Wnt Signaling Is Required for Long-Term Memory Formation

Cell Reports

Volumn 4, Issue 6, 2013, Pages 1082-1089

  Tan, Ying ^a   Yu, Dinghui ^a   Busto, Germain U ^b   Wilson, Curtis ^a   Davis, Ronald L ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; WNT PROTEIN; WNT1 PROTEIN;

ARM GENE; ARTICLE; DROSOPHILA; GENE SILENCING; GENOTYPE; IMMUNOHISTOCHEMISTRY; INSECT GENOME; LONG TERM MEMORY; MUSHROOM BODY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSGENE;

BASIDIOMYCOTA;

ANIMALS; ARMADILLO DOMAIN PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; MEMORY, LONG-TERM; NEURONS; OLFACTORY PATHWAYS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSGENES; WNT SIGNALING PATHWAY;

EID: 84884596320     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.08.007     Document Type: Article

References (32)

1. Akalal D.B., Yu D., Davis R.L. The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants. J.Neurosci. 2011, 31:5643-5647.
2. Ataman B., Ashley J., Gorczyca M., Ramachandran P., Fouquet W., Sigrist S.J., Budnik V. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron 2008, 57:705-718.
3. Bhanot P., Fish M., Jemison J.A., Nusse R., Nathans J., Cadigan K.M. Frizzled and Dfrizzled-2 function as redundant receptors for Wingless during Drosophila embryonic development. Development 1999, 126:4175-4186.
4. Bhat K.M. frizzled and frizzled 2 play a partially redundant role in wingless signaling and have similar requirements to wingless in neurogenesis. Cell 1998, 95:1027-1036.
5. Cerpa W., Godoy J.A., Alfaro I., Farías G.G., Metcalfe M.J., Fuentealba R., Bonansco C., Inestrosa N.C. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J.Biol. Chem. 2008, 283:5918-5927.
6. Chen C.M., Struhl G. Wingless transduction by the Frizzled and Frizzled2 proteins of Drosophila. Development 1999, 126:5441-5452.
7. Chen J., Park C.S., Tang S.J. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J.Biol. Chem. 2006, 281:11910-11916.
8. Ciani L., Salinas P.C. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 2005, 6:351-362.
9. Davidson G., Wu W., Shen J., Bilic J., Fenger U., Stannek P., Glinka A., Niehrs C. Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 2005, 438:867-872.
10. Davis R.L. Olfactory learning. Neuron 2004, 44:31-48.
11. Davis R.L. Traces of Drosophila memory. Neuron 2011, 70:8-19.
12. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
13. Gogolla N., Galimberti I., Deguchi Y., Caroni P. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62:510-525.
14. Inestrosa N.C., Arenas E. Emerging roles of Wnts in the adult nervous system. Nat. Rev. Neurosci. 2010, 11:77-86.
15. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
16. Maguschak K.A., Ressler K.J. β-catenin is required for memory consolidation. Nat. Neurosci. 2008, 11:1319-1326.
17. Mao Z., Roman G., Zong L., Davis R.L. Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch. Proc. Natl. Acad. Sci. USA 2004, 101:198-203.
18. Mathew D., Ataman B., Chen J., Zhang Y., Cumberledge S., Budnik V. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 2005, 310:1344-1347.
19. Moon R.T., Kohn A.D., De Ferrari G.V., Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 2004, 5:691-701.
20. Nelson W.J., Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004, 303:1483-1487.
21. Rosso S.B., Sussman D., Wynshaw-Boris A., Salinas P.C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 2005, 8:34-42.
22. Sahores M., Gibb A., Salinas P.C. Frizzled-5, a receptor for thesynaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 2010, 137:2215-2225.
23. Shimogori T., VanSant J., Paik E., Grove E.A. Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. J.Comp. Neurol. 2004, 473:496-510.
24. Speese S.D., Ashley J., Jokhi V., Nunnari J., Barria R., Li Y., Ataman B., Koon A., Chang Y.T., Li Q., et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012, 149:832-846.
25. Stranahan A.M., Lee K., Becker K.G., Zhang Y., Maudsley S., Martin B., Cutler R.G., Mattson M.P. Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol. Aging 2010, 31:1937-1949.
26. Tabatadze N., Tomas C., McGonigal R., Lin B., Schook A., Routtenberg A. Wnt transmembrane signaling and long-term spatial memory. Hippocampus 2012, 22:1228-1241.
27. Tan Y., Yu D., Pletting J., Davis R.L. Gilgamesh is required for rutabaga-independent olfactory learning in Drosophila. Neuron 2010, 67:810-820.
28. Tissir F., Goffinet A.M. Expression of planar cell polarity genes during development of the mouse CNS. Eur. J. Neurosci. 2006, 23:597-607.
29. Tully T., Preat T., Boynton S.C., Del Vecchio M. Genetic dissection of consolidated memory in Drosophila. Cell 1994, 79:35-47.
30. Wayman G.A., Impey S., Marks D., Saneyoshi T., Grant W.F., Derkach V., Soderling T.R. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 2006, 50:897-909.
31. Yu X., Malenka R.C. Beta-catenin is critical for dendritic morphogenesis. Nat. Neurosci. 2003, 6:1169-1177.
32. Yu D., Akalal D.B., Davis R.L. Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 2006, 52:845-855.