Tau alteration and neuronal degeneration in tauopathies: Mechanisms and models

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1739, Issue 2, 2005, Pages 331-354

  Brandt, Roland ^a   Hundelt, Monika ^a   Shahani, Neelam ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Alzheimer's disease; Cytoskeleton; Microtubule associated protein; Neurodegeneration; Neurofibrillary tangle; Paired helical filament; Tau; Tauopathy

Indexed keywords

CYTOCHALASIN; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 27; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; TAU PROTEIN; TUBULIN;

ALZHEIMER DISEASE; BINDING AFFINITY; BRAIN CORTEX; BRAIN REGION; CELL ASSAY; CELL INCLUSION; CELL LINE; CELL ULTRASTRUCTURE; CHROMOSOME 17; CYTOTOXICITY; DEGENERATIVE DISEASE; DEGLYCOSYLATION; EXON; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GENE OVEREXPRESSION; GENETIC CODE; GLIA; GLYCOSYLATION; HUMAN; MICROTUBULE; MISSENSE MUTATION; MOLECULAR DYNAMICS; NERVE CELL; NERVE CELL DEGENERATION; NEURITE; NEUROFILAMENT; NONHUMAN; PAIRED HELICAL FILAMENT; PARKINSONISM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA SPLICING; SENILE DEMENTIA; SEQUENCE HOMOLOGY; SPINAL CORD; TAUOPATHY; UBIQUITINATION;

ALZHEIMER DISEASE; ANIMALS; CELLS, CULTURED; CHROMOSOMES, HUMAN, PAIR 17; DEMENTIA; HUMANS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTATION; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; PARKINSON DISEASE; PROTEIN ISOFORMS; TAU PROTEINS; TAUOPATHIES;

ANIMALIA;

EID: 10944241542     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2004.06.018     Document Type: Review

References (228)

1. L.I. Binder, A. Frankfurter, and L.I. Rebhun The distribution of tau in the mammalian central nervous system J. Cell Biol. 101 1985 1371 1378
2. R.L. Neve, P. Harris, K.S. Kosik, D.M. Kurnit, and T.A. Donlon Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2 Brain Res. 387 1986 271 280
3. M. Goedert, C.M. Wischik, R.A. Crowther, J.E. Walker, and A. Klug 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. U. S. A. 85 1988 4051 4055
4. N. Gustke, B. Trinczek, J. Biernat, E.M. Mandelkow, and E. Mandelkow Domains of tau protein and interactions with microtubules Biochemistry 33 1994 9511 9522
5. B. Trinczek, J. Biernat, K. Baumann, E.M. Mandelkow, and E. Mandelkow Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules Mol. Biol. Cell 6 1995 1887 1902
6. G. Lee, R.L. Neve, and K.S. Kosik The microtubule binding domain of tau protein Neuron 2 1989 1615 1624
7. M. Goedert, and R. Jakes Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization EMBO J. 9 1990 4225 4230
8. M. Goedert, M.G. Spillantini, M.C. Potier, J. Ulrich, and R.A. Crowther 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
9. I.S. Georgieff, R.K. Liem, W. Mellado, J. Nunez, and M.L. Shelanski High molecular weight tau: preferential localization in the peripheral nervous system J. Cell Sci. 100 Pt 1 1991 55 60
10. D. Couchie, C. Mavilia, I.S. Georgieff, R.K. Liem, M.L. Shelanski, and J. Nunez Primary structure of high molecular weight tau present in the peripheral nervous system Proc. Natl. Acad. Sci. U. S. A. 89 1992 4378 4381
11. M. Goedert, M.G. Spillantini, and R.A. Crowther Cloning of a big tau microtubule-associated protein characteristic of the peripheral nervous system Proc. Natl. Acad. Sci. U. S. A. 89 1992 1983 1987
12. N. Shahani, and R. Brandt Functions and malfunctions of the tau proteins Cell. Mol. Life Sci. 59 2002 1668 1680
13. A. Probst, D. Langui, and J. Ulrich Alzheimer's disease: a description of the structural lesions Brain Pathol. 1 1991 229 239
14. N.L. Foster, K. Wilhelmsen, A.A. Sima, M.Z. Jones, C.J. D'Amato, and S. Gilman Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference, Conference Participants Ann. Neurol. 41 1997 706 715
15. M.G. Spillantini, and M. Goedert Tau protein pathology in neurodegenerative diseases Trends Neurosci. 21 1998 428 433
16. R.A. Crowther, and M. Goedert Abnormal tau-containing filaments in neurodegenerative diseases J. Struct. Biol. 130 2000 271 279
17. P. Poorkaj, T.D. Bird, E. Wijsman, E. Nemens, R.M. Garruto, L. Anderson, A. Andreadis, W.C. Wiederholt, M. Raskind, and G.D. Schellenberg Tau is a candidate gene for chromosome 17 frontotemporal dementia Ann. Neurol. 43 1998 815 825
18. M. Hutton, C.L. Lendon, P. Rizzu, M. Baker, S. Froelich, H. Houlden, S. Pickering-Brown, S. Chakraverty, A. Isaacs, A. Grover, J. Hackett, J. Adamson, S. Lincoln, D. Dickson, P. Davies, R.C. Petersen, M. Stevens, E. de Graaff, E. Wauters, J. van Baren, M. Hillebrand, M. Joosse, J.M. Kwon, P. Nowotny, and P. Heutink Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Nature 393 1998 702 705
19. M.G. Spillantini, J.R. Murrell, M. Goedert, M.R. Farlow, A. Klug, and B. Ghetti Mutation in the tau gene in familial multiple system tauopathy with presenile dementia Proc. Natl. Acad. Sci. U. S. A. 95 1998 7737 7741
20. D.J. Nicholl, M.A. Greenstone, C.E. Clarke, P. Rizzu, D. Crooks, A. Crowe, J.Q. Trojanowski, V.M. Lee, and P. Heutink An English kindred with a novel recessive tauopathy and respiratory failure Ann. Neurol. 54 2003 682 686
21. E. Braak, H. Braak, and E.M. Mandelkow A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads Acta Neuropathol. (Berl.) 87 1994 554 567
22. A. Kenessey, and S.H. Yen The extent of phosphorylation of fetal tau is comparable to that of PHF-tau from Alzheimer paired helical filaments Brain Res. 629 1993 40 46
23. E.S. Matsuo, R.W. Shin, M.L. Billingsley, A. Van deVoorde, M. O'Connor, J.Q. Trojanowski, and V.M. Lee Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau Neuron 13 1994 989 1002
24. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, H. Yoshida, A. Watanabe, K. Titani, and Y. Ihara Hyperphosphorylation of tau in PHF Neurobiol. Aging 16 1995 365 371 (discussion 371-380)
25. R. Hoffmann, V.M. Lee, S. Leight, I. Varga, and L. Otvos Jr. Unique Alzheimer's disease paired helical filament specific epitopes involve double phosphorylation at specific sites Biochemistry 36 1997 8114 8124
26. Q. Zheng-Fischhofer, J. Biernat, E.M. Mandelkow, S. Illenberger, R. Godemann, and E. Mandelkow Sequential phosphorylation of Tau by glycogen synthase kinase-3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical- filament-like conformation Eur. J. Biochem. 252 1998 542 552
27. M.G. Spillantini, R.A. Crowther, W. Kamphorst, P. Heutink, and J.C. van Swieten Tau pathology in two Dutch families with mutations in the microtubule-binding region of tau Am. J. Pathol. 153 1998 1359 1363
28. M. Kidd Paired helical filaments in electron microscopy of Alzheimer's disease Nature 197 1963 192 193
29. R.A. Crowther, and C.M. Wischik Image reconstruction of the Alzheimer paired helical filament EMBO J. 4 1985 3661 3665
30. R.A. Crowther Straight and paired helical filaments in Alzheimer disease have a common structural unit Proc. Natl. Acad. Sci. U. S. A. 88 1991 2288 2292
31. J. Kondo, T. Honda, H. Mori, Y. Hamada, R. Miura, M. Ogawara, and Y. Ihara The carboxyl third of tau is tightly bound to paired helical filaments Neuron 1 1988 827 834
32. K.S. Kosik, L.D. Orecchio, L. Binder, J.Q. Trojanowski, V.M. Lee, and G. Lee Epitopes that span the tau molecule are shared with paired helical filaments Neuron 1 1988 817 825
33. C.M. Wischik, M. Novak, H.C. Thogersen, P.C. Edwards, M.J. Runswick, R. Jakes, J.E. Walker, C. Milstein, M. Roth, and A. Klug Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease Proc. Natl. Acad. Sci. U. S. A. 85 1988 4506 4510
34. V.M. Lee, B.J. Balin, L. Otvos Jr., and J.Q. Trojanowski A68: a major subunit of paired helical filaments and derivatized forms of normal Tau Science 251 1991 675 678
35. M.G. Spillantini, R.A. Crowther, and M. Goedert Comparison of the neurofibrillary pathology in Alzheimer's disease and familial presenile dementia with tangles Acta Neuropathol. (Berl.) 92 1996 42 48
36. M. Hong, V. Zhukareva, V. Vogelsberg-Ragaglia, Z. Wszolek, L. Reed, B.I. Miller, D.H. Geschwind, T.D. Bird, D. McKeel, A. Goate, J.C. Morris, K.C. Wilhelmsen, G.D. Schellenberg, J.Q. Trojanowski, and V.M. Lee Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17 Science 282 1998 1914 1917
37. J.C. van Swieten, M. Stevens, S.M. Rosso, P. Rizzu, M. Joosse, I. de Koning, W. Kamphorst, R. Ravid, M.G. Spillantini, M.F. Niermeijer, and P. Heutink Phenotypic variation in hereditary frontotemporal dementia with tau mutations Ann. Neurol. 46 1999 617 626
38. C.F. Lippa, V. Zhukareva, T. Kawarai, K. Uryu, M. Shafiq, L.E. Nee, J. Grafman, Y. Liang, P.H. St. George-Hyslop, J.Q. Trojanowski, and V.M. Lee Frontotemporal dementia with novel tau pathology and a Glu342Val tau mutation Ann. Neurol. 48 2000 850 858
39. J.R. Murrell, M.G. Spillantini, P. Zolo, M. Guazzelli, M.J. Smith, M. Hasegawa, F. Redi, R.A. Crowther, P. Pietrini, B. Ghetti, and M. Goedert Tau gene mutation G389R causes a tauopathy with abundant pick body-like inclusions and axonal deposits J. Neuropathol. Exp. Neurol. 58 1999 1207 1226
40. S.G. Greenberg, and P. Davies A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis Proc. Natl. Acad. Sci. U. S. A. 87 1990 5827 5831
41. M. Goedert, M.G. Spillantini, N.J. Cairns, and R.A. Crowther Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms Neuron 8 1992 159 168
42. S.F. Mulot, K. Hughes, J.R. Woodgett, B.H. Anderton, and D.P. Hanger PHF-tau from Alzheimer's brain comprises four species on SDS-PAGE which can be mimicked by in vitro phosphorylation of human brain tau by glycogen synthase kinase-3 beta FEBS Lett. 349 1994 359 364
43. M.G. Spillantini, M. Goedert, R.A. Crowther, J.R. Murrell, M.R. Farlow, and B. Ghetti Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments Proc. Natl. Acad. Sci. U. S. A. 94 1997 4113 4118
44. N. Sergeant, J.P. David, M. Goedert, R. Jakes, P. Vermersch, L. Buee, D. Lefranc, A. Wattez, and A. Delacourte Two-dimensional characterization of paired helical filament-tau from Alzheimer's disease: demonstration of an additional 74-kDa component and age-related biochemical modifications J. Neurochem. 69 1997 834 844
45. M. Neumann, W. Schulz-Schaeffer, R.A. Crowther, M.J. Smith, M.G. Spillantini, M. Goedert, and H.A. Kretzschmar Pick's disease associated with the novel Tau gene mutation K369I Ann. Neurol. 50 2001 503 513
46. H. Mori, J. Kondo, and Y. Ihara Ubiquitin is a component of paired helical filaments in Alzheimer's disease Science 235 1987 1641 1644
47. V. Manetto, G. Perry, M. Tabaton, P. Mulvihill, V.A. Fried, H.T. Smith, P. Gambetti, and L. Autilio-Gambetti Ubiquitin is associated with abnormal cytoplasmic filaments characteristic of neurodegenerative diseases Proc. Natl. Acad. Sci. U. S. A. 85 1988 4501 4505
48. G.P. Wang, S. Khatoon, K. Iqbal, and I. Grundke-Iqbal Brain ubiquitin is markedly elevated in Alzheimer disease Brain Res. 566 1991 146 151
49. C. Bancher, I. Grundke-Iqbal, K. Iqbal, V.A. Fried, H.T. Smith, and H.M. Wisniewski Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease Brain Res. 539 1991 11 18
50. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, K. Titani, and Y. Ihara Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments Neuron 10 1993 1151 1160
51. V. Chau, J.W. Tobias, A. Bachmair, D. Marriott, D.J. Ecker, D.K. Gonda, and A. Varshavsky A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein Science 243 1989 1576 1583
52. L. Gregori, M.S. Poosch, G. Cousins, and V. Chau A uniform isopeptide-linked multiubiquitin chain is sufficient to target substrate for degradation in ubiquitin-mediated proteolysis J. Biol. Chem. 265 1990 8354 8357
53. H. Shimura, D. Schwartz, S.P. Gygi, and K.S. Kosik CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival J. Biol. Chem. 279 2004 4869 4876
54. F.M. De Vrij, J.A. Sluijs, L. Gregori, D.F. Fischer, W.T. Hermens, D. Goldgaber, J. Verhaagen, F.W. Van Leeuwen, and E.M. Hol Mutant ubiquitin expressed in Alzheimer's disease causes neuronal death FASEB J. 15 2001 2680 2688
55. S.M. Rosso, L. Donker Kaat, T. Baks, M. Joosse, I. de Koning, Y. Pijnenburg, D. de Jong, D. Dooijes, W. Kamphorst, R. Ravid, M.F. Niermeijer, F. Verheij, H.P. Kremer, P. Scheltens, C.M. van Duijn, P. Heutink, and J.C. van Swieten Frontotemporal dementia in The Netherlands: patient characteristics and prevalence estimates from a population-based study Brain 126 2003 2016 2022
56. W.L. Lin, J. Lewis, S.H. Yen, M. Hutton, and D.W. Dickson Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation Am. J. Pathol. 162 2003 213 218
57. E. Adamec, J.R. Murrell, M. Takao, W. Hobbs, R.A. Nixon, B. Ghetti, and J.P. Vonsattel P301L tauopathy: confocal immunofluorescence study of perinuclear aggregation of the mutated protein J. Neurol. Sci. 200 2002 85 93
58. M. Novak, J. Kabat, and C.M. Wischik Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament EMBO J. 12 1993 365 370
59. M. Novak Truncated tau protein as a new marker for Alzheimer's disease Acta Virol. 38 1994 173 189
60. R. Mena, P.C. Edwards, C.R. Harrington, E.B. Mukaetova-Ladinska, and C.M. Wischik Staging the pathological assembly of truncated tau protein into paired helical filaments in Alzheimer's disease Acta Neuropathol. (Berl.) 91 1996 633 641
61. G. Ugolini, A. Cattaneo, and M. Novak Co-localization of truncated tau and DNA fragmentation in Alzheimer's disease neurones NeuroReport 8 1997 3709 3712
62. F. Garcia-Sierra, N. Ghoshal, B. Quinn, R.W. Berry, and L.I. Binder Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease J. Alzheimer's Dis. 5 2003 65 77
63. L.S. Yang, and H. Ksiezak-Reding Calpain-induced proteolysis of normal human tau and tau associated with paired helical filaments Eur. J. Biochem. 233 1995 9 17
64. T.C. Gamblin, F. Chen, A. Zambrano, A. Abraha, S. Lagalwar, A.L. Guillozet, M. Lu, Y. Fu, F. Garcia-Sierra, N. LaPointe, R. Miller, R.W. Berry, L.I. Binder, and V.L. Cryns Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 100 2003 10032 10037
65. P. Rizzu, M. Joosse, R. Ravid, A. Hoogeveen, W. Kamphorst, J.C. van Swieten, R. Willemsen, and P. Heutink Mutation-dependent aggregation of tau protein and its selective depletion from the soluble fraction in brain of P301L FTDP-17 patients Hum. Mol. Genet. 9 2000 3075 3082
66. S. Yen, C. Easson, P. Nacharaju, M. Hutton, and S.H. Yen FTDP-17 tau mutations decrease the susceptibility of tau to calpain I digestion FEBS Lett. 461 1999 91 95
67. P.M. Stanford, C.E. Shepherd, G.M. Halliday, W.S. Brooks, P.W. Schofield, H. Brodaty, R.N. Martins, J.B. Kwok, and P.R. Schofield Mutations in the tau gene that cause an increase in three repeat tau and frontotemporal dementia Brain 126 2003 814 826
68. G.T. Bramblett, J.Q. Trojanowski, and V.M. Lee Regions with abundant neurofibrillary pathology in human brain exhibit a selective reduction in levels of binding-competent tau and accumulation of abnormal tau-isoforms (A68 proteins) Lab. Invest. 66 1992 212 222
69. G.T. Bramblett, M. Goedert, R. Jakes, S.E. Merrick, J.Q. Trojanowski, and V.M. Lee Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding Neuron 10 1993 1089 1099
70. H. Yoshida, and Y. Ihara Tau in paired helical filaments is functionally distinct from fetal tau: assembly incompetence of paired helical filament-tau J. Neurochem. 61 1993 1183 1186
71. M. Hasegawa, M.J. Smith, and M. Goedert Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly FEBS Lett. 437 1998 207 210
72. R. Dayanandan, M. Van Slegtenhorst, T.G. Mack, L. Ko, S.H. Yen, K. Leroy, J.P. Brion, B.H. Anderton, M. Hutton, and S. Lovestone Mutations in tau reduce its microtubule binding properties in intact cells and affect its phosphorylation FEBS Lett. 446 1999 228 232
73. P. Rizzu, J.C. Van Swieten, M. Joosse, M. Hasegawa, M. Stevens, A. Tibben, M.F. Niermeijer, M. Hillebrand, R. Ravid, B.A. Oostra, M. Goedert, C.M. van Duijn, and P. Heutink High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands Am. J. Hum. Genet. 64 1999 414 421
74. S. Hayashi, Y. Toyoshima, M. Hasegawa, Y. Umeda, K. Wakabayashi, S. Tokiguchi, T. Iwatsubo, and H. Takahashi Late-onset frontotemporal dementia with a novel exon 1 (Arg5His) tau gene mutation Ann. Neurol. 51 2002 525 530
75. P. Poorkaj, N.A. Muma, V. Zhukareva, E.J. Cochran, K.M. Shannon, H. Hurtig, W.C. Koller, T.D. Bird, J.Q. Trojanowski, V.M. Lee, and G.D. Schellenberg An R5L tau mutation in a subject with a progressive supranuclear palsy phenotype Ann. Neurol. 52 2002 511 516
76. C. Rizzini, M. Goedert, J.R. Hodges, M.J. Smith, R. Jakes, R. Hills, J.H. Xuereb, R.A. Crowther, and M.G. Spillantini Tau gene mutation K257T causes a tauopathy similar to Pick's disease J. Neuropathol. Exp. Neurol. 59 2000 990 1001
77. A. Grover, E. England, M. Baker, N. Sahara, J. Adamson, B. Granger, H. Houlden, U. Passant, S.H. Yen, M. DeTure, and M. Hutton A novel tau mutation in exon 9 (1260V) causes a four-repeat tauopathy Exp. Neurol. 184 2003 131 140
78. T. Kobayashi, S. Ota, K. Tanaka, Y. Ito, M. Hasegawa, Y. Umeda, Y. Motoi, M. Takanashi, M. Yasuhara, M. Anno, Y. Mizuno, and H. Mori A novel L266V mutation of the tau gene causes frontotemporal dementia with a unique tau pathology Ann. Neurol. 53 2003 133 137
79. M. Hogg, Z.M. Grujic, M. Baker, S. Demirci, A.L. Guillozet, A.P. Sweet, L.L. Herzog, S. Weintraub, M.M. Mesulam, N.E. LaPointe, T.C. Gamblin, R.W. Berry, L.I. Binder, R. de Silva, A. Lees, M. Espinoza, P. Davies, A. Grover, N. Sahara, T. Ishizawa, D. Dickson, S.H. Yen, M. Hutton, and E.H. Bigio The L266V tau mutation is associated with frontotemporal dementia and Pick-like 3R and 4R tauopathy Acta Neuropathol. (Berl.) 106 2003 323 336
80. O. Bugiani, J.R. Murrell, G. Giaccone, M. Hasegawa, G. Ghigo, M. Tabaton, M. Morbin, A. Primavera, F. Carella, C. Solaro, M. Grisoli, M. Savoiardo, M.G. Spillantini, F. Tagliavini, M. Goedert, and B. Ghetti Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau J. Neuropathol. Exp. Neurol. 58 1999 667 677
81. E. van Herpen, S.M. Rosso, L.A. Serverijnen, H. Yoshida, G. Breedveld, R. van de Graaf, W. Kamphorst, R. Ravid, R. Willemsen, D. Dooijes, D. Majoor-Krakauer, J.M. Kros, R.A. Crowther, M. Goedert, P. Heutink, and J.C. van Swieten Variable phenotypic expression and extensive tau pathology in two families with the novel tau mutation L315R Ann. Neurol. 54 2003 573 581
82. S.M. Rosso, E. van Herpen, W. Deelen, W. Kamphorst, L.A. Severijnen, R. Willemsen, R. Ravid, M.F. Niermeijer, D. Dooijes, M.J. Smith, M. Goedert, P. Heutink, and J.C. van Swieten A novel tau mutation, S320F, causes a tauopathy with inclusions similar to those in Pick's disease Ann. Neurol. 51 2002 373 376
83. M. Perez, F. Lim, M. Arrasate, and J. Avila The FTDP-17-linked mutation R406W abolishes the interaction of phosphorylated tau with microtubules J. Neurochem. 74 2000 2583 2589
84. H. Yoshida, R.A. Crowther, and M. Goedert Functional effects of tau gene mutations deltaN296 and N296H J. Neurochem. 80 2002 548 551
85. A. Grover, M. DeTure, S.H. Yen, and M. Hutton Effects on splicing and protein function of three mutations in codon N296 of tau in vitro Neurosci. Lett. 323 2002 33 36
86. P. Nacharaju, J. Lewis, C. Easson, S. Yen, J. Hackett, M. Hutton, and S.H. Yen Accelerated filament formation from tau protein with specific FTDP-17 missense mutations FEBS Lett. 447 1999 195 199
87. M. Goedert, R. Jakes, and R.A. Crowther Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments FEBS Lett. 450 1999 306 311
88. S. Barghorn, Q. Zheng-Fischhofer, M. Ackmann, J. Biernat, M. von Bergen, E.M. Mandelkow, and E. Mandelkow Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias Biochemistry 39 2000 11714 11721
89. S.H. Yen, M. Hutton, M. DeTure, L.W. Ko, and P. Nacharaju Fibrillogenesis of tau: insights from tau missense mutations in FTDP-17 Brain Pathol. 9 1999 695 705
90. H. Braak, and E. Braak Neuropathological stageing of Alzheimer-related changes Acta Neuropathol. (Berl.) 82 1991 239 259
91. J.L. Price, P.B. Davis, J.C. Morris, and D.L. White The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease Neurobiol. Aging 12 1991 295 312
92. M.G. Spillantini, T.D. Bird, and B. Ghetti Frontotemporal dementia and Parkinsonism linked to chromosome 17: a new group of tauopathies Brain Pathol. 8 1998 387 402
93. S.S. Mirra, J.R. Murrell, M. Gearing, M.G. Spillantini, M. Goedert, R.A. Crowther, A.I. Levey, R. Jones, J. Green, J.M. Shoffner, B.H. Wainer, M.L. Schmidt, J.Q. Trojanowski, and B. Ghetti Tau pathology in a family with dementia and a P301L mutation in tau J. Neuropathol. Exp. Neurol. 58 1999 335 345
94. M. Goedert, M.G. Spillantini, R.A. Crowther, S.G. Chen, P. Parchi, M. Tabaton, D.J. Lanska, W.R. Markesbery, K.C. Wilhelmsen, D.W. Dickson, R.B. Petersen, and P. Gambetti Tau gene mutation in familial progressive subcortical gliosis Nat. Med. 5 1999 454 457
95. M. Yasuda, J. Takamatsu, I. D'Souza, R.A. Crowther, T. Kawamata, M. Hasegawa, H. Hasegawa, M.G. Spillantini, S. Tanimukai, P. Poorkaj, L. Varani, G. Varani, T. Iwatsubo, M. Goedert, D.G. Schellenberg, and C. Tanaka A novel mutation at position +12 in the intron following exon 10 of the tau gene in familial frontotemporal dementia (FTD-Kumamoto) Ann. Neurol. 47 2000 422 429
96. K. Miyamoto, A. Kowalska, M. Hasegawa, T. Tabira, K. Takahashi, W. Araki, I. Akiguchi, and A. Ikemoto Familial frontotemporal dementia and parkinsonism with a novel mutation at an intron 10+11-splice site in the tau gene Ann. Neurol. 50 2001 117 120
97. S.M. Pickering-Brown, A.M. Richardson, J.S. Snowden, A.M. McDonagh, A. Burns, W. Braude, M. Baker, W.K. Liu, S.H. Yen, J. Hardy, M. Hutton, Y. Davies, D. Allsop, D. Craufurd, D. Neary, and D.M. Mann Inherited frontotemporal dementia in nine British families associated with intronic mutations in the tau gene Brain 125 2002 732 751
98. P.M. Stanford, G.M. Halliday, W.S. Brooks, J.B. Kwok, C.E. Storey, H. Creasey, J.G. Morris, M.J. Fulham, and P.R. Schofield Progressive supranuclear palsy pathology caused by a novel silent mutation in exon 10 of the tau gene: expansion of the disease phenotype caused by tau gene mutations Brain 123 Pt 5 2000 880 893
99. L.A. Reed, M.L. Schmidt, Z.K. Wszolek, B.J. Balin, V. Soontornniyomkij, V.M. Lee, J.Q. Trojanowski, and R.L. Schelper The neuropathology of a chromosome 17-linked autosomal dominant parkinsonism and dementia ("pallido-ponto- nigral degeneration") J. Neuropathol. Exp. Neurol. 57 1998 588 601
100. M.B. Delisle, J.R. Murrell, R. Richardson, J.A. Trofatter, O. Rascol, X. Soulages, M. Mohr, P. Calvas, and B. Ghetti A mutation at codon 279 (N279K) in exon 10 of the Tau gene causes a tauopathy with dementia and supranuclear palsy Acta Neuropathol. (Berl.) 98 1999 62 77
101. M. Iijima, T. Tabira, P. Poorkaj, G.D. Schellenberg, J.Q. Trojanowski, V.M. Lee, M.L. Schmidt, K. Takahashi, T. Nabika, T. Matsumoto, Y. Yamashita, S. Yoshioka, and H. Ishino A distinct familial presenile dementia with a novel missense mutation in the tau gene NeuroReport 10 1999 497 501
102. E. Iseki, T. Matsumura, W. Marui, H. Hino, T. Odawara, N. Sugiyama, K. Suzuki, H. Sawada, T. Arai, and K. Kosaka Familial frontotemporal dementia and parkinsonism with a novel N296H mutation in exon 10 of the tau gene and a widespread tau accumulation in the glial cells Acta Neuropathol. (Berl.) 102 2001 285 292
103. I. D'Souza, P. Poorkaj, M. Hong, D. Nochlin, V.M. Lee, T.D. Bird, and G.D. Schellenberg 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. U. S. A. 96 1999 5598 5603
104. I. Ferrer, I. Hernandez, B. Puig, M.J. Rey, M. Ezquerra, E. Tolosa, and M. Boada Ubiquitin-negative mini-pick-like bodies in the dentate gyrus in p301l tauopathy J. Alzheimer's Dis. 5 2003 445 454
105. S. Pickering-Brown, M. Baker, S.H. Yen, W.K. Liu, M. Hasegawa, N. Cairns, P.L. Lantos, M. Rossor, T. Iwatsubo, Y. Davies, D. Allsop, R. Furlong, F. Owen, J. Hardy, D. Mann, and M. Hutton Pick's disease is associated with mutations in the tau gene Ann. Neurol. 48 2000 859 867
106. J.Z. Wang, I. Grundke-Iqbal, and K. Iqbal Glycosylation of microtubule-associated protein tau: an abnormal posttranslational modification in Alzheimer's disease Nat. Med. 2 1996 871 875
107. Y. Sato, Y. Naito, I. Grundke-Iqbal, K. Iqbal, and T. Endo Analysis of N-glycans of pathological tau: possible occurrence of aberrant processing of tau in Alzheimer's disease FEBS Lett. 496 2001 152 160
108. F. Liu, T. Zaidi, K. Iqbal, I. Grundke-Iqbal, R.K. Merkle, and C.X. Gong Role of glycosylation in hyperphosphorylation of tau in Alzheimer's disease FEBS Lett. 512 2002 101 106
109. F. Liu, T. Zaidi, K. Iqbal, I. Grundke-Iqbal, and C.X. Gong Aberrant glycosylation modulates phosphorylation of tau by protein kinase A and dephosphorylation of tau by protein phosphatase 2A and 5 Neuroscience 115 2002 829 837
110. S.E. Arnold, B.T. Hyman, J. Flory, A.R. Damasio, and G.W. Van Hoesen The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease Cereb. Cortex 1 1991 103 116
111. L.S. Griffith, and B. Schmitz O-linked N-acetylglucosamine is upregulated in Alzheimer brains Biochem. Biophys. Res. Commun. 213 1995 424 431
112. J. Guevara, B. Espinosa, E. Zenteno, L. Vazguez, J. Luna, G. Perry, and R. Mena Altered glycosylation pattern of proteins in Alzheimer disease J. Neuropathol. Exp. Neurol. 57 1998 905 914
113. M. Takahashi, Y. Tsujioka, T. Yamada, Y. Tsuboi, H. Okada, T. Yamamoto, and Z. Liposits Glycosylation of microtubule-associated protein tau in Alzheimer's disease brain Acta Neuropathol. (Berl.) 97 1999 635 641
114. M.D. Weingarten, A.H. Lockwood, S.Y. Hwo, and M.W. Kirschner A protein factor essential for microtubule assembly Proc. Natl. Acad. Sci. U. S. A. 72 1975 1858 1862
115. J.P. Brion, A.M. Couck, E. Passareiro, and J. Flament-Durand Neurofibrillary tangles of Alzheimer's disease: an immunohistochemical study J. Submicrosc. Cytol. 17 1985 89 96
116. I. Grundke-Iqbal, K. Iqbal, Y.C. Tung, M. Quinlan, H.M. Wisniewski, and L.I. Binder Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology Proc. Natl. Acad. Sci. U. S. A. 83 1986 4913 4917
117. N.J. Pollock, S.S. Mirra, L.I. Binder, L.A. Hansen, and J.G. Wood Filamentous aggregates in Pick's disease, progressive supranuclear palsy, and Alzheimer's disease show antigenic determinants with microtubule-associated protein tau Lancet 2 1986 1211
118. D.B. Murphy, K.A. Johnson, and G.G. Borisy Role of tubulin-associated proteins in microtubule nucleation and elongation J. Mol. Biol. 117 1977 33 52
119. K.A. Butner, and M.W. Kirschner Tau protein binds to microtubules through a flexible array of distributed weak sites J. Cell Biol. 115 1991 717 730
120. R. Brandt, and G. Lee Functional organization of microtubule-associated protein tau. Identification of regions which affect microtubule growth, nucleation, and bundle formation in vitro J. Biol. Chem. 268 1993 3414 3419
121. R. Brandt, and G. Lee The balance between tau protein's microtubule growth and nucleation activities: implications for the formation of axonal microtubules J. Neurochem. 61 1993 997 1005
122. D. Panda, J.C. Samuel, M. Massie, S.C. Feinstein, and L. Wilson Differential regulation of microtubule dynamics by three- and four-repeat tau: implications for the onset of neurodegenerative disease Proc. Natl. Acad. Sci. U. S. A. 100 2003 9548 9553
123. M.L. Billingsley, and R.L. Kincaid Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration Biochem. J. 323 1997 577 591
124. R. Brandt, and G. Lee Orientation, assembly, and stability of microtubule bundles induced by a fragment of tau protein Cell Motil. Cytoskelet. 28 1994 143 154
125. J. Léger, M. Kempf, G. Lee, and R. Brandt Conversion of serine to aspartate imitates phosphorylation-induced changes in the structure and function of microtubule-associated protein tau J. Biol. Chem. 272 1997 8441 8446
126. M. Morishima-Kawashima, M. Hasegawa, K. Takio, M. Suzuki, H. Yoshida, K. Titani, and Y. Ihara Proline-directed and non-proline-directed phosphorylation of PHF-tau J. Biol. Chem. 270 1995 823 829
127. Q. Lu, and J.G. Wood Functional studies of Alzheimer's disease tau protein J. Neurosci. 13 1993 508 515
128. A.C. Alonso, T. Zaidi, I. Grundke-Iqbal, and K. Iqbal Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease Proc. Natl. Acad. Sci. U. S. A. 91 1994 5562 5566
129. K. Iqbal, T. Zaidi, C. Bancher, and I. Grundke-Iqbal Alzheimer paired helical filaments. Restoration of the biological activity by dephosphorylation FEBS Lett. 349 1994 104 108
130. T.D. Garver, R.A. Lehman, and M.L. Billingsley Microtubule assembly competence analysis of freshly-biopsied human tau, dephosphorylated tau, and Alzheimer tau J. Neurosci. Res. 44 1996 12 20
131. J.Z. Wang, I. Grundke-Iqbal, and K. Iqbal Restoration of biological activity of Alzheimer abnormally phosphorylated tau by dephosphorylation with protein phosphatase-2A, -2B and -1 Brain Res. Mol. Brain Res. 38 1996 200 208
132. A.C. Alonso, I. Grundke-Iqbal, and K. Iqbal Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules Nat. Med. 2 1996 783 787
133. A.D. Alonso, I. Grundke-Iqbal, H.S. Barra, and K. Iqbal 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
134. J. Eidenmuller, T. Fath, A. Hellwig, J. Reed, E. Sontag, and R. Brandt Structural and functional implications of tau hyperphosphorylation: information from phosphorylation-mimicking mutated tau proteins Biochemistry 39 2000 13166 13175
135. M. Kempf, A. Clement, A. Faissner, G. Lee, and R. Brandt Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner J. Neurosci. 16 1996 5583 5592
136. A. Cáceres, and K.S. Kosik Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons Nature 343 1990 461 463
137. I. Tint, T. Slaughter, I. Fischer, and M.M. Black Acute inactivation of tau has no effect on dynamics of microtubules in growing axons of cultured sympathetic neurons J. Neurosci. 18 1998 8660 8673
138. A. Harada, K. Oguchi, S. Okabe, J. Kuno, S. Terada, T. Ohshima, R. Sato-Yoshitake, Y. Takei, T. Noda, and N. Hirokawa Altered microtubule organization in small-calibre axons of mice lacking tau protein Nature 369 1994 488 491
139. H.N. Dawson, A. Ferreira, M.V. Eyster, N. Ghoshal, L.I. Binder, and M.P. Vitek Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice J. Cell Sci. 114 2001 1179 1187
140. Y. Kanai, R. Takemura, T. Oshima, H. Mori, Y. Ihara, M. Yanagisawa, T. Masaki, and N. Hirokawa Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA J. Cell Biol. 109 1989 1173 1184
141. G. Lee, and S.L. Rook Expression of tau protein in non-neuronal cells: microtubule binding and stabilization J. Cell Sci. 102 1992 227 237
142. R. Takemura, S. Okabe, T. Umeyama, Y. Kanai, N.J. Cowan, and N. Hirokawa Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau J. Cell Sci. 103 1992 953 964
143. B. Esmaeli-Azad, J.H. McCarty, and S.C. Feinstein Sense and antisense transfection analysis of tau function-tau influences net microtubule assembly, neurite outgrowth and neuritic stability J. Cell Sci. 107 1994 869 879
144. R. Brandt, G. Lee, D.B. Teplow, D. Shalloway, and M. Abdel-Ghany Differential effect of phosphorylation and substrate modulation on tau's ability to promote microtubule growth and nucleation J. Biol. Chem. 269 1994 11776 11782
145. M. Lu, and K.S. Kosik Competition for microtubule-binding with dual expression of tau missense and splice isoforms Mol. Biol. Cell 12 2001 171 184
146. S. Arawaka, M. Usami, N. Sahara, G.D. Schellenberg, G. Lee, and H. Mori The tau mutation (val337met) disrupts cytoskeletal networks of microtubules NeuroReport 10 1999 993 997
147. T. Frappier, N.S. Liang, K. Brown, C.L. Leung, T. Lynch, R.K. Liem, and M.L. Shelanski Abnormal microtubule packing in processes of SF9 cells expressing the FTDP-17 V337M tau mutation FEBS Lett. 455 1999 262 266
148. M. DeTure, L.W. Ko, S. Yen, P. Nacharaju, C. Easson, J. Lewis, M. van Slegtenhorst, M. Hutton, and S.H. Yen Missense tau mutations identified in FTDP-17 have a small effect on tau-microtubule interactions Brain Res. 853 2000 5 14
149. V. Vogelsberg-Ragaglia, J. Bruce, C. Richter-Landsberg, B. Zhang, M. Hong, J.Q. Trojanowski, and V.M. Lee Distinct FTDP-17 missense mutations in tau produce tau aggregates and other pathological phenotypes in transfected CHO cells Mol. Biol. Cell 11 2000 4093 4104
150. M. DeTure, L.W. Ko, C. Easson, and S.H. Yen Tau assembly in inducible transfectants expressing wild-type or FTDP-17 tau Am. J. Pathol. 161 2002 1711 1722
151. P.K. Krishnamurthy, and G.V. Johnson Mutant (R406W) human tau is hyperphosphorylated and does not efficiently bind microtubules in a neuronal cortical cell model J. Biol. Chem. 279 2004 7893 7900
152. K. Edson, B. Weisshaar, and A. Matus Actin depolymerisation induces process formation on MAP2-transfected non-neuronal cells Development 117 1993 689 700
153. J. Léger, R. Brandt, and G. Lee Identification of tau protein regions required for process formation in PC12 cells J. Cell Sci. 107 1994 3403 3412
154. J. Knops, K.S. Kosik, G. Lee, J.D. Pardee, G.L. Cohen, and L. McConlogue Overexpression of tau in a nonneuronal cell induces long cellular processes J. Cell Biol. 114 1991 725 733
155. P.W. Baas, T.P. Pienkowski, and K.S. Kosik Processes induced by tau expression in Sf9 cells have an axon-like microtubule organization J. Cell Biol. 115 1991 1333 1344
156. P.W. Baas, and M.M. Black Individual microtubules in the axon consist of domains that differ in both composition and stability J. Cell Biol. 111 1990 495 509
157. P.W. Baas, T.P. Pienkowski, K.A. Cimbalnik, K. Toyama, S. Bakalis, F.J. Ahmad, and K.S. Kosik Tau confers drug stability but not cold stability to microtubules in living cells J. Cell Sci. 107 1994 135 143
158. M.M. Black, T. Slaughter, S. Moshiach, M. Obrocka, and I. Fischer Tau is enriched on dynamic microtubules in the distal region of growing axons J. Neurosci. 16 1996 3601 3619
159. J.W. Mandell, and G.A. Banker A spatial gradient of tau protein phosphorylation in nascent axons J. Neurosci. 16 1996 5727 5740
160. T. Maas, J. Eidenmuller, and R. Brandt Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments J. Biol. Chem. 275 2000 15733 15740
161. J. Biernat, and E.M. Mandelkow The development of cell processes induced by tau protein requires phosphorylation of serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains Mol. Biol. Cell 10 1999 727 740
162. U. Wagner, M. Utton, J.M. Gallo, and C.C. Miller Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organization J. Cell Sci. 109 1996 1537 1543
163. S.E. Merrick, J.Q. Trojanowski, and V.M. Lee Selective destruction of stable microtubules and axons by inhibitors of protein serine/threonine phosphatases in cultured human neurons (NT2N cells) J. Neurosci. 17 1997 5726 5737
164. E. Sontag, V. Nunbhakdi-Craig, G. Lee, R. Brandt, C. Kamibayashi, J. Kuret, C.L. White III, M.C. Mumby, and G.S. Bloom Molecular interactions among protein phosphatase 2A, tau, and microtubules J. Biol. Chem. 274 1999 25490 25498
165. E. Sontag, V. Nunbhakdi-Craig, G. Lee, G.S. Bloom, and M.C. Mumby Regulation of the phosphorylation state and microtubule-binding activity of tau by protein phosphatase 2A Neuron 17 1996 1201 1207
166. T. Fath, J. Eidenmuller, and R. Brandt Tau-mediated cytotoxicity in a pseudohyperphosphorylation model of Alzheimer's disease J. Neurosci. 22 2002 9733 9741
167. A. Ebneth, R. Godemann, K. Stamer, S. Illenberger, B. Trinczek, and E. Mandelkow Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease J. Cell Biol. 143 1998 777 794
168. B. Trinczek, A. Ebneth, E.M. Mandelkow, and E. Mandelkow Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles J. Cell Sci. 112 Pt 14 1999 2355 2367
169. K. Stamer, R. Vogel, E. Thies, E. Mandelkow, and E.M. Mandelkow Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress J. Cell Biol. 156 2002 1051 1063
170. D.W. Williams, M. Tyrer, and D. Shepherd Tau and tau reporters disrupt central projections of sensory neurons in Drosophila J. Comp. Neurol. 428 2000 630 640
171. C.W. Wittmann, M.F. Wszolek, J.M. Shulman, P.M. Salvaterra, J. Lewis, M. Hutton, and M.B. Feany Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles Science 293 2001 711 714
172. J.M. Shulman, and M.B. Feany Genetic modifiers of tauopathy in Drosophila Genetics 165 2003 1233 1242
173. G.R. Jackson, M. Wiedau-Pazos, T.K. Sang, N. Wagle, C.A. Brown, S. Massachi, and D.H. Geschwind Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila Neuron 34 2002 509 519
174. B.C. Kraemer, B. Zhang, J.B. Leverenz, J.H. Thomas, J.Q. Trojanowski, and G.D. Schellenberg Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy Proc. Natl. Acad. Sci. U. S. A. 100 2003 9980 9985
175. J. Götz, A. Probst, M.G. Spillantini, T. Schäfer, R. Jakes, K. Bürki, and M. Goedert Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform EMBO J. 14 1995 1304 1313
176. T. Ishihara, M. Hong, B. Zhang, Y. Nakagawa, M.K. Lee, J.Q. Trojanowski, and V.M. Lee Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform Neuron 24 1999 751 762
177. J.P. Julien Neurofilaments and motor neuron disease Trends Cell Biol. 7 1997 243 249
178. K. Spittaels, C. Van den Haute, J. Van Dorpe, K. Bruynseels, K. Vandezande, I. Laenen, H. Geerts, M. Mercken, R. Sciot, A. Van Lommel, R. Loos, and F. Van Leuven Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein Am. J. Pathol. 155 1999 2153 2165
179. A. Probst, J. Götz, K.H. Wiederhold, M. Tolnay, C. Mistl, A.L. Jaton, M. Hong, T. Ishihara, V.M. Lee, J.Q. Trojanowski, R. Jakes, R.A. Crowther, M.G. Spillantini, K. Burki, and M. Goedert Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein Acta Neuropathol. 99 2000 469 481
180. K. Spittaels, C. Van den Haute, J. Van Dorpe, H. Geerts, M. Mercken, K. Bruynseels, R. Lasrado, K. Vandezande, I. Laenen, T. Boon, J. Van Lint, J. Vandenheede, D. Moechars, R. Loos, and F. Van Leuven Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the nervous system of human four-repeat tau transgenic mice J. Biol. Chem. 275 2000 41340 41349
181. R. Nuydens, G. Van Den Kieboom, C. Nolten, C. Verhulst, P. Van Osta, K. Spittaels, C. Van den Haute, E. De Feyter, H. Geerts, and F. Van Leuven Coexpression of GSK-3beta corrects phenotypic aberrations of dorsal root ganglion cells, cultured from adult transgenic mice overexpressing human protein tau Neurobiol. Dis. 9 2002 38 48
182. S. Kins, A. Crameri, D.R. Evans, B.A. Hemmings, R. Nitsch, and J. Götz Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice J. Biol. Chem. 276 2001 38193 38200
183. J. Gotz, F. Chen, R. Barmettler, and R.M. Nitsch Tau filament formation in transgenic mice expressing P301L tau J. Biol. Chem. 276 2001 529 534
184. K. Tanemura, T. Akagi, M. Murayama, N. Kikuchi, O. Murayama, T. Hashikawa, Y. Yoshiike, J.M. Park, K. Matsuda, S. Nakao, X. Sun, S. Sato, H. Yamaguchi, and A. Takashima Formation of filamentous tau aggregations in transgenic mice expressing V337M human tau Neurobiol. Dis. 8 2001 1036 1045
185. Y. Tatebayashi, T. Miyasaka, D.H. Chui, T. Akagi, K. Mishima, K. Iwasaki, M. Fujiwara, K. Tanemura, M. Murayama, K. Ishiguro, E. Planel, S. Sato, T. Hashikawa, and A. Takashima Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau Proc. Natl. Acad. Sci. U. S. A. 99 2002 13896 13901
186. B. Allen, E. Ingram, M. Takao, M.J. Smith, R. Jakes, K. Virdee, H. Yoshida, M. Holzer, M. Craxton, P.C. Emson, C. Atzori, A. Migheli, R.A. Crowther, B. Ghetti, M.G. Spillantini, and M. Goedert Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein J. Neurosci. 22 2002 9340 9351
187. F. Dou, W.J. Netzer, K. Tanemura, F. Li, F.U. Hartl, A. Takashima, G.K. Gouras, P. Greengard, and H. Xu Chaperones increase association of tau protein with microtubules Proc. Natl. Acad. Sci. U. S. A. 100 2003 721 726
188. H. Shimura, Y. Miura-Shimura, and K.S. Kosik Binding of Tau to HSP27 leads to decreased concentration of hyperphosphorylated Tau and enhanced cell survival J. Biol. Chem. 279 2004 17957 17962
189. G.A. Jicha, R. Bowser, I.G. Kazam, and P. Davies Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau J. Neurosci. Res. 48 1997 128 132
190. G.A. Jicha, B. Berenfeld, and P. Davies Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease J. Neurosci. Res. 55 1999 713 723
191. D.W. Cleveland, S.Y. Hwo, and M.W. Kirschner Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly J. Mol. Biol. 116 1977 227 247
192. O. Schweers, E. Schonbrunn-Hanebeck, A. Marx, and E. Mandelkow Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure J. Biol. Chem. 269 1994 24290 24297
193. J.M. Litersky, and G.V. Johnson Phosphorylation by cAMP-dependent protein kinase inhibits the degradation of tau by calpain J. Biol. Chem. 267 1992 1563 1568
194. D.A. Kirschner, C. Abraham, and D.J. Selkoe X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation Proc. Natl. Acad. Sci. U. S. A. 83 1986 503 507
195. J. Berriman, L.C. Serpell, K.A. Oberg, A.L. Fink, M. Goedert, and R.A. Crowther Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure Proc. Natl. Acad. Sci. U. S. A. 100 2003 9034 9038
196. M. Sadqi, F. Hernandez, U. Pan, M. Perez, M.D. Schaeberle, J. Avila, and V. Munoz Alpha-helix structure in Alzheimer's disease aggregates of tau-protein Biochemistry 41 2002 7150 7155
197. M.D. Ledesma, M. Perez, C. Colaco, and J. Avila Tau glycation is involved in aggregation of the protein but not in the formation of filaments Cell. Mol. Biol. 44 1998 1111 1116
198. A. Alonso, T. Zaidi, M. Novak, I. Grundke-Iqbal, and K. Iqbal Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments Proc. Natl. Acad. Sci. U. S. A. 98 2001 6923 6928
199. E. Montejo de Garcini, L. Serrano, and J. Avila Self assembly of microtubule associated protein tau into filaments resembling those found in Alzheimer disease Biochem. Biophys. Res. Commun. 141 1986 790 796
200. H. Wille, G. Drewes, J. Biernat, E.M. Mandelkow, and E. Mandelkow Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro J. Cell Biol. 118 1992 573 584
201. M. Goedert, R. Jakes, M.G. Spillantini, M. Hasegawa, M.J. Smith, and R.A. Crowther Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans Nature 383 1996 550 553
202. M. Pérez, J.M. Valpuesta, M. Medina, E.M. de Garcini, and J. Avila Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction J. Neurochem. 67 1996 1183 1190
203. D.M. Wilson, and L.I. Binder Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease Am. J. Pathol. 150 1997 2181 2195
204. A. Schneider, J. Biernat, M. von Bergen, E. Mandelkow, and E.M. Mandelkow Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments Biochemistry 38 1999 3549 3558
205. J. Eidenmuller, T. Fath, T. Maas, M. Pool, E. Sontag, and R. Brandt Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein Biochem. J. 357 2001 759 767
206. P. Friedhoff, M. von Bergen, E.M. Mandelkow, P. Davies, and E. Mandelkow A nucleated assembly mechanism of Alzheimer paired helical filaments Proc. Natl. Acad. Sci. U. S. A. 95 1998 15712 15717
207. T.M. Yao, K. Tomoo, T. Ishida, H. Hasegawa, M. Sasaki, and T. Taniguchi Aggregation analysis of the microtubule binding domain in tau protein by spectroscopic methods J. Biochem. (Tokyo) 134 2003 91 99
208. S. Barghorn, and E. Mandelkow Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments Biochemistry 41 2002 14885 14896
209. T. Gomez-Isla, R. Hollister, H. West, S. Mui, J.H. Growdon, R.C. Petersen, J.E. Parisi, and B.T. Hyman Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease Ann. Neurol. 41 1997 17 24
210. H. Lasn, B. Winblad, and N. Bogdanovic The number of neurons in the inferior olivary nucleus in Alzheimer's disease and normal aging: a stereological study using the optical fractionator J. Alzheimer's Dis. 3 2001 159 168
211. A. Ferrari, F. Hoerndli, T. Baechi, R.M. Nitsch, and J. Gotz beta-Amyloid induces paired helical filament-like tau filaments in tissue culture J. Biol. Chem. 278 2003 40162 40168
212. L.C. Cork, R.E. Powers, D.J. Selkoe, P. Davies, J.J. Geyer, and D.L. Price Neurofibrillary tangles and senile plaques in aged bears J. Neuropathol. Exp. Neurol. 47 1988 629 641
213. P.T. Nelson, and C.B. Saper Ultrastructure of neurofibrillary tangles in the cerebral cortex of sheep Neurobiol. Aging 16 1995 315 323
214. K.E. Roertgen, J.E. Parisi, H.B. Clark, D.L. Barnes, T.D. O'Brien, and K.H. Johnson A beta-associated cerebral angiopathy and senile plaques with neurofibrillary tangles and cerebral hemorrhage in an aged wolverine (Gulo gulo) Neurobiol. Aging 17 1996 243 247
215. C. Schultz, F. Dehghani, G.B. Hubbard, D.R. Thal, G. Struckhoff, E. Braak, and H. Braak Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons J. Neuropathol. Exp. Neurol. 59 2000 39 52
216. J. Savory, Y. Huang, M.R. Wills, and M.M. Herman Reversal by desferrioxamine of tau protein aggregates following two days of treatment in aluminum-induced neurofibrillary degeneration in rabbit: implications for clinical trials in Alzheimer's disease Neurotoxicology 19 1998 209 214
217. O. Ghribi, M.M. Herman, and J. Savory The endoplasmic reticulum is the main site for caspase-3 activation following aluminum-induced neurotoxicity in rabbit hippocampus Neurosci. Lett. 324 2002 217 221
218. C. Andorfer, Y. Kress, M. Espinoza, R. de Silva, K.L. Tucker, Y.A. Barde, K. Duff, and P. Davies Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms J. Neurochem. 86 2003 582 590
219. T. Ishihara, B. Zhang, M. Higuchi, Y. Yoshiyama, J.Q. Trojanowski, and V.M. Lee Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice Am. J. Pathol. 158 2001 555 562
220. J. Lewis, E. McGowan, J. Rockwood, H. Melrose, P. Nacharaju, M. Van Slegtenhorst, K. Gwinn-Hardy, M. Paul Murphy, M. Baker, X. Yu, K. Duff, J. Hardy, A. Corral, W.L. Lin, S.H. Yen, D.W. Dickson, P. Davies, and M. Hutton Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein Nat. Genet. 25 2000 402 405
221. K. Tanemura, M. Murayama, T. Akagi, T. Hashikawa, T. Tominaga, M. Ichikawa, H. Yamaguchi, and A. Takashima Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau J. Neurosci. 22 2002 133 141
222. J. Gotz, F. Chen, J. van Dorpe, and R.M. Nitsch Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils Science 293 2001 1491 1495
223. J. Lewis, D.W. Dickson, W.L. Lin, L. Chisholm, A. Corral, G. Jones, S.H. Yen, N. Sahara, L. Skipper, D. Yager, C. Eckman, J. Hardy, M. Hutton, and E. McGowan Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP Science 293 2001 1487 1491
224. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
225. L. Ho, Z. Xiang, P. Mukherjee, W. Zhang, N. De Jesus, M. Mirjany, S. Yemul, and G.M. Pasinetti Gene expression profiling of the tau mutant (P301L) transgenic mouse brain Neurosci. Lett. 310 2001 1 4
226. T.D. Bird, D. Nochlin, P. Poorkaj, M. Cherrier, J. Kaye, H. Payami, E. Peskind, T.H. Lampe, E. Nemens, P.J. Boyer, and G.D. Schellenberg A clinical pathological comparison of three families with frontotemporal dementia and identical mutations in the tau gene (P301L) Brain 122 Pt 4 1999 741 756
227. M. Rapoport, H.N. Dawson, L.I. Binder, M.P. Vitek, and A. Ferreira Tau is essential to beta-amyloid-induced neurotoxicity Proc. Natl. Acad. Sci. U. S. A. 99 2002 6364 6369
228. F. Lim, F. Hernandez, J.J. Lucas, P. Gomez-Ramos, M.A. Moran, and J. Avila FTDP-17 mutations in tau transgenic mice provoke lysosomal abnormalities and Tau filaments in forebrain Mol. Cell. Neurosci. 18 2001 702 714