Amyloid β accelerates phosphorylation of tau and neurofibrillary tangle formation in an amyloid precursor protein and tau double-transgenic mouse model

Journal of Neuroscience Research

Volumn 88, Issue 16, 2010, Pages 3547-3554

  Seino, Yusuke ^a   Kawarabayashi, Takeshi ^b   Wakasaya, Yasuhito ^b   Watanabe, Mitsunori ^b   Takamura, Ayumi ^b   Yamamoto Watanabe, Yukiko ^b   Kurata, Tomoko ^c   Abe, Koji ^c   Ikeda, Masaki ^d   Westaway, David ^e   Murakami, Tetsuro ^f   Hyslop, Peter St George ^f   Matsubara, Etsuro ^b   Shoji, Mikio ^b  

^a Mutsu General Hospital   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

^c OKAYAMA UNIVERSITY   (Japan)

^d GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF ALBERTA   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alzheimer's disease; Double transgenic mouse; Neurofibrillary tangles

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; TAU PROTEIN;

AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; MATING; MOUSE; NERVE CELL; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TAUOPATHY; TRANSGENIC MOUSE; WHITE MATTER;

AGE FACTORS; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID NEUROPATHIES; ANIMALS; BRAIN DISEASES; DISEASE MODELS, ANIMAL; LONGITUDINAL STUDIES; MICE; MICE, TRANSGENIC; NEUROFIBRILLARY TANGLES; NEURONS; TAU PROTEINS; TAUOPATHIES;

EID: 78049433259     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22516     Document Type: Article

References (32)

1. Caccamo A, Oddo S, Tran LX, LaFerla FM. 2007. Lithium reduces tau phosphorylation but not Aβ or working memory deficits in a transgenic model with both plaques and tangles. Am J Pathol 170: 1669-1675.
2. de Calignon A, Spires-Jones TL, Pitstick R, Carlson GA, Hyman BT. 2009. Tangle-bearing neurons survive despite disruption of membrane integrity in a mouse model of tauopathy. J Neuropathol Exp Neurol 68: 757-761.
3. Ghiso JA, Holton J, Miravalle L, Calero M, Lashley T, Vidal R, Houlden H, Wood N, Neubert TA, Rostagno A, Plant G, Revesz T, Frangione B. 2001. Systemic amyloid deposits in familial British dementia. J Biol Chem 276: 43909-43914.
4. Götz J, Chen F, van Dorpe J, Nitsch RM. 2001. Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Aβ42 fibrils. Science 293: 1491-1495.
5. Guix FX, Ill-Raga G, Bravo R, Nakaya T, de Fabritiis G, Coma M, Miscione GP, Villà-Freixa J, Suzuki T, Fernàndez-Busquets X, Valverde MA, de Strooper B, Muñoz FJ. 2009. Amyloid-dependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain 132: 1335-1345.
6. Hardy J. 2009. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J Neurochem 110: 1129-1134.
7. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K. 1998. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4: 97-100.
8. Holmes C, Boche D, Wilkinson D, Yadegarfar G, Hopkins V, Bayer A, Jones RW, Bullock R, Love S, Neal JW, Zotova E, Nicoll JA. 2008. Long-term effects of Aβ42 immunization in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372: 216-223.
9. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P. 1998. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393: 702-705.
10. Kawarabayashi T, Shoji M, Younkin LH, Wen-Lang L, Dickson DW, Murakami T, Matsubara E, Abe K, Ashe KH, Younkin SG. 2004. Dimeric amyloid β protein rapidly accumulates in lipid rafts followed by apolipoprotein E and phosphorylated tau accumulation in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 24: 3801-3809.
11. LaFerla FM, Oddo S. 2005. Alzheimer's disease: Aβ, tau and synaptic dysfunction. Trends Mol Med 11: 170-176.
12. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E. 2001. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293: 1487-1491.
13. Love S, Bridges LR, Case CP. 1995. Neurofibrillary tangles in Niemann-Pick disease type C. Brain 118: 119-129.
14. Murakami T, Paitel E, Kawarabayashi T, Ikeda M, Chishti MA, Janus C, Matsubara E, Sasaki A, Kawarai T, Phinney AL, Harigaya Y, Horne P, Egashira N, Mishima K, Hanna A, Yang J, Iwasaki, K, Takahashi M, Fujiwara M, Ishiguro K, Bergeron C, Carlson GA, Abe K, Westaway D, St. George-Hyslop P, Shoji M. 2006. Cortical neuronal and glial pathology in TgTauP301L transgenic mice: neuronal degeneration, memory disturbance, and phenotypic variation. Am J Pathol 169: 1365-1375.
15. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM. 2004. Aβ immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43: 321-332.
16. Oddo S, Vasilevko V, Caccamo A, Kitazawa M, Cribbs DH, LaFerla FM. 2006a. Reduction of soluble Aβ and tau, but not soluble Aβ alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J Biol Chem 281: 39413-39423.
17. Oddo S, Caccamo A, Tran L, Lambert MP, Glabe CG, Klein WL, LaFerla FM. 2006b. Temporal profile of amyloid-β (Aβ) oligomerization in an in vivo model of Alzheimer disease. A link between Aβ and tau pathology. J Biol Chem 281: 1599-1604.
18. Oddo S, Caccamo A, Cheng D, Jouleh B, Torp R, LaFerla FM. 2007. Genetically augmenting tau levels does not modulate the onset or progression of Aβ pathology in transgenic mice. J Neurochem 102: 1053-1063.
19. Oddo S, Caccamo A, Tseng B, Cheng D, Vasilevko V, Cribbs DH, LaFerla FM. 2008. Blocking Aβ42 accumulation delays the onset and progression of tau pathology via the C terminus of heat shock protein70-interacting protein: a mechanistic link between Aβ and tau pathology. J Neurosci 28: 12163-12175.
20. Oddo S, Caccamo A, Cheng D, LaFerla FM. 2009. Genetically altering Aβ distribution from the brain to the vasculature ameliorates tau pathology. Brain Pathol 19: 421-430.
21. Paquet D, Bhat R, Sydow A, Mandelkow EM, Berg S, Hellberg S, Fälting J, Distel M, Köster RW, Schmid B, Haass C. 2009. A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest 119: 1382-1395.
22. Paulson JB, Ramsden M, Forster C, Sherman MA, McGowan E, Ashe KH. 2008. Amyloid plaque and neurofibrillary tangle pathology in a regulatable mouse model of Alzheimer's disease. Am J Pathol 173: 762-772.
23. Pérez M, Ribe E, Rubio A, Lim F, Morán MA, Ramos PG, Ferrer I, Isla MT, Avila J. 2005. Characterization of a double (amyloid precursor protein-tau) transgenic: tau phosphorylation and aggregation. Neuroscience 130: 339-347.
24. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A. 2002. Tau is essential to β-amyloid-induced neurotoxicity. Proc Natl Acad Sci U S A 99: 6364-6369.
25. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L. 2007. Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
26. 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, Ashe KH. 2005. Tau suppression in a neurodegenerative mouse model improves memory function. Science 309: 476-481.
27. Spires TL, Orne JD, SantaCruz K, Pitstick R, Carlson GA, Ashe KH, Hyman BT. 2006. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am J Pathol 168: 1598-1607.
28. Spires-Jones TL, de Calignon A, Matsui T, Zehr C, Pitstick R, Wu HY, Osetek JD, Jones PB, Bacskai BJ, Feany MB, Carlson GA, Ashe KH, Lewis J, Hyman BT. 2008. In vivo imaging reveals dissociation between caspase activation and acute neuronal death in tangle-bearing neurons. J Neurosci 28: 862-867.
29. Spires-Jones TL, Stoothoff WH, de Calignon A, Jones PB, Hyman BT. 2009. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci 32: 150-159.
30. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS. 2005. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-1288.
31. Terwel D, Muyllaert D, Dewachter I, Borghgraef P, Croes S, Devijver H, Van Leuven F. 2008. Amyloid activates GSK-3β to aggravate neuronal tauopathy in bigenic mice. Am J Pathol 172: 786-798.
32. Tomidokoro Y, Ishiguro K, Harigaya Y, Matsubara E, Ikeda M, Park JM, Yasutake K, Kawarabayashi T, Okamoto K, Shoji M. 2001. Aβ amyloidosis induces the initial stage of tau accumulation in APP(Sw) mice. Neurosci Lett 299: 169-172.