The role of WNT signaling in neuroprotection

Drug News and Perspectives

Volumn 22, Issue 10, 2009, Pages 579-591

  Cerpa, Waldo ^a   Toledo, Enrique M ^a   Varela Nallar, Lorena ^a   Inestrosa, Nibaldo C ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

AF 267B; AMYLOID BETA PROTEIN; ANTISENSE OLIGONUCLEOTIDE; BETA CATENIN; ESTRADIOL; GLUTAMATE RECEPTOR; LITHIUM; MUSCARINIC M1 RECEPTOR AGONIST; NEUROTRANSMITTER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE C ACTIVATOR; ROSIGLITAZONE; TROLOX C; UNCLASSIFIED DRUG; WNT PROTEIN;

ALZHEIMER DISEASE; BRAIN DAMAGE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; DRUG TARGETING; EMBRYO DEVELOPMENT; HUMAN; LEARNING DISORDER; LONG TERM POTENTIATION; MEMORY DISORDER; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE;

AMYLOID BETA-PROTEIN; ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; SIGNAL TRANSDUCTION; SYNAPSES; WNT PROTEINS;

EID: 77949514363     PISSN: 02140934     EISSN: None     Source Type: Journal    
DOI: 10.1358/dnp.2009.22.10.1443391     Document Type: Review

References (131)

1. Logan, C.Y. and Nusse, R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004, 20: 781-810.
2. McMahon, A.P. Cell signalling in induction and anterior-posterior patterning of the vertebrate central nervous system. Curr Opin Neurobiol 1993, 3(1): 4-7.
3. McMahon, A.P. and Bradley, A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 1990, 62(6): 1073-85.
4. Miller, J.R. The Wnts. Genome Biol 2002, 3(1): Reviews3001. 1-15.
5. Nusse, R. An ancient cluster of Wnt paralogues. Trends Genet 2001, 17(8): 443.
6. Polakis, P. The many ways of Wnt in cancer. Curr Opin Genet Dev 2007, 17(1): 45-51.
7. Rubinfeld, B., Souza, B., Albert, I., Muller, O., Chamberlain, S.H., Masiarz, F.R., Munemitsu, S. and Polakis, P. Association of the APC gene product with beto-catenin. Science 1993, 262(5140): 1731-4.
8. De Ferrari, G.V. and Moon, R.T. The ups and downs of Wnt signaling in prevalent neurological disorders. Oncogene 2006, 25(57): 7545-53.
9. Lovestone, S., Killick, R., Di Forti, M. and Murray, R. Schizophrenia as a GSK-3 dysregulation disorder. Trends Neurosci 2007, 30(4): 142-9.
10. Williams, R.S. and Harwood, A.J. Lithium therapy and signal transduction. Trends Pharmacol Sci 2000, 21(2): 61-4.
11. Bassuk, A.G., Wallace, R.H., Buhr, A. et al. A homozygous mutation in human PRICKLE1 causes an autosomal-recessive progressive myoclonus epilepsy-ataxia syndrome. Am J Hum Genet 2008, 83(5): 572-81.
12. De Ferrari, G.V. and Inestrosa, N.C. Wnt signaling function in Alzheimer's disease. Brain Res Brain Res Rev 2000, 33(1): 1-12.
13. De Ferrari, G.V., Papassotiropoulos, A., Biechele, T. et al. Common genetic variation within the low-density lipoprotein receptor-related protein 6 and late-onset Alzheimer's disease. Proc Natl Acad Sci U S A 2007, 104(22): 9434-9.
14. Inestrosa, N.C., Alvarez, A., Godoy, J., Reyes, A. and De Ferrari, G.V. Acetylcholinesterase-amyloid-beta-peptide interaction and Wnt signaling involvement in Abeta neurotoxicity. Acta Neurol Scand Suppl 2000, 176: 53-9.
15. van Amerongen, R. and Berns, A. Knockout mouse models to study Wnt signal transduction. Trends Genet 2006, 22(12): 678-89.
16. Nusse, R. and Varmus, H.E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982, 31(1): 99-109.
17. Cabrera, C.V., Alonso, M.C., Johnston, P., Phillips, R.G. and Lawrence, P.A. Phenocopies induced with antisense RNA identify the wingless gene. Cell 1987, 50(4): 659-63.
18. Rijsewijk, F., Schuermann, M., Wagenaar, E., Parren, P., Weigel, D. and Nusse, R. The Drosophilo homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Celt 1987, 50(4): 649-57.
19. Du, S.J., Purcell, S.M., Christian, J.L., McGrew, L.L. and Moon, R.T. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol Cell Biol 1995, 15(5): 2625-34.
20. Gordon, M.D. and Nusse, R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006, 281(32): 22429-33.
21. Moon, R.T., DeMarais, A. and Olson, D.J. Responses to Wnt signals in vertebrate embryos may involve changes in cell adhesion and cell movement. J Cell Sci Suppl 1993, 17: 183-8.
22. Mikels, A.J. and Nusse, R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 2006, 4(4): e115.
23. Kohn, A.D. and Moon, R.T. Wnt and calcium signaling: Beta-catenin-independent pathways. Cell Calcium 2005, 38(3-4): 439-46.
24. Kuhl, M., Sheldahl, L.C., Malbon, C.C. and Moon, R.T. Ca(2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J Biol Chem 2000, 275(17): 12701-11.
25. Miller, J.R., Hocking, A.M., Brown, J.D. and Moon, R.T. Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene 1999, 18(55): 7860-72.
26. Tamai, K., Semenov, M., Kato, Y. et al. LDL-receptor-related proteins in Wnt signal transduction. Nature 2000, 407(6803): 530-5.
27. Davidson, G., Wu, W., Shen, J., Bilic, J., Fenger, U., Stannek, P., Glinka, A. and Niehrs, C. Casein kinase 1 gamma couples Wnt receptor activation to cytoplasmic signal transduction. Nature 2005, 438(7069): 867-72.
28. Zeng, X., Tamai, K., Doble, B. et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 2005, 438(7069): 873-7.
29. Dale, T.C. Signal transduction by the Wnt family of ligands. Biochem J 1998, 329(Pt 2): 209-23.
30. Chen, R.H., Ding, W.V. and McCormick, F. Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 2000, 275(23): 17894-9.
31. van Amerongen, R., Mikels, A. and Nusse, R. Alternative Wnt signaling is initiated by distinct receptors. Sci Signal 2008, 1(35): re9.
32. Hsieh, J.C., Kodjabachian, L., Rebbert, M.L. et al. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 1999, 398(6726): 431-6.
33. Wouda, R.R., Bansraj, M.R., de Jong, A.W., Noordermeer, J.N. and Fradkin, L.G. Src family kinases are required for WNT5 signaling through the Derailed/RYK receptor in the Drosophila embryonic central nervous system. Development 2008, 135(13): 2277-87.
34. Oishi, I., Suzuki, H., Onishi, N. et al. The receptor tyrosine kinase Ror2 is involved in noncanonical Wnt5a/JNK signalling pathway. Genes Cells 2003, 8(7): 645-54.
35. Xu, Y.K. and Nusse, R. The Frizzled CRD domain is conserved in diverse proteins including several receptor tyrosine kinases. Curr Biol 1998, 8(12): R405-6.
36. Cerpa, W., Godoy, J.A., Alfaro, I., Farias, G.G., Metcalfe, M.J., Fuentealba, R., Bonansco, C. and Inestrosa, N.C. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 2008, 283(9): 5918-27.
37. Davis, E.K., Zou, Y. and Ghosh, A. Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocam pal synapse formation. Neural Dev 2008, 3: 32-48.
38. Chen, J., Park, C.S. and Tang, S.J. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J Biol Chem 2006, 281(17): 11910-6.
39. Hooper, C., Markevich, V., Plattner, F. et al. Glycogen synthase kinose-3 inhibition is integral to long-term potentiation. Eur J Neurosci 2007, 25(1): 81-6.
40. Hernandez, F., Borrell, J., Guaza, C., Avila, J. and Lucas, J.J. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J Neurochem 2002, 83(6): 1529-33.
41. Peineau, S., Taghibiglou, C., Bradley, C. et al. LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 2007, 53(5): 703-17.
42. Rosso, S.B., Sussman, D., Wynshaw-Boris, A. and Salinas, P.C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 2005, 8(1): 34-42.
43. Yu, X. and Malenka, R.C. Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 2003, 6(11): 1169-77.
44. Lohmann, C., Myhr, K.L. and Wong, R.O. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 2002, 418(6894): 177-81.
45. Speese, S.D. and Budnik, V. Wnts: Up-and-coming at the synapse. Trends Neurosci 2007, 30(6): 268-75.
46. Gogolla, N., Galimberti, I., Deguchi, Y. and Caroni, P. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62(4): 510-25.
47. Salinas, P.C. and Zou, Y. Wnt signaling in neural circuit assembly. Annu Rev Neurosci 2008, 31: 339-58.
48. Stranahan, A.M., Lee, K., Becker, K.G. et al. Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging 2008. Epub ahead of print.
49. Wu, P., Jiang, C., Shen, Q. and Hu, Y. Systematic gene expression profile of hypothalamus in calorie-restricted mice implicates the involvement of mTOR signaling in neuroprotective activity. Mech Ageing Dev 2009, 130(9): 602-10.
50. De Ferrari, G.V., Chacon, M.A., Barria, M.I. et al. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by beta-amyloid fibrils. Mol Psychiatry 2003, 8(2): 195-208.
51. Garrido, J.L., Godoy, J.A., Alvarez, A., Bronfman, M. and Inestrosa, N.C. Protein kinase C inhibits amyloid beta peptide neuro toxicity by acting on members of the Wnt pathway. FASEB J 2002, 16(14): 1982-4.
52. Inestrosa, N., De Ferrari, G.V., Garrido, J.L., Alvarez, A., Olivares, G.H., Barria, M.I., Bronfman, M. and Chacon, M.A. Wnt signaling involvement in beta-amyloid-dependent neurodegeneration. Neurochem Int 2002, 41(5): 341-4.
53. Alvarez, G., Munoz-Montano, J.R., Satrustegui, J., Avila, J., Bogonez, E. and Diaz-Nido, J. Regulation of tau phosphorylation and protection against beta-amyloid-induced neurodegeneration by lithium. Possible implications for Alzheimer's disease. Bipolar Disord 2002, 4(3): 153-65.
54. Caricasole, A., Copani, A., Caraci, F. et al. Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is associated with neuronal degeneration in Alzheimer's brain. J Neurosci 2004, 24(26): 6021-7.
55. Ghanevati, M. and Miller, C.A. Phospho-beta-catenin accumulation in Alzheimer's disease and in aggresomes attributable to proteasome dysfunction. J Mol Neurosci 2005, 25(1): 79-94.
56. Magdesian, M.H., Carvalho, M.M., Mendes, F.A., Saraiva, L.M., Juliano, M.A., Juliano, L., Garcia-Abreu, J. and Ferreira, ST. Amyloid-beta binds to the extracellular cysteine-rich domain of Frizzled and inhibits Wnt/beta-catenin signaling. J Biol Chem 2008, 283(14): 9359-68.
57. Takashima, A., Murayama, M., Murayama, O. et al. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci USA 1998, 95(16): 9637-641.
58. Zhang, Z., Hartmann, H., Do, V.M. et al. Destabilization of beta-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 1998, 395(6703): 698-702.
59. Moon, R.T., Kohn, A.D., De Ferrari, G.V. and Kaykas, A. WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 2004, 5(9): 691-701.
60. Pei, J.J., Braak, E., Braak, H., Grundke-Iqbal, I., Iqbal, K., Winblad, B. and Cowburn, R.F. Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J Neuropathol Exp Neurol 1999, 58(9): 1010-9.
61. Lucas, J.J., Hernandez, F., Gomez-Ramos, P., Moran, M.A., Hen, R. and Avila, J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 2001, 20(1-Z): 27-39.
62. Ertekin-Taner, N., Ronald, J., Asahara, H. et al. Fine mapping of the alpha-T catenin gene to a quantitative trait locus on chromosome 10 in late-onset Alzheimer's disease pedigrees. Hum Mol Genet 2003, 12(23): 3133-43.
63. Busciglio, J., Lorenzo, A., Yeh, J. and Yankner, B.A. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 1995, 14(4): 879-88.
64. Caricasole, A., Copani, A., Caruso, A., Caraci, F., Iacovelli, L., Sortino, M.A., Terstappen, G.C. and Nicoletti, F. The Wnt pathway, cell-cycle activation and beta-amyloid: Novel therapeutic strategies in Alzheimer's disease? Trends Pharmacol Sci 2003, 24(5): 233-8.
65. Alvarez, A.R., Godoy, J.A., Mullendorff, K., Olivares, G.H., Bronfman, M. and Inestrosa, N.C. Wnt-3a overcomes beta-amyloid toxicity in rat hippocampal neurons. Exp Cell Res 2004, 297(1): 186-96.
66. Fuentealba, R.A., Farias, G., Scheu, J., Bronfman, M., Marzolo, M.P. and Inestrosa, N.C. Signal transduction during amyloid-beta-peptide neurotoxicity: Role in Alzheimer disease. Brain Res Brain Res Rev 2004, 47(1-3): 275-89.
67. Li, H.L., Wang, H.H., Liu, S.J. et al. Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc Natl Acad Sci U S A 2007, 104(9): 3591-6.
68. Raber, J., Huang, Y. and Ashford, J.W. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol Aging 2004, 25(5): 641-50.
69. Strittmatter, W.J. and Roses, A.D. Apolipoprotein E and Alzheimer disease. Proc Natl Acad Sci U S A 1995, 92(11): 4725-7.
70. Caruso, A., Motolese, M., Iacovelli, L. et al. Inhibition of the canonical Wnt signaling pathway by apolipoprotein E4 in PC12 cells. J Neurochem 2006, 98(2): 364-71.
71. Leroy, K. and Brion, J.P. Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J Chem Neuroanat 1999, 16(4): 279-93.
72. Peineau, S., Bradley, C., Taghibiglou, C., Doherty, A., Bortolotto, Z.A., Wang, Y.T. and Collingridge, G.L. The role of GSK-3 in synaptic plasticity. Br J Pharmacol 2008, 153(Suppl. 1): S428-37.
73. Quintanilla, R.A., Munoz, F.J., Metcalfe, M.J., Hitschfeld, M., Olivares, G., Godoy, J.A. and Inestrosa, N.C. Trolox and 17beta-estradiol protect against amyloid beta-peptide neurotoxicity by a mechanism that involves modulation of the Wnt signaling pathway. J Biol Chem 2005, 280(12): 11615-25.
74. Sheldahl, L.C., Slusarski, D.C., Pandur, P., Miller, J.R., Kuhl, M. and Moon, R.T. Dishevelled activates Ca2+ flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 2003, 161(4): 769-77.
75. Mao, B., Wu, W., Li, Y., Hoppe, D., Stannek, P., Glinka, A. and Niehrs, C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 2001, 411(6835): 321-5.
76. Zorn, A.M. Wnt signalling: Antagonistic Dickkopfs. Curr Biol 2001, 11(15): R592-5.
77. Mudher, A. and Lovestone, S. Alzheimer's disease-do tauists and baptists finally shake hands? Trends Neurosci 2002, 25(1): 22-6.
78. Cappuccio, I., Calderone, A., Busceti, C.L. et al. Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is required for the development of ischemic neuronal death. J Neurosci 2005, 25(10): 2647-57.
79. Jones, S.E., Jomary, C., Grist, J., Stewart, H.J. and Neal, M.J. Modulated expression of secreted frizzled-related proteins in human retinal degeneration. Neuroreport 2000, 11(18): 3963-7.
80. Jones, S.E., Jomary, C., Grist, J., Stewart, H.J. and Neal, M.J. Altered expression of secreted frizzled-related protein-2 in retinitis pigmentosa retinas. Invest Ophthalmol Vis Sci 2000, 41(6): 1297-301.
81. Rattner, A., Hsieh, J.C., Smallwood, P.M., Gilbert, D.J., Copeland, N.G., Jenkins, N.A. and Nathans, J. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci U S A 1997, 94(7): 2859-63.
82. Melkonyan, H.S., Chang, W.C., Shapiro, J.P., Mahadevappa, M., Fitzpatrick, P.A., Kiefer, M.C., Tomei, L.D. and Umansky, S.R. SARPs: A family of secreted apoptosis-related proteins. Proc Natl Acad Sci U S A 1997, 94(25): 13636-41.
83. Baranski, M., Berdougo, E., Sandler, J.S., Darnell, D.K. and Burrus, L.W. The dynamic expression pattern of frzb-1 suggests multiple roles in chick development. Dev Biol 2000, 217(1): 25-41.
84. de Vrij, F.M., Fischer, D.F., van Leeuwen, F.W. and Hol, E.M. Protein quality control in Alzheimer's disease by the ubiquitin proteasome system. Prog Neurobiol 2004, 74(5): 249-70.
85. Oddo, S. The ubiquitin-proteasome system in Alzheimer's disease. J Cell Mol Med 2008, 12(2): 363-73.
86. Liu, C., Li, Y., Semenov, M. et al. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108(6): 837-47.
87. Aberle, H., Bauer, A., Stappert, J., Kispert, A. and Kemler, R. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 1997, 16(13): 3797-804.
88. Farias, G.G., Valles, A.S., Colombres, M., Godoy, J.A., Toledo, E.M., Lukas, R.J., Barrantes, F.J. and Inestrosa, N.C. Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 2007, 27(20): 5313-25.
89. Fuenzalida, K., Quintanilla, R., Ramos, P., Piderit, D., Fuentealba, R.A., Martinez, G., Inestrosa, N.C. and Bronfman, M. Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J Biol Chem 2007, 282(51): 37006-15.
90. Toledo, E.M., Colombres, M. and Inestrosa, N.C. Wnt signaling in neuroprotection and stem cell differentiation. Prog Neurobiol 2008, 86(3): 281-96.
91. Chacon, M.A., Varela-Nallar, L. and Inestrosa, N.C. Frizzled-1 is involved in the neuroprotective effect of Wnt3a against Abeta oligomers. J Cell Physiol 2008, 217(1): 215-27.
92. Lein, E.S., Hawrylycz, M.J., Ao, N. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445(7124): 168-76.
93. Varela-Nallar, L., Grabowski, C.P., Alfaro, I.E., Alvarez, A.R. and Inestrosa, N.C. Role of the Wnt receptor Frizzled-1 in presynaptic differentiation and function. Neural Dev 2009, 4: 41-55.
94. Ferreira, S.T., Vieira, M.N. and De Felice, F.G. Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases. IUBMB Life 2007, 59(4-5): 332-45.
95. Bijur, G.N., De Sarno, P. and Jope, R.S. Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J Biol Chem 2000, 275(11): 7583-90.
96. Bijur, G.N. and Jope, R.S. Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta. J Biol Chem 2001, 276(40): 37436-42.
97. Phiel, C.J., Wilson, C.A., Lee, V.M. and Klein, P.S. GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 2003, 423(6938): 435-9.
98. Sun, X., Sato, S., Murayama, O., Murayama, M., Park, J.M., Yamaguchi, H. and Takashima, A. Lithium inhibits amyloid secretion in COS7 cells transfected with amyloid precursor protein C100. Neurosci Lett 2002, 321(1-2): 61-4.
99. Hardy, J. Alzheimer's disease: The amyloid cascade hypothesis: An update and reappraisal. J Alzheimers Dis 2006, 9(Suppl. 3): 151-3.
100. Farias, G.G., Godoy, J.A., Hernandez, F., Avila, J., Fisher, A. and Inestrosa, N.C. M1 muscarinic receptor activation protects neurons from beta-amyloid toxicity. A role for Wnt signaling pathway. Neurobiol Dis 2004, 17(2): 337-48.
101. Caccamo, A., Oddo, S., Billings, L.M., Green, K.N., Martinez-Coria, H., Fisher, A. and LaFerla, F.M. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 2006, 49(5): 671-82.
102. Lehrke, M. and Lazar, M.A. The many faces of PPARgamma. Cell 2005, 123(6): 993-9.
103. Schoonjans, K., Peinado-Onsurbe, J., Lefebvre, A.M., Heyman, R.A., Briggs, M., Deeb, S., Staels, B. and Auwerx, J. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J 1996, 15(19): 5336-48.
104. Willson, T.M. and Wahli, W. Peroxisome proliferator-activated receptor agonists. Curr Opin Chem Biol 1997, 1(2): 235-41.
105. Inestrosa, N.C., Godoy, J.A., Quintanilla, R.A., Koenig, C.S. and Bronfman, M. Peroxisome proliferator-activated receptor gamma is expressed in hippocampal neurons and its activation prevents beta-amyloid neurodegeneration: Role of Wnt signaling. Exp Cell Res 2005, 304(1): 91-104.
106. Heneka, M.T., Sastre, M., Dumitrescu-Ozimek, L. et al. Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain 2005, 128(Pt. 6): 1442-53.
107. Pedersen, W.A. and Flynn, E.R. Insulin resistance contributes to aberrant stress responses in the Tg2576 mouse model of Alzheimer's disease. Neurobiol Dis 2004, 17(3): 500-6.
108. Toledo, E.M. and Inestrosa, N.C. Activation of Wnt signaling by lithium and rosiglitazone reduced spatial memory impairment and neurodegeneration in brains of an APPswe/PSEN1DeltaE9 mouse model of Alzheimer's disease. Mol Psychiatry 2009. Epub ahead of print.
109. Cerpa, W., Hancke, J.L., Morazzoni, P., Bombardelli, E., Riva, A., Marin, P.P. and Inestrosa, N.C. The Hyperforin Derivative IDN5706 Occludes Spatial Memory Impairments and Neuropathological Changes in a Double Transgenic Alzheimer's Mouse Model. Curr Alzheimer Res 2009. Epub ahead of print.
110. Hardy, J. and Selkoe, D.J. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 2002, 297(5580): 353-6.
111. Small, D.H., Mok, S.S. and Bornstein, J.C. Alzheimer's disease and Abeta toxicity: From top to bottom. Nat Rev Neurosci 2001, 2(8): 595-8.
112. Lacor, P.N., Buniel, M.C., Chang, L. et al. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 2004, 24(45): 10191-200.
113. Shankar, G.M., Bloodgood, B.L., Townsend, M., Walsh, D.M., Selkoe, D.J. and Sabatini, B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 2007, 27(11): 2866-75.
114. Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., Rowan, M.J. and Selkoe, D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416(6880): 535-9.
115. Almeida, C.G., Tampellini, D., Takahashi, R.H., Greengard, P., Lin, M.T., Snyder, E.M. and Gouras, G.K. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 2005, 20(2): 187-98.
116. Roselli, F., Tirard, M., Lu, J., Hutzler, P., Lamberti, P., Livrea, P., Morabito, M. and Almeida, O.F. Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. J Neurosci 2005, 25(48): 11061-70.
117. Dinamarca, M.C., Colombres, M., Cerpa, W., Bonansco, C. and Inestrosa, N.C. Beta-amyloid oligomers affect the structure and function of the postsynaptic region: Role of the Wnt signaling pathway. Neurodegener Dis 2008, 5(3-4): 149-52.
118. Iwamoto, T., Yamada, Y., Hori, K., Watanabe, Y., Sobue, K. and Inui, M. Differential modulation of NR1-NR2A and NR1-NR2B subtypes of NMDA receptor by PDZ domain-containing proteins. J Neurochem 2004, 89(1): 100-8.
119. Dong, Y.N., Waxman, E.A. and Lynch, D.R. Interactions of postsynaptic density-95 and the NMDA receptor 2 subunit control calpain-mediated cleavage of the NMDA receptor. J Neurosci 2004, 24(49): 11035-45.
120. Niethammer, M., Kim, E. and Sheng, M. Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 1996, 16(7): 2157-63.
121. Chen, L., Chetkovich, D.M., Petralia, R.S., Sweeney, N.T., Kawasaki, Y., Wenthold, R.J., Bredt, D.S. and Nicoll, R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 2000, 408(6815): 936-43.
122. McGee, A.W. and Bredt, D.S. Assembly and plasticity of the glutamatergic postsynaptic specialization. Curr Opin Neurobiol 2003, 13(1): 111-8.
123. Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., Sisodia, S. and Malinow, R. APP processing and synaptic function. Neuron 2003, 37(6): 925-37.
124. Inestrosa, N.C., Varela-Nallar, L., Grabowski, C.P. and Colombres, M. Synaptotoxicity in Alzheimer's disease: The Wnt signaling pathway as a molecular target. IUBMB Life 2007, 59(4-5): 316-21.
125. Cerpa, W., Farias, G.G., Fuelzalida, M., Bonansco, C. and Inestrosa, N.C. Wnt-5a occludes Abeta oligomer-induced depression of glutamatergic transmission in hippocompal neurons. Mol Neurodegener 2009. In press.
126. Farias, G.G., Alfaro, I.E., Cerpa, W., Grabowski, C.P., Godoy, J.A., Bonansco, C. and Inestrosa, N.C. Wnt-5a/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons. J Biol Chem 2009, 284(23): 15857-66.
127. Shankar, G.M., Li, S., Mehta, T.H. et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008, 14(8): 837-42.
128. Malinow, R. and Tsien, R.W. Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 1990, 346(6280): 177-80.
129. He, F., Xiong, W., Yu, X. et al. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development 2008, 135(23): 3871-9.
130. Nomachi, A., Nishita, M., Inaba, D., Enomoto, M., Hamasaki, M. and Minami, Y. Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 2008, 283(41): 27973-81.
131. Lin, Y., Jover-Mengual, T., Wong, J., Bennett, M.V. and Zukin, R.S. PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 2006, 103(52): 19902-7.