamarino SA, Song HJ, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375. CrossRef Medline
23. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X (2002) Control of beta-catenin phosphorylation/degradation by a dualkinase mechanism. Cell 108:837-847. CrossRef Medline
24. Maguschak KA, Ressler KJ (2008) Beta-catenin is required for memory consolidation. Nat Neurosci 11:1319-1326. CrossRef Medline
25. Maguschak KA, Ressler KJ (2011) Wnt signaling in amygdala-dependent learning and memory. J Neurosci 31:13057-13067. CrossRef Medline
26. Murase S, Mosser E, Schuman EM (2002) Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35:91-105. CrossRef Medline
27. Park M, Shen K (2012) WNTs in synapse formation and neuronal circuitry. EMBO J 31:2697-2704. CrossRef Medline
28. Purro SA, Dickins EM, Salinas PC (2012) The secreted Wnt antagonist Dickkopf-1 is required for amyloid beta-mediated synaptic loss. J Neurosci 32:3492-3498. CrossRef Medline
29. Qin X, Zhang H, Zhou X, Wang C, Zhang H, Zhang X, Ye L (2007) Proliferation and migration mediated by Dkk-1/Wnt/beta-catenin cascade in a model of hepatocellular carcinoma cells. Transl Res 150:281-294. Medline
30. Qu Q, Sun G, Murai K, Ye P, Li W, Asuelime G, Cheung K, Shi Y (2013) Wnt7a regulates multiple steps of neurogenesis. Mol Cell Bio DOI 10.1128/MCB. 00325-13.
31. Rai M, Walthall JM, Hu J, Hatzopoulos AK (2012) Continuous antagonism by Dkk1 counter activates canonical Wnt signaling and promotes cardiomyocyte differentiation of embryonic stem cells. Stem Cells Dev 21:54-66. CrossRef Medline
32. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334. CrossRef Medline
33. Sadot E, Conacci-Sorrell M, Zhurinsky J, Shnizer D, Lando Z, Zharhary D, Kam Z, Ben-Ze'ev A, Geiger B (2002) Regulation of S33/S37 phosphorylated beta-catenin in normal and transformed cells. J Cell Sci 115:2771-2780. Medline
34. Sahores M, Gibb A, Salinas PC (2010) Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 137:2215-2225. CrossRef Medline
35. Salcedo-Tello P, Ortiz-Matamoros A, Arias C (2011) GSK3 Function in the brain during development, neuronal plasticity, and neurodegeneration. Int J Alzheimers Dis 2011:189728. CrossRef Medline
36. Salinas PC, Zou Y (2008) Wnt signaling in neural circuit assembly. Annu Rev Neurosci 31:339-358. CrossRef Medline
37. Seib DR, Corsini NS, Ellwanger K, Plaas C, Mateos A, Pitzer C, Niehrs C, Celikel T, Martin-Villalba A (2013) Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 12:204-214. CrossRef Medline
38. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A (1999) The cyclin D1 gene is a target of the beta-catenin/ LEF-1 pathway. Proc Natl Acad Sci U S A 96:5522-5527. CrossRef Medline
39. Spinsanti P, De Vita T, Caruso A, Melchiorri D, Misasi R, Caricasole A, Nicoletti F (2008) Differential activation of the calcium/protein kinaseCand the canonical beta-catenin pathway byWnt1and Wnt7a produces opposite effects on cell proliferation in PC12 cells. J Neurochem 104:1588-1598. CrossRef Medline
40. Tabatadze N, Tomas C, McGonigal R, Lin B, Schook A, Routtenberg A (2012) Wnt transmembrane signaling and long-term spatial memory. Hippocampus 22:1228-1241. CrossRef Medline
41. Varela-Nallar L, Alfaro IE, Serrano FG, Parodi J, Inestrosa NC (2010) Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses. Proc Natl Acad Sci U S A 107:21164-21169. CrossRef Medline
42. Wey A, Knoepfler PS (2010) c-myc and N-myc promote active stem cell metabolism and cycling as architects of the developing brain. Oncotarget 1:120-130. Medline
43. Wey A, Martínez Cerdeno V, Pleasure D, Knoepfler PS (2010) c-and N-myc regulate neural precursor cell fate, cell cycle, and metabolism to direct cerebellar development. Cerebellum 9:537-547. CrossRef Medline
44. Wharton KA Jr (2003) Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev Biol 253:1-17. CrossRef Medline
45. Yamada M, Ohnishi J, Ohkawara B, Iemura S, Satoh K, Hyodo-Miura J, Kawachi K, Natsume T, Shibuya H (2006) NARF, an nemo-like kinase (NLK)-associated ring finger protein regulates the ubiquitylation and degradation of T cell factor/lymphoid enhancer factor (TCF/LEF). J Biol Chem 281:20749-20760. CrossRef Medline
46. Zhang L, Yang X, Yang S, Zhang J (2011) The Wnt /beta-catenin signaling pathway in the adult neurogenesis. Eur J Neurosci 33:1-8. CrossRef Medline
47. Zhao Z, Fan L, Fortress AM, Boulware MI, Frick KM (2012) Hippocampal histone acetylation regulates object recognition and the estradiol-induced enhancement of object recognition. J Neurosci 32:2344-2351. CrossRef Medline