A decade of tau transgenic animal models and beyond

Brain Pathology

Volumn 17, Issue 1, 2007, Pages 91-103

  Götz, Jürgen ^a   Deters, Natasha ^a   Doldissen, Amy ^a   Bokhari, Laita ^a   Ke, Yazi ^a   Wiesner, Andreas ^a   Schonrock, Nicole ^a   Ittner, Lars M ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AF 267B; ALPHA BETA ANTIBODY; ANTIBODY; K 252A; LITHIUM; MUSCARINIC AGENT; RAPAMYCIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ACTIVE IMMUNIZATION; ALZHEIMER DISEASE; CONFERENCE PAPER; DEGENERATIVE DISEASE; DISEASE COURSE; DISEASE MODEL; GENE ACTIVITY; HUMAN; INVERTEBRATE; MEDICAL RESEARCH; NONHUMAN; PASSIVE IMMUNIZATION; PATHOPHYSIOLOGY; TRANSGENIC MOUSE; TREATMENT INDICATION; WILD TYPE;

ALZHEIMER DISEASE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DEMENTIA; DISEASE MODELS, ANIMAL; DROSOPHILA; MICE; MICE, TRANSGENIC; TAU PROTEINS;

EID: 33847199377     PISSN: 10156305     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2007.00051.x     Document Type: Conference Paper

References (156)

1. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC, Atzori C, Migheli A, Crowther RA, Ghetti B, Spillantini MG, Goedert M (2002) Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 22:9340-9351.
2. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, Barde YA, Duff K, Davies P (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 86:582-590.
3. Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, Davies P (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25:5446-5454.
4. Arendt T (2003) Synaptic plasticity and cell cycle activation in neurons are alternative effector pathways: the "Dr. Jekyll and Mr. Hyde concept" of Alzheimer's disease or the yin and yang of neuroplasticity. Prog Neurobiol 71:83-248.
5. Arendt T, Holzer M, Fruth R, Brückner MK, Gärtner U (1995) Paired helical filament-like phosphorylation of tau, deposition of beta/A4-amyloid and memory impairment in rat induced by chronic inhibition of phosphatase 1 and 2A. Neuroscience 69:691-698.
6. Arnold SE, Han LY, Clark CM, Grossman M, Trojanowski JQ (2000) Quantitative neurohistological features of frontotemporal degeneration. Neurobiol Aging 21:913-919.
7. Augustinack JC, Schneider A, Mandelkow EM, Hyman BT (2002) Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol (Berl) 103:26-35.
8. Bancher C, Grundke-Iqbal I, Iqbal K, Fried VA, Smith HT, Wisniewski HM (1991) Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease. Brain Res 539:11-18.
9. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T (2000) Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
10. Baumeister R, Ge L (2002) The worm in us - caenorhabditis elegans as a model of human disease. Trends Biotechnol 20:147-148.
11. Berger Z, Ravikumar B, Menzies FM, Oroz LG, Underwood BR, Pangalos MN, Schmitt I, Wullner U, Evert BO, O'Kane CJ, Rubinsztein DC (2006) Rapamycin alleviates toxicity of different aggregate-prone proteins. Hum Mol Genet 15:433-442.
12. Bhaskar K, Yen SH, Lee G (2005) Disease-related modifications in tau affect the interaction between Fyn and Tau. J Biol Chem 280:35119-35125.
13. Brion JP, Tremp G, Octave JN (1999) Transgenic expression of the shortest human tau affects its compartmentalization and its phosphorylation as in the pretangle stage of Alzheimer's disease. Am J Pathol 154:255-270.
14. Broggio E, Pluchon C, Ingrand P, Gil R (2001) Taste impairment in Alzheimer's disease. Rev Neurol (Paris) 157:409-413.
15. Buée L, Bussière T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130.
16. Bugiani O, Murrell JR, Giaccone G, Hasegawa M, Ghigo G, Tabaton M, Morbin M, Primavera A, Carella F, Solaro C, Grisoli M, Savoiardo M, Spillantini MG, Tagliavini F, Goedert M, Ghetti B (1999) Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol 58:667-677.
17. Caccamo A, Oddo S, Billings LM, Green KN, Martinez-Coria H, Fisher A, LaFerla FM (2006) M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49:671-682.
18. Chau KW, Chan WY, Shaw PC, Chan HY (2006) Biochemical investigation of Tau protein phosphorylation status and its solubility properties in Drosophila. Biochem Biophys Res Commun 346:150-159.
19. Chee FC, Mudher A, Cuttle MF, Newman TA, MacKay D, Lovestone S, Shepherd D (2005) Overexpression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Neurobiol Dis 20:918-928.
20. Chen F, David D, Ferrari A, Götz J (2004) Post-translational modifications of tau - role in human tauopathies and modeling in transgenic animals. Curr Drug Targets 5:503-515.
21. Chen F, Wollmer MA, Hoerndli F, Münch G, Kuhla B, Rogaev EI, Tsolaki M, Papassotiropoulos A, Götz J (2004) Role for glyoxalase I in Alzheimer's disease. Proc Natl Acad Sci USA 101:7687-7692.
22. Cripps D, Thomas SN, Jeng Y, Yang F, Davies P, Yang AJ (2006) Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J Biol Chem 281:10825-10838.
23. David D, Hoerndli F, Götz J (2005) Functional Genomics meets neurodegenerative disorders Part I: transcriptomic and proteomic technology. Prog Neurobiol 76:153-168.
24. David DC, Hauptmann S, Scherping I, Schuessel K, Keil U, Rizzu P, Ravid R, Dröse S, Brandt U, Müller WE, Eckert E, Götz J (2005) Proteomic and functional analysis reveal a mitochondrial dysfunction in P301L tau transgenic mice. J Biol Chem 280:23802-23814.
25. David DC, Ittner LM, Gehrig P, Nergenau D, Shepherd C, Halliday G, Götz J (2006) β-Amyloid treatment of two complementary P301L tauexpressing Alzheimer's disease models reveals similar deregulated cellular processes. Proteomics 6:6566-6577.
26. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:1179-1187.
27. Delacourte A, Sergeant N, Champain D, Wattez A, Maurage CA, Lebert F, Pasquier F, David JP (2002) Nonoverlapping but synergetic tau and APP pathologies in sporadic Alzheimer's disease. Neurology 59:398-407.
28. Delobel P, Lavenir I, Ghetti B, Holzer M, Goedert M (2006) Cell-cycle markers in a transgenic mouse model of human tauopathy: increased levels of cyclin-dependent kinase inhibitors p21Cip1 and p27Kip1. Am J Pathol 168:878-887.
29. Dickey CA, Yue M, Lin WL, Dickson DW, Dunmore JH, Lee WC, Zehr C, West G, Cao S, Clark AM, Caldwell GA, Caldwell KA, Eckman C, Patterson C, Hutton M, Petrucelli L (2006) Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species. J Neurosci 26:6985-6996.
30. Dodart JC, Bales KR, Gannon KS, Greene SJ, DeMattos RB, Mathis C, DeLong CA, Wu S, Wu X, Holtzman DM, Paul SM (2002) Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 5:452-457.
31. Dou F, Netzer WJ, Tanemura K, Li F, Hartl FU, Takashima A, Gouras GK, Greengard P, Xu H (2003) Chaperones increase association of tau protein with microtubules. Proc Natl Acad Sci USA 100:721-726.
32. Duff K, Knight H, Refolo LM, Sanders S, Yu X, Picciano M, Malester B, Hutton M, Adamson J, Goedert M, Bürki K, Davies P (2000) Characterization of pathology in transgenic mice overexpressing human genomic and cDNA tau transgenes. Neurobiol Dis 7:87-98.
33. Engel T, Lucas JJ, Gomez-Ramos P, Moran MA, Avila J, Hernandez F (2006) Co-expression of FTDP-17 tau and GSK-3β in transgenic mice induce tau polymerization and neurodegeneration. Neurobiol Aging 27:1258-1268.
34. Engel T, Hernandez F, Avila J, Lucas JJ (2006) Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J Neurosci 26:5083-5090.
35. Ferrari A, Hoerndli F, Baechi T, Nitsch RM, Götz J (2003) Beta-amyloid induces PHF-like tau filaments in tissue culture. J Biol Chem 278:40162-40168.
36. Forman MS, Lal D, Zhang B, Dabir DV, Swanson E, Lee VM, Trojanowski JQ (2005) Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. J Neurosci 25:3539-3550.
37. Francis R, McGrath G, Zhang J, Ruddy DA, Sym M, Apfeld J, Nicoll M, Maxwell M, Hai B, Ellis MC, Parks AL, Xu W, Li J, Gurney M, Myers RL, Himes CS, Hiebsch R, Ruble C, Nye JS, Curtis D (2002) aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev Cell 3:85-97.
38. Geula C, Wu CK, Saroff D, Lorenzo A, Yuan M, Yankner BA (1998) Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity. Nat Med 4:827-831.
39. Giannakopoulos P, Herrmann FR, Bussière T, Bouras C, Kovari E, Perl DP, Morrison JH, Gold G, Hof PR (2003) Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease. Neurology 60:1495-1500.
40. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
41. Goedert M, Wischik CM, Crowther RA, Walker JE, Klug A (1988) Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc Natl Acad Sci USA 85:4051-4055.
42. Goedert M, Jakes R, Crowther RA, Six J, Lübke U, Vandermeeren M, Cras P, Trojanowski JQ, Lee VMY (1993) The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 90:5066-5070.
43. Goedert M, Spillantini MG, Jakes R, Crowther RA, Vanmechelen E, Probst A, Götz J, Bürki K, Cohen P (1995) Molecular dissection of the paired helical filament. Neurobiol Aging 16:325-334.
44. Goedert M, Spillantini MG, Crowther RA, Chen SG, Parchi P, Tabaton M, Lanska DJ, Markesbery WR, Wilhelmsen KC, Dickson DW, Petersen RB, Gambetti P (1999) Tau gene mutation in familial progressive subcortical gliosis. Nat Med 5:454-457.
45. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 41:17-24.
46. Gong CX, Singh TJ, Grundke-Iqbal I, Iqbal K (1993) Phosphoprotein phosphatase activities in Alzheimer disease brain. J Neurochem 61:921-927.
47. Gosal D, Ross OA, Toft M (2006) Parkinson's disease: the genetics of a heterogeneous disorder. Eur J Neurol 13:616-627.
48. Götz J (2001) Tau and transgenic animal models. Brain Res Brain Res Rev 35:266-286.
49. Götz J, Probst A, Spillantini MG, Schäfer T, Jakes R, Bürki K, Goedert M (1995) Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO J 14:1304-1313.
50. Götz J, Chen F, Barmettler R, Nitsch RM (2001) Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 276:529-534.
51. Götz J, Chen F, van Dorpe J, Nitsch RM (2001) Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Abeta 42 fibrils. Science 293:1491-1495.
52. Götz J, Tolnay M, Barmettler R, Chen F, Probst A, Nitsch RM (2001) Oligodendroglial tau filament formation in transgenic mice expressing G272V tau. Eur J Neurosci 13:2131-2140.
53. Götz J, Streffer JR, David D, Schild A, Hoerndli F, Pennanen L, Kurosinski P, Chen F (2004) Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy. Mol Psychiatry 9:664-683.
54. Götz J, Ittner LM, Kins S (2006) Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer's disease? J Neurochem 98:993-1006.
55. Götz J, Ittner LM, Schonrock N (2006) Alzheimer's disease and frontotemporal dementia: prospects of a tailored therapy? Med J Aust 185:381-384.
56. Hall GF, Cohen MJ (1983) Extensive dendritic sprouting induced by close axotomy of central neurons in the lamprey. Science 222:518-521.
57. Hall GF, Chu B, Lee G, Yao J (2000) Human tau filaments induce microtubule and synapse loss in an in vivo model of neurofibrillary degenerative disease. J Cell Sci 113:1373-1387.
58. Hall GF, Lee VM, Lee G, Yao J (2001) Staging of neurofibrillary degeneration caused by human tau overexpression in a unique cellular model of human tauopathy. Am J Pathol 158:235-246.
59. Hall GF, Lee S, Yao J (2002) Neurofibrillary degeneration can be arrested in an in vivo cellular model of human tauopathy by application of a compound which inhibits tau filament formation in vitro. J Mol Neurosci 19:253-260.
60. Harada A, Oguchi K, Okabe S, Kuno J, Terada S, Ohshima T, Sato-Yoshitake R, Takei Y, Noda T, Hirokawa N (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369:488-491.
61. Hernandez F, Lim F, Lucas JJ, Perez-Martin C, Moreno F, Avila J (2002) Transgenic mouse models with tau pathology to test therapeutic agents for Alzheimer's disease. Mini Rev Med Chem 2:51-58.
62. Higuchi M, Ishihara T, Zhang B, Hong M, Andreadis A, Trojanowski J, Lee VMY (2002) Transgenic mouse model of tauopathies with glial pathology and nervous system degeneration. Neuron 35:433-446.
63. Higuchi M, Zhang B, Forman MS, Yoshiyama Y, Trojanowski JQ, Lee VMY (2005) Axonal degeneration induced by targeted expression of mutant human tau in oligodendrocytes of transgenic mice that model glial tauopathies. J Neurosci 25:9434-9443.
64. Hirano A, Nakano I, Kurland LT, Mulder DW, Holley PW, Saccomanno G (1984) Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 43:471-480.
65. Ho L, Xiang Z, Mukherjee P, Zhang W, De Jesus N, Mirjany M, Yemul S, Pasinetti GM (2001) Gene expression profiling of the tau mutant (P301L) transgenic mouse brain. Neurosci Lett 310:1-4.
66. Hock C, Konietzko U, Papassotiropoulos A, Wollmer A, Streffer J, von Rotz RC, Davey G, Moritz E, Nitsch RM (2002) Generation of antibodies specific for beta-amyloid by vaccination of patients with Alzheimer disease. Nat Med 8:1270-1275.
67. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, Muller-Tillmanns B, Lemke U, Henke K, Moritz E, Garcia E, Wollmer MA, Umbricht D, de Quervain DJ, Hofmann M, Maddalena A, Papassotiropoulos A, Nitsch RM (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38:547-554.
68. Hoerndli F, David D, Götz J (2005) Functional genomics meets neurodegenerative disorders. Part II: transcriptomic and proteomic technology. Prog Neurobiol 76:169-188.
69. 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.
70. Ikegami S, Harada A, Hirokawa N (2000) Muscle weakness, hyperactivity, and impairment in fear conditioning in tau-deficient mice. Neurosci Lett 279:129-132.
71. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, Lee VMY (1999) Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24:751-762.
72. Ishihara T, Zhang B, Higuchi M, Yoshiyama Y, Trojanowski JQ, Lee VMY (2001) Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am J Pathol 158:555-562.
73. Jackson GR, Wiedau-Pazos M, Sang T-K, Wagle N, Brown CA, Massachi S, Geschwind DH (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34:509-519.
74. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D (2000) A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408:979-982.
75. Karsten SL, Sang TK, Gehman LT, Chatterjee S, Liu J, Lawless GM, Sengupta S, Berry RW, Pomakian J, Oh HS, Schulz C, Hui KS, Wiedau-Pazos M, Vinters HV, Binder LI, Geschwind DH, Jackson GR (2006) A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration. Neuron 51:549-560.
76. Keil U, Bonert A, Marques CA, Scherping I, Weyermann J, Strosznajder JB, Muller-Spahn F, Haass C, Czech C, Pradier L, Muller WE, Eckert A (2004) Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J Biol Chem 279:50310-50320.
77. Khurana V, Lu Y, Steinhilb ML, Oldham S, Shulman JM, Feany MB (2006) TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr Biol 16:230-241.
78. Kins S, Crameri A, Evans DR, Hemmings BA, Nitsch RM, Götz J (2001) Reduced PP2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J Biol Chem 276:38193-38200.
79. Kins S, Kurosinski P, Nitsch RM, Götz J (2003) Activation of the ERK and JNK signaling pathways caused by neuron specific inhibition of PP2A in transgenic mice. Am J Pathol 163:833-843.
80. Koolen DA, Vissers LE, Pfundt R, de Leeuw N, Knight SJ, Regan R, Kooy RF, Reyniers E, Romano C, Fichera M, Schinzel A, Baumer A, Anderlid BM, Schoumans J, Knoers NV, van Kessel AG, Sistermans EA, Veltman JA, Brunner HG, De Vries BB (2006) A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism. Nat Genet 38:999-1001.
81. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD (2003) Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci USA 100:9980-9985.
82. Kraemer BC, Burgess JK, Chen JH, Thomas JH, Schellenberg GD (2006) Molecular pathways that influence human tau-induced pathology in Caenorhabditis elegans. Hum Mol Genet 15:1483-1496.
83. Kulic L, Kurosinski P, Chen F, Tracy J, Mohajeri MH, Li H, Nitsch RM, Götz J (2005) Active immunization trial in Abeta(42)-injected P301L tau transgenic mice. Neurobiol Dis 22:50-56.
84. Kurosinski P, Guggisberg M, Götz J (2002) Alzheimer's and Parkinson's disease - overlapping or synergistic pathologies? Trends Mol Med 8:3-5.
85. Le Corre S, Klafki HW, Plesnila N, Hubinger G, Obermeier A, Sahagun H, Monse B, Seneci P, Lewis J, Eriksen J, Zehr C, Yue M, McGowan E, Dickson DW, Hutton M, Roder HM (2006) An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc Natl Acad Sci USA 103:9673-9678.
86. Lee VMY, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
87. Lee VMY, Kenyon TK, Trojanowski JQ (2005) Transgenic animal models of tauopathies. Biochim Biophys Acta 1739:251-259.
88. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Murphy PM, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M (2000) Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25:402-405.
89. Lewis J, Dickson DW, Lin W-L, Chisholm L, Corral A, Jones G, Yen S-H, 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.
90. Li G, Faibushevich A, Turunen BJ, Yoon SO, Georg G, Michaelis ML, Dobrowsky RT (2003) Stabilization of the cyclin-dependent kinase 5 activator, p35, by paclitaxel decreases beta-amyloid toxicity in cortical neurons. J Neurochem 84:347-362.
91. Lim F, Hernandez F, Lucas JJ, Gomez-Ramos P, Moran MA, Avila J (2001) FTDP-17 mutations in tau transgenic mice provoke lysosomal abnormalities and Tau filaments in forebrain. Mol Cell Neurosci 18:702-714.
92. Lin SL, Ying SY (2006) Gene silencing in vitro and in vivo using intronic microRNAs. Methods Mol Biol 342:295-312.
93. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW (2003) Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation. Am J Pathol 162:213-218.
94. Liu F, Grundke-Iqbal I, Iqbal K, Gong CX (2005) Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur J Neurosci 22:1942-1950.
95. Lupski JR (2006) Genome structural variation and sporadic disease traits. Nat Genet 38:974-976.
96. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, Sisk A, Mucke L (2000) Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287:1265-1269.
97. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 82:4245-4249.
98. Menendez J, Rodriguez-Navarro JA, Solano RM, Casarejos MJ, Rodal I, Guerrero R, Sanchez MP, Avila J, Mena MA, De Yebenes JG (2006) Suppression of Parkin enhances nigrostriatal and motor neuron lesion in mice over-expressing human-mutated tau protein. Hum Mol Genet 15:2045-2058.
99. Mershin A, Pavlopoulos E, Fitch O, Braden BC, Nanopoulos DV, Skoulakis EM (2004) Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn Mem 11:277-287.
100. Miyasaka T, Ding Z, Gengyo-ando K, Oue M, Yamaguchi H, Mitani S, Ihara Y (2005) Progressive neurodegeneration in C. elegans model of tauopathy. Neurobiol Dis 20:372-383.
101. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, Connor K, Hatcher J, Hope C, Gordon M, Arendash GW (2000) A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408:982-985.
102. Mudher A, Shepherd D, Newman TA, Mildren P, Jukes JP, Squire A, Mears A, Drummond JA, Berg S, MacKay D, Asuni AA, Bhat R, Lovestone S (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol Psychiatry 9:522-530.
103. Munoz DG, Greene C, Perl DP, Selkoe DJ (1988) Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J Neuropathol Exp Neurol 47:9-18.
104. Murata S, Minami Y, Minami M, Chiba T, Tanaka K (2001) CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep 2:1133-1138.
105. Nishimura I, Yang Y, Lu B (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116:671-682.
106. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, Duff K (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565.
107. Noble W, Planel E, Zehr C, Olm V, Meyerson J, Suleman F, Gaynor K, Wang L, LaFrancois J, Feinstein B, Burns M, Krishnamurthy P, Wen Y, Bhat R, Lewis J, Dickson D, Duff K (2005) Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci USA 102:6990-6995.
108. Noda T, Ohsumi Y (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273:3963-3966.
109. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles. Intracellular abeta and synaptic dysfunction. Neuron 39:409-421.
110. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43:321-332.
111. Pei JJ, Gong CX, An WL, Winblad B, Cowburn RF, Grundke-Iqbal I, Iqbal K (2003) Okadaic-acid-induced inhibition of protein phosphatase 2A produces activation of mitogen-activated protein kinases ERK1/2, MEK1/2, and p70 S6, similar to that in Alzheimer's disease. Am J Pathol 163:845-858.
112. Pennanen L, Welzl H, D'Adamo P, Nitsch RM, Götz J (2004) Accelerated extinction of conditioned taste aversion in P301L tau transgenic mice. Neurobiol Dis 15:500-509.
113. Pennanen L, Götz J (2005) Different tau epitopes define Abeta(42)-mediated tau insolubility. Biochem Biophys Res Commun 337:1097-1101.
114. Pennanen L, Wolfer DP, Nitsch RM, Götz J (2006) Impaired spatial reference memory and increased exploratory behavior in P301L tau transgenic mice. Genes Brain Behav 5:369-379.
115. Perez M, Hernandez F, Gomez-Ramos A, Smith M, Perry G, Avila J (2002) Formation of aberrant phosphotau fibrillar polymers in neural cultured cells. Eur J Biochem 269:1484-1489.
116. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423:435-439.
117. Planel E, Yasutake K, Fujita SC, Ishiguro K (2001) Inhibition of protein phosphatase 2A overrides tau protein kinase I/glycogen synthase kinase 3 beta and cyclin-dependent kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse. J Biol Chem 276:34298-34306.
118. Plattner F, Angelo M, Giese KP (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 281:25457-25465.
119. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43:815-825.
120. Probst A, Götz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, Hong M, Ishihara T, Lee VMY, Trojanowski JQ, Jakes R, Crowther RA, Spillantini MG, Bürki K, Goedert M (2000) Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol (Berl) 99:469-481.
121. Ravikumar B, Duden R, Rubinsztein DC (2002) Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 11:1107-1117.
122. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36:585-595.
123. Rouleau GA, Clark AW, Rooke K, Pramatarova A, Krizus A, Suchowersky O, Julien JP, Figlewicz D (1996) SOD1 mutation is associated with accumulation of neurofilaments in amyotrophic lateral sclerosis. Ann Neurol 39:128-131.
124. Sahara N, Murayama M, Mizoroki T, Urushitani M, Imai Y, Takahashi R, Murata S, Tanaka K, Takashima A (2005) In vivo evidence of CHIP up-regulation attenuating tau aggregation. J Neurochem 94:1254-1263.
125. 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.
126. Sasaki N, Fukatsu R, Tsuzuki K, Hayashi Y, Yoshida T, Fujii N, Koike T, Wakayama I, Yanagihara R, Garruto R, Amano N, Makita Z (1998) Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases. Am J Pathol 153:1149-1155.
127. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400:173-177.
128. Schiffman SS, Clark CM, Warwick ZS (1990) Gustatory and olfactory dysfunction in dementia: not specific to Alzheimer's disease. Neurobiol Aging 11:597-600.
129. Schindowski K, Bretteville A, Leroy K, Begard S, Brion JP, Hamdane M, Buée L (2006) Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am J Pathol 169:599-616.
130. Shahani N, Brandt R (2002) Functions and malfunctions of the tau proteins. Cell Mol Life Sci 59:1668-1680.
131. Shahani N, Subramaniam S, Wolf T, Tackenberg C, Brandt R (2006) Tau aggregation and progressive neuronal degeneration in the absence of changes in spine density and morphology after targeted expression of Alzheimer's disease-relevant tau constructs in organotypic hippocampal slices. J Neurosci 26:6103-6114.
132. Sharp AJ, Hansen S, Selzer RR, Cheng Z, Regan R, Hurst JA, Stewart H, Price SM, Blair E, Hennekam RC, Fitzpatrick CA, Segraves R, Richmond TA, Guiver C, Albertson DG, Pinkel D, Eis PS, Schwartz S, Knight SJ, Eichler EE (2006) Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat Genet 38:1038-1042.
133. Shaw-Smith C, Pittman AM, Willatt L, Martin H, Rickman L, Gribble S, Curley R, Cumming S, Dunn C, Kalaitzopoulos D, Porter K, Prigmore E, Krepischi-Santos AC, Varela MC, Koiffmann CP, Lees AJ, Rosenberg C, Firth HV, de Silva R, Carter NP (2006) Microdeletion encompassing MAPT at chromosome 17q21.3 is associated with developmental delay and learning disability. Nat Genet 38:1032-1037.
134. Shimura H, Schwartz D, Gygi SP, Kosik KS (2004) CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 279:4869-4876.
135. Shulman JM, Feany MB (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165:1233-1242.
136. Sigurdsson EM, Scholtzova H, Mehta PD, Frangione B, Wisniewski T (2001) Immunization with a nontoxic/nonfibrillar amyloid-beta homologous peptide reduces Alzheimer's disease-associated pathology in transgenic mice. Am J Pathol 159:439-447.
137. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 95:7737-7741.
138. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, Laenen I, Geerts H, Mercken M, Sciot R, Van Lommel A, Loos R, Van Leuven F (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 155:2153-2165.
139. Spittaels K, Van Den Haute C, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, Lasrado R, Vandezande K, Laenen I, Boon T, Van Lint J, Vandenheede J, Moechars D, Loos R, Van Leuven F (2000) Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem 275:41340-41349.
140. 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.
141. Tanemura K, Akagi T, Murayama M, Kikuchi N, Murayama O, Hashikawa T, Yoshiike Y, Park JM, Matsuda K, Nakao S, Sun X, Sato S, Yamaguchi H, Takashima A (2001) Formation of filamentous tau aggregations in transgenic mice expressing V337M human tau. Neurobiol Dis 8:1036-1045.
142. Tanemura K, Murayama M, Akagi T, Hashikawa T, Tominaga T, Ichikawa M, Yamaguchi H, Takashima A (2002) Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 22:133-141.
143. Tashiro K, Hasegawa M, Ihara Y, Iwatsubo T (1997) Somatodendritic localization of phosphorylated tau in neonatal and adult rat cerebral cortex.
144. Tatebayashi Y, Miyasaka T, Chui DH, Akagi T, Mishima K, Iwasaki K, Fujiwara M, Tanemura K, Murayama M, Ishiguro K, Planel E, Sato S, Hashikawa T, Takashima A (2002) Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci USA 99:13896-13901.
145. Terwel D, Lasrado R, Snauwaert J, Vandeweert E, Van Haesendonck C, Borghgraef P, Van Leuven F (2005) Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J Biol Chem 280:3963-3973.
146. Tilleman K, van den Haute C, Geerts H, Van Leuven F, Esmans EL, Moens L (2002) Proteomics analysis of the neurodegeneration in the brain of tau transgenic mice. Proteomics 2:656-665.
147. Tucker KL, Meyer M, Barde YA (2001) Neurotrophins are required for nerve growth during development. Nat Neurosci 4:29-37.
148. Van den Haute C, Spittaels K, Van Dorpe J, Lasrado R, Vandezande K, Laenen I, Geerts H, Van Leuven F (2001) Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol Dis 8:32-44.
149. Varela MC, Krepischi-Santos AC, Paz JA, Knijnenburg J, Szuhai K, Rosenberg C, Koiffmann CP (2006) A 17q21.31 microdeletion encompassing the MAPT gene in a mentally impaired patient. Cytogenet Genome Res 114:89-92.
150. Vega IE, Cui L, Propst JA, Hutton ML, Lee G, Yen SH (2005) Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates. Brain Res Mol Brain Res 138:135-144.
151. Vogelsberg-Ragaglia V, Bruce J, Richter-Landsberg C, Zhang B, Hong M, Trojanowski JQ, Lee VM (2000) Distinct FTDP-17 missense mutations in tau produce tau aggregates and other pathological phenotypes in transfected CHO cells. Mol Biol Cell 11:4093-4104.
152. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293:711-714.
153. Yasuda M, Kawamata T, Komure O, Kuno S, D'Souza I, Poorkaj P, Kawai J, Tanimukai S, Yamamoto Y, Hasegawa H, Sasahara M, Hazama F, Schellenberg GD, Tanaka C (1999) A mutation in the microtubule-associated protein tau in pallido-nigro-luysian degeneration. Neurology 53:864-868.
154. Yoo BC, Kim SH, Cairns N, Fountoulakis M, Lubec G (2001) Deranged expression of molecular chaperones in brains of patients with Alzheimer's disease. Biochem Biophys Res Commun 280:249-258.
155. Zhou L, Miller BL, McDaniel CH, Kelly L, Kim OJ, Miller CA (1998) Frontotemporal dementia: neuropil spheroids and presynaptic terminal degeneration. Ann Neurol 44:99-109.
156. Zhukareva V, Vogelsberg-Ragaglia V, Van Deerlin VM, Bruce J, Shuck T, Grossman M, Clark CM, Arnold SE, Masliah E, Galasko D, Trojanowski JQ, Lee VM (2001) Loss of brain tau defines novel sporadic and familial tauopathies with frontotemporal dementia. Ann Neurol 49:165-175.