The tau N279K exon 10 splicing mutation recapitulates frontotemporal dementia and Parkinsonism linked to chromosome 17 tauopathy in a mouse model

Journal of Neuroscience

Volumn 27, Issue 34, 2007, Pages 9155-9168

  Dawson, Hana N ^a   Cantillana, Viviana ^a   Chen, Liling ^a   Vitek, Michael P ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Caspase 3; Motor skills disorders; Parkinsonian disorders; Promoter; Tauopathy

Indexed keywords

MESSENGER RNA; TAU PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CHROMOSOME 17; CONTROLLED STUDY; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; MOTOR DYSFUNCTION; MOUSE; NERVE CELL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TAUOPATHY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ASPARAGINE; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; CHROMOSOMES, HUMAN, PAIR 17; DEMENTIA; EMBRYO; EXONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LYSINE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURONS; PARKINSONIAN DISORDERS; RNA SPLICING; TAU PROTEINS;

EID: 34548145867     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5492-06.2007     Document Type: Article

References (112)

1. Arai T, Ikeda K, Akiyama H, Shikamoto Y, Tsuchiya K, Yagishita S, Beach T, Rogers J, Schwab C, McGeer PL (2001) Distinct isoforms of tau aggregated in neurons and glial cells in brains of patients with Pick's disease, corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol (Berl) 101:167-173.
2. Arima K, Kowalska A, Hasegawa M, Mukoyama M, Watanabe R, Kawai M, Takahashi K, Iwatsubo T, Tabira T, Sunohara N (2000) Two brothers with frontotemporal dementia and parkinsonism with an N279K mutation of the tau gene. Neurology 54:1787-1795.
3. Auboeuf D, Honig A, Berget SM, O'Malley BW (2002) Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science 298:416-419.
4. Baker M, Litvan I, Houlden H, Adamson J, Dickson D, Perez-Tur J, Hardy J, Lynch T, Bigio E, Hutton M (1999) Association of an extended haplo-type in the tau gene with progressive supranuclear palsy. Hum Mol Genet 8:711-715.
5. Berry RW, Abraha A, Lagalwar S, LaPointe N, Gamblin TC, Cryns VL, Binder LI (2003) Inhibition of tau polymerization by its carboxy-terminal caspase cleavage fragment. Biochemistry 42:8325-8331.
6. Biernat J, Mandelkow EM, Schroter C, Lichtenberg-Kraag B, Steiner B, Berling B, Meyer H, Mercken M, Vandermeeren A, Goedert M (1992) The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J 11:1593-1597.
7. Binder LI, Frankfurter A, Rebhun LI (1985) The distribution of tau in the mammalian central nervous system. J Cell Biol 101:1371-1378.
8. Botez G, Probst A, Ipsen S, Tolnay M (1999) Astrocytes expressing hyperphosphorylated tau protein without glial fibrillary tangles in argyrophilic grain disease. Acta Neuropathol (Berl) 98:251-256.
9. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130.
10. Buee-Scherrer V, Condamines O, Mourton-Gilles C, Jakes R, Goedert M, Pau B, Delacourte A (1996) AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Brain Res Mol Brain Res 39:79-88.
11. Butner KA, Kirschner MW (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites. J Cell Biol 115:717-730.
12. Caceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
13. Carpenter MB (1991) Core text of neuroanatomy. Baltimore: Williams and Wilkins.
14. Cheshire WP, Tsuboi Y, Wszolek ZK (2002) Physiologic assessment of autonomic dysfunction in pallidopontonigral degeneration with N279K mutation in the tau gene on chromosome 17. Auton Neurosci 102:71-77.
15. Clark LN, Poorkaj P, Wszolek Z, Geschwind DH, Nasreddine ZS, Miller B, Li D, Payami H, Awert F, Markopoulou K, Andreadis A, D'Souza I, Lee VM, Reed L, Trojanowski JQ, Zhukareva V, Bird T, Schellenberg G, Wilhelmsen KC (1998) Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci USA 95:13103-13107.
16. Cotman CW, Poon WW, Rissman RA, Blurton-Jones M (2005) The role of caspase cleavage of tau in Alzheimer disease neuropathology. J Neuropathol Exp Neurol 64:104-112.
17. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267-310.
18. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR (1997) Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci USA 94:11456-11460.
19. Cramer P, Srebrow A, Kadener S, Werbajh S, de la Mata M, Melen G, Nogués G, Kornblihtt AR (2001) Coordination between transcription and pre-mRNA processing. FEBS Lett 498:179-182.
20. Crawley JN (2000) What's wrong with my mouse: behavioral phenotyping of transgenic and knockout mouse. New York: Wiley.
21. 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.
22. Delisle MB, Murrell JR, Richardson R, Trofatter JA, Rascol O, Soulages X, Mohr M, Calvas P, Ghetti B (1999) Amutation at codon 279 (N279K) in exon 10 of the Tau gene causes a tauopathy with dementia and supranuclear palsy. Acta Neuropathol (Berl) 98:62-77.
23. Delisle MB, Uro-Coste E, Murrell JR, Rascol O, Ghetti B (2000) Neurodegenerative disease associated with a mutation of codon 279 (N279K) in exon 10 of Tau protein (in French). Bull Acad Natl Med 184:799-809.
24. de Silva R, Weiler M, Morris HR, Martin ER, Wood NW, Lees AJ (2001) Strong association of a novel Tau promoter haplotype in progressive supranuclear palsy. Neurosci Lett 311:145-148.
25. Di ME, Tabaton M, Vigo T, Abbruzzese G, Bellone E, Donati C, Frasson E, Marchese R, Montagna P, Munoz DG, Pramstaller PP, Zanusso G, Ajmar F, Mandich P (2000) Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann Neurol 47:374-377.
26. Drubin DG, Caput D, Kirschner MW (1984) Studies on the expression of the microtubule-associated protein, tau, during mouse brain development, with newly isolated complementary DNA probes. J Cell Biol 98:1090-1097.
27. D'Souza I, Schellenberg GD (2000) Determinants of 4-repeat tau expression. Coordination between enhancing and inhibitory splicing sequences for exon 10 inclusion. J Biol Chem 275:17700-17709.
28. D'Souza I, Schellenberg GD (2002) tau Exon 10 expression involves a bipartite intron 10 regulatory sequence and weak 5′ and 3′ splice sites. J Biol Chem 277:26587-26599.
29. D'Souza I, Schellenberg GD (2005) Regulation of tau isoform expression and dementia. Biochim Biophys Acta 1739:104-115.
30. D'Souza I, Poorkaj P, Hong M, Nochlin D, Lee VM, Bird TD, Schellenberg GD (1999) Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc Natl Acad Sci USA 96:5598-5603.
31. Duff K, Knight H, Refolo LM, Sanders S, Yu X, Picciano M, Malester B, Hutton M, Adamson J, Goedert M, Burki K, Davies P (2000) Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol Dis 7:87-98.
32. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143:777-794.
33. Ezquerra M, Pastor P, Valldeoriola F, Molinuevo JL, Blesa R, Tolosa E, Oliva R (1999) Identification of a novel polymorphism in the promoter region of the tau gene highly associated to progressive supranuclear palsy in humans. Neurosci Lett 275:183-186.
34. Fasulo L, Ugolini G, Visintin M, Bradbury A, Brancolini C, Verzillo V, Novak M, Cattaneo A (2000) The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem 75:624-633.
35. Forman MS, Trojanowski JQ, Lee VM (2004) Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10:1055-1063.
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. Foster NL, Wilhelmsen K, Sima AA, Jones MZ, D'Amato CJ, Gilman S (1997) Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Conference participants. Ann Neurol 41:706-715.
38. Gamblin TC, King ME, Dawson H, Vitek MP, Kuret J, Berry RW, Binder LI (2000) In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants. Biochemistry 39:6136-6144.
39. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, Lu M, Fu Y, Garcia-Sierra F, LaPointe N, Miller R, Berry RW, Binder LI, Cryns VL (2003a) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 100:10032-10037.
40. Gamblin TC, Berry RW, Binder LI (2003b) Modeling tau polymerization in vitro: a review and synthesis. Biochemistry 42:15009-15017.
41. Garcia-Sierra F, Ghoshal N, Quinn B, Berry RW, Binder LI (2003) Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease. J Alzheimers Dis 5:65-77.
42. Goedert M, Hasegawa M (1999) The tauopathies: toward an experimental animal model. Am J Pathol 154:1-6.
43. Goedert M, Jakes R (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 9:4225-4230.
44. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubuleassociated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J 8:393-399.
45. Goode BL, Chau M, Denis PE, Feinstein SC (2000) Structural and functional differences between 3-repeat and 4-repeat tau isoforms. Implications for normal tau function and the onset of neurodegenetative disease. J Biol Chem 275:38182-38189.
46. Gordon MN, King DL, Diamond DM, Jantzen PT, Boyett KV, Hope CE, Hatcher JM, DiCarlo G, Gottschall WP, Morgan D, Arendash GW (2001) Correlation between cognitive deficits and Abeta deposits in transgenic APP+PS1 mice. Neurobiol Aging 22:377-385.
47. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E (1994) Domains of tau protein and interactions with microtubules. Biochemistry 33:9511-9522.
48. Hamm RJ, Pike BR, O'Dell DM, Lyeth BG, Jenkins LW (1994) The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J Neurotrauma 11:187-196.
49. Hasegawa M, Smith MJ, Goedert M (1998) Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 437:207-210.
50. Hauw JJ, Verny M, Delaere P, Cervera P, He Y, Duyckaerts C (1990) Constant neurofibrillary changes in the neocortex in progressive supranuclear palsy. Basic differences with Alzheimer's disease and aging. Neurosci Lett 119:182-186.
51. Himmler A (1989) Structure of the bovine tau gene: alternatively spliced transcripts generate a protein family. Mol Cell Biol 9:1389-1396.
52. Himmler A, Drechsel D, Kirschner MW, Martin Jr DW (1989) Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol Cell Biol 9:1381-1388.
53. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282:1914-1917.
54. Houlden H, Baker M, Morris HR, MacDonald N, Pickering-Brown S, Adamson J, Lees AJ, Rossor MN, Quinn NP, Kertesz A, Khan MN, Hardy J, Lantos PL, St. George-Hyslop P, Munoz DG, Mann D, Lang AE, Bergeron C, Bigio EH, Litvan I, et al. (2001) Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology 56:1702-1706.
55. 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, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
56. Iqbal K, Braak E, Braak H, Zaidi T, Grundke-Iqbal I (1991) A silver impregnation method for labeling both Alzheimer paired helical filaments and their polypeptides separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Neurobiol Aging 12:357-361.
57. Katsuse O, Iseki E, Arai T, Akiyama H, Togo T, Uchikado H, Kato M, de Silva R, Lees A, Kosaka K (2003) 4-Repeat tauopathy sharing pathological and biochemical features of corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol (Berl) 106:251-260.
58. Kawai J, Sasahara M, Hazama F, Kuno S, Komure O, Nomura S, Yamaguchi M (1993) Pallidonigroluysian degeneration with iron deposition: a study of three autopsy cases. Acta Neuropathol (Berl) 86:609-616.
59. King ME, Ahuja V, Binder LI, Kuret J (1999) Ligand-dependent tau filament formation: implications for Alzheimer's disease progression. Biochemistry 38:14851-14859.
60. Klein RL, Dayton RD, Lin WL, Dickson DW (2005) Tau gene transfer, but not alpha-synuclein, induces both progressive dopamine neuron degeneration and rotational behavior in the rat. Neurobiol Dis 20:64-73.
61. Klein RL, Dayton RD, Leidenheimer NJ, Jansen K, Golde TE, Zweig RM (2006) Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol Ther 13:517-527.
62. Kwok JB, Teber ET, Loy C, Hallupp M, Nicholson G, Mellick GD, Buchanan DD, Silburn PA, Schofield PR (2004) Tau haplotypes regulate transcription and are associated with Parkinson's disease. Ann Neurol 55:329-334.
63. Levy SF, Leboeuf AC, Massie MR, Jordan MA, Wilson L, Feinstein SC (2005) Three- and four-repeat tau regulate the dynamic instability of two distinct microtubule subpopulations in qualitatively different manners. Implications for neurodegeneration. J Biol Chem 280:13520-13528.
64. Liu WK, Le TV, Adamson J, Baker M, Cookson N, Hardy J, Hutton M, Yen SH, Dickson DW (2001) Relationship of the extended tau haplotype to tau biochemistry and neuropathology in progressive supranuclear palsy. Ann Neurol 50:494-502.
65. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
66. Mailliot C, Sergeant N, Bussiere T, Caillet-Boudin ML, Delacourte A, Buee L (1998) Phosphorylation of specific sets of tau isoforms reflects different neurofibrillary degeneration processes. FEBS Lett 433:201-204.
67. Makrides V, Shen TE, Bhatia R, Smith BL, Thimm J, Lal R, Feinstein SC (2003) Microtubule-dependent oligomerization of tau. Implications for physiological tau function and tauopathies. J Biol Chem 278:33298-33304.
68. Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, O'Connor M, Trojanowski JQ, Lee VM (1994) Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13:989-1002.
69. Mercken M, Vandermeeren M, Lübke U, Six J, Boons J, Van deVoorde A, Martin JJ, Gheuens J (1992) Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol (Berl) 84:265-272.
70. 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.
71. Morris HR, Osaki Y, Holton J, Lees AJ, Wood NW, Revesz T, Quinn N (2003) Tau exon 10 + 16 mutation FTDP-17 presenting clinically as sporadic young onset PSP. Neurology 61:102-104.
72. Motoi Y, Takanashi M, Itaya M, Ikeda K, Mizuno Y, Mori H (2004) Glial localization of four-repeat tau in atypical progressive supranuclear palsy. Neuropathology 24:60-65.
73. Nacharaju P, Lewis J, Easson C, Yen S, Hackett J, Hutton M, Yen SH (1999) Accelerated filament formation from tau protein with specific FTDP-17 missense mutations. FEBS Lett 447:195-199.
74. Newman J, Rissman RA, Sarsoza F, Kim RC, Dick M, Bennett DA, Cotman CW, Rohn TT, Head E (2005) Caspase-cleaved tau accumulation in neurodegenerative diseases associated with tau and alpha-synuclein pathology. Acta Neuropathol (Berl) 110:135-144.
75. Oliva R, Tolosa E, Ezquerra M, Molinuevo JL, Valldeoriola F, Burguera J, Calopa M, Villa M, Ballesta F (1998) Significant changes in the tau A0 and A3 alleles in progressive supranuclear palsy and improved genotyping by silver detection. Arch Neurol 55:1122-1124.
76. Oyanagi K, Chen KM, Craig UK, Yamazaki M, Perl DP (2000) Parkinsonism, dementia and vertical gaze palsy in a Guamanian with atypical neuroglial degeneration. Acta Neuropathol (Berl) 99:73-80.
77. Pagani F, Stuani C, Zuccato E, Kornblihtt AR, Baralle FE (2003) Promoter architecture modulates CFTR exon 9 skipping. J Biol Chem 278:1511-1517.
78. Panda D, Samuel JC, Massie M, Feinstein SC, Wilson L (2003) Differential regulation of microtubule dynamics by three- and four-repeat tau: implications for the onset of neurodegenerative disease. Proc Natl Acad Sci USA 100:9548-9553.
79. Pastor P, Ezquerra M, Tolosa E, Munoz E, Marti MJ, Valldeoriola F, Molinuevo JL, Calopa M, Oliva R (2002) Further extension of the H1 haplotype associated with progressive supranuclear palsy. Mov Disord 17:550-556.
80. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. London: Academic.
81. Pittman AM, Myers AJ, Duckworth J, Bryden L, Hanson M, Abou-Sleiman P, Wood NW, Hardy J, Lees A, de Silva R (2004) The structure of the tau haplotype in controls and in progressive supranuclear palsy. Hum Mol Genet 13:1267-1274.
82. 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.
83. Rademakers R, Cruts M, van Broeckhoven C (2004) The role of tau (MAPT) in frontotemporal dementia and related tauopathies. Hum Mutat 24:277-295.
84. Reed LA, Schmidt ML, Wszolek ZK, Balin BJ, Soontornniyomkij V, Lee VM, Trojanowski JQ, Schelper RL (1998) The neuropathology of a chromosome 17-linked autosomal dominant parkinsonism and dementia ("pallido-ponto-nigral degeneration"). J Neuropathol Exp Neurol 57:588-601.
85. Reed LA, Wszolek ZK, Hutton M (2001) Phenotypic correlations in FTDP-17. Neurobiol Aging 22:89-107.
86. Rissman RA, Poon WW, Blurton-Jones M, Oddo S, Torp R, Vitek MP, LaFerla FM, Rohn TT, Cotman CW (2004) Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest 114:121-130.
87. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
88. Sergeant N, Wattez A, Delacourte A (1999) Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: tau pathologies with exclusively "exon 10" isoforms. J Neurochem 72:1243-1249.
89. Shahani N, Brandt R (2002) Functions and malfunctions of the tau proteins. Cell Mol Life Sci 59:1668-1680.
90. Sobrido MJ, Miller BL, Havlioglu N, Zhukareva V, Jiang Z, Nasreddine ZS, Lee VM, Chow TW, Wilhelmsen KC, Cummings JL, Wu JY, Geschwind DH (2003) Novel tau polymorphisms, tau haplotypes, and splicing in familial and sporadic frontotemporal dementia. Arch Neurol 60:698-702.
91. Soliveri P, Rossi G, Monza D, Tagliavini F, Piacentini S, Albanese A, Bugiani O, Girotti F (2003) A case of dementia parkinsonism resembling progressive supranuclear palsy due to mutation in the tau protein gene. Arch Neurol 60:1454-1456.
92. 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.
93. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051-1063.
94. Takanashi M, Ohta S, Matsuoka S, Mori H, Mizuno Y (2002) Mixed multiple system atrophy and progressive supranuclear palsy: a clinical and pathological report of one case. Acta Neuropathol (Berl) 103:82-87.
95. Takuma H, Arawaka S, Mori H (2003) Isoforms changes of tau protein during development in various species. Brain Res Dev Brain Res 142:121-127.
96. Togo T, Dickson DW (2002) Tau accumulation in astrocytes in progressive supranuclear palsy is a degenerative rather than a reactive process. Acta Neuropathol (Berl) 104:398-402.
97. Togo T, Sahara N, Yen SH, Cookson N, Ishizawa T, Hutton M, de Silva R, Lees A, Dickson DW (2002) Argyrophilic grain disease is a sporadic 4-repeat tauopathy. J Neuropathol Exp Neurol 61:547-556.
98. Tsuboi Y, Uitti RJ, Delisle MB, Ferreira JJ, Brefel-Courbon C, Rascol O, Ghetti B, Murrell JR, Hutton M, Baker M, Wszolek ZK (2002a) Clinical features and disease haplotypes of individuals with the N279K tau gene mutation: a comparison of the pallidopontonigral degeneration kindred and a French family. Arch Neurol 59:943-950.
99. Tsuboi Y, Baker M, Hutton ML, Uitti RJ, Rascol O, Delisle MB, Soulages X, Murrell JR, Ghetti B, Yasuda M, Komure O, Kuno S, Arima K, Sunohara N, Kobayashi T, Mizuno Y, Wszolek ZK (2002b) Clinical and genetic studies of families with the tau N279K mutation (FTDP-17). Neurology 59:1791-1793.
100. Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, Manogue K, Cerami A (1994) Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc Natl Acad Sci USA 91:4766-4770.
101. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72:1858-1862.
102. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
103. Wilhelmsen KC (1997) Disinhibition-dementia-parkinsonism-amyotrophy complex (DDPAC) is a non-Alzheimer's frontotemporal dementia. J Neural Transm Suppl 49:269-275.
104. Wilhelmsen KC, Forman MS, Rosen HJ, Alving LI, Goldman J, Feiger J, Lee JV, Segall SK, Kramer JH, Lomen-Hoerth C, Rankin KP, Johnson J, Feiler HS, Weiner MW, Lee VM, Trojanowski JQ, Miller BL (2004) 17q-linked frontotemporal dementia-amyotrophic lateral sclerosis without tau mutations with tau and alpha-synuclein inclusions. Arch Neurol 61:398-406.
105. Wszolek ZK, Pfeiffer RF, Bhatt MH, Schelper RL, Cordes M, Snow BJ, Rodnitzky RL, Wolters EC, Arwert F, Calne DB (1992) Rapidly progressive autosomal dominant parkinsonism and dementia with pallido-pontonigral degeneration. Ann Neurol 32:312-320.
106. Yamada T, McGeer PL, McGeer EG (1992) Appearance of paired nucleated, Tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 135:99-102.
107. Yamada T, Calne DB, Akiyama H, McGeer EG, McGeer PL (1993) Further observations on Tau-positive glia in the brains with progressive supranuclear palsy. Acta Neuropathol (Berl) 85:308-315.
108. Yamaguchi H, Nakazato Y, Kawarabayashi T, Ishiguro K, Ihara Y, Morimatsu M, Hirai S (1991) Extracellular neurofibrillary tangles associated with degenerating neurites and neuropil threads in Alzheimer-type dementia. Acta Neuropathol (Berl) 81:603-609.
109. Yang W, Sopper MM, Leystra-Lantz C, Strong MJ (2003) Microtubule- associated tau protein positive neuronal and glial inclusions in ALS. Neurology 61:1766-1773.
110. Yasojima K, McGeer EG, McGeer PL (1999) Tangled areas of Alzheimer brain have upregulated levels of exon 10 containing tau mRNA. Brain Res 831:301-305.
111. 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.
112. Yoshiyama Y, Zhang B, Bruce J, Trojanowski JQ, Lee VM (2003) Reduction of detyrosinated microtubules and Golgi fragmentation are linked to tau-induced degeneration in astrocytes. J Neurosci 23:10662-10671.