Tau-knockout mice show reduced GSK3-induced hippocampal degeneration and learning deficits

Neurobiology of Disease

Volumn 37, Issue 3, 2010, Pages 622-629

  de Barreda, Elena Gómez ^a   Pérez, Mar ^a   Ramos, Pilar Gómez ^a   de Cristobal, Javier ^b   Martín Maestro, Patricia ^a   Morán, Asunción ^a   Dawson, Hana N ^c   Vitek, Michael P ^c   Lucas, José J ^a,d   Hernández, Félix ^a,d   Avila, Jesús ^a,d  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Noscira SA   (Spain)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Alzheimer disease; Dentate gyrus; GSK 3; tau

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; GENE OVEREXPRESSION; GLIOSIS; GLYCOGEN SYNTHESIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; ATROPHY; BETA CATENIN; BIOLOGICAL MARKERS; CELL NUCLEUS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLIOSIS; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; LEARNING DISORDERS; MAZE LEARNING; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; NEURONS; PHOSPHORYLATION; TAU PROTEINS;

EID: 75949107662     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.11.017     Document Type: Article

References (46)

1. Alonso A.D., Grundke-Iqbal I., Barra H.S., and Iqbal K. Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 298-303
2. Alvarez G., Munoz-Montano J.R., Satrustegui J., Avila J., Bogonez E., and Diaz-Nido J. Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett. 453 (1999) 260-264
3. Anderton B.H. Alzheimer's disease: clues from flies and worms. Curr. Biol. 9 (1999) R106-109
4. Avila J. Tau phosphorylation and aggregation in Alzheimer's disease pathology. FEBS Lett. 580 (2006) 2922-2927
5. Baki L., Shioi J., Wen P., Shao Z., Schwarzman A., Gama-Sosa M., Neve R., and Robakis N.K. PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J. 23 (2004) 2586-2596
6. Barth A.I., Nathke I.S., and Nelson W.J. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell. Biol. 9 (1997) 683-690
7. Busciglio J., Lorenzo A., Yeh J., and Yankner B.A. beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14 (1995) 879-888
8. Dawson H.N., Ferreira A., Eyster M.V., Ghoshal N., Binder L.I., and Vitek M.P. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell. Sci. 114 (2001) 1179-1187
9. Engel T., Hernandez F., Avila J., and Lucas J.J. Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci. 26 (2006) 5083-5090
10. Engel T., Lucas J.J., Gomez-Ramos P., Moran M.A., Avila J., and Hernandez F. Cooexpression of FTDP-17 tau and GSK-3beta in transgenic mice induce tau polymerization and neurodegeneration. Neurobiol. Aging 27 (2006) 1258-1268
11. Ferreira A., Lu Q., Orecchio L., and Kosik K.S. Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar A beta. Mol. Cell. Neurosci. 9 (1997) 220-234
12. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349 (1991) 704-706
13. Goedert M., Spillantini M.G., Potier M.C., Ulrich J., and Crowther R.A. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J. 8 (1989) 393-399
14. Gomez-Ramos A., Diaz-Hernandez M., Cuadros R., Hernandez F., and Avila J. Extracellular tau is toxic to neuronal cells. FEBS Lett. 580 (2006) 4842-4850
15. Gotz J., Chen F., van Dorpe J., and Nitsch R.M. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 293 (2001) 1491-1495
16. Grimes C.A., and Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 65 (2001) 391-426
17. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T., and Hirokawa N. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369 (1994) 488-491
18. Hernandez F., and Avila J. The role of glycogen synthase kinase 3 in the early stages of Alzheimers' disease. FEBS Lett. 582 (2008) 3848-3854
19. 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. 83 (2002) 1529-1533
20. Hetman M., Cavanaugh J.E., Kimelman D., and Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20 (2000) 2567-2574
21. Ishiguro K., Shiratsuchi A., Sato S., Omori A., Arioka M., Kobayashi S., Uchida T., and Imahori K. Glycogen synthase kinase 3 beta is identical to tau protein kinase I generating several epitopes of paired helical filaments. FEBS Lett. 325 (1993) 167-172
22. Jackson G.R., Wiedau-Pazos M., Sang T.K., Wagle N., Brown C.A., Massachi S., and Geschwind D.H. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34 (2002) 509-519
23. Kimura T., Yamashita S., Fukuda T., Park J.M., Murayama M., Mizoroki T., Yoshiike Y., Sahara N., and Takashima A. Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J. 26 (2007) 5143-5152
24. Li H.L., Wang H.H., Liu S.J., Deng Y.Q., Zhang Y.J., Tian Q., Wang X.C., Chen X.Q., Yang Y., Zhang J.Y., Wang Q., Xu H., Liao F.F., and Wang J.Z. Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 3591-3596
25. Linseman D.A., Butts B.D., Precht T.A., Phelps R.A., Le S.S., Laessig T.A., Bouchard R.J., Florez-McClure M.L., and Heidenreich K.A. Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J. Neurosci. 24 (2004) 9993-10002
26. Liu T., Perry G., Chan H.W., Verdile G., Martins R.N., Smith M.A., and Atwood C.S. Amyloid-beta-induced toxicity of primary neurons is dependent upon differentiation-associated increases in tau and cyclin-dependent kinase 5 expression. J. Neurochem. 88 (2004) 554-563
27. 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. 20 (2001) 27-39
28. Magdesian M.H., Carvalho M.M., Mendes F.A., Saraiva L.M., Juliano M.A., Juliano L., Garcia-Abreu J., and Ferreira S.T. Amyloid-beta binds to the extracellular cysteine-rich domain of Frizzled and inhibits Wnt/beta-catenin signaling. J. Biol. Chem. 283 (2008) 9359-9368
29. Manji H.K., Moore G.J., and Chen G. Lithium at 50: have the neuroprotective effects of this unique cation been overlooked?. Biol. Psychiatry 46 (1999) 929-940
30. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K., and Ihara Y. Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 270 (1995) 823-829
31. Novak M., Jakes R., Edwards P.C., Milstein C., and Wischik C.M. Difference between the tau protein of Alzheimer paired helical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 5837-5841
32. Paxinos G.F.K. The Mouse Brain (2001), Academic Press
33. 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. 58 (1999) 1010-1019
34. Perez M., Santa-Maria I., Gomez de Barreda E., Zhu X., Cuadros R., Cabrero J.R., Sanchez-Madrid F., Dawson H.N., Vitek M.P., Perry G., Smith M.A., and Avila J. Tau-an inhibitor of deacetylase HDAC6 function. J. Neurochem. 109 (2009) 1756-1766
35. Price D.L., and Sisodia S.S. Mutant genes in familial Alzheimer's disease and transgenic models. Annu. Rev. Neurosci. 21 (1998) 479-505
36. Ramon-Cueto A., and Avila J. Differential expression of microtubule-associated protein 1B phosphorylated isoforms in the adult rat nervous system. Neuroscience 77 (1997) 485-501
37. Rapoport M., Dawson H.N., Binder L.I., Vitek M.P., and Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6364-6369
38. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.Q., and Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 316 (2007) 750-754
39. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., Forster C., Yue M., Orne J., Janus C., Mariash A., Kuskowski M., Hyman B., Hutton M., and Ashe K.H. Tau suppression in a neurodegenerative mouse model improves memory function. Science 309 (2005) 476-481
40. Shiurba R.A., Ishiguro K., Takahashi M., Sato K., Spooner E.T., Mercken M., Yoshida R., Wheelock T.R., Yanagawa H., Imahori K., and Nixon R.A. Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology. Brain Res. 737 (1996) 119-132
41. Small S.A., and Duff K. Linking Abeta and tau in late-onset Alzheimer's disease: a dual pathway hypothesis. Neuron 60 (2008) 534-542
42. Takashima A., Murayama M., Murayama O., Kohno T., Honda T., Yasutake K., Nihonmatsu N., Mercken M., Yamaguchi H., Sugihara S., and Wolozin B. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9637-9641
43. Townsend M., Mehta T., and Selkoe D.J. Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway. J. Biol. Chem. 282 (2007) 33305-33312
44. Vincent I., Rosado M., Kim E., and Davies P. Increased production of paired helical filament epitopes in a cell culture system reduces the turnover of tau. J. Neurochem. 62 (1994) 715-723
45. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 9 (1990) 2431-2438
46. Zhang Z., Hartmann H., Do V.M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Sommer B., van de Wetering M., Clevers H., Saftig P., De Strooper B., He X., and Yankner B.A. Destabilization of beta-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395 (1998) 698-702