Accumulation of filamentous tau in the cerebral cortex of human tau R406W transgenic mice

American Journal of Pathology

Volumn 166, Issue 2, 2005, Pages 521-531

  Ikeda, Masaki ^a,j   Shoji, Mikio ^k   Kawarai, Toshitaka ^c   Kawarabayashi, Takeshi ^b   Matsubara, Etsuro ^b   Murakami, Tetsuro ^b   Sasaki, Atsushi ^a   Tomidokoro, Yasushi ^a   Ikarashi, Yasushi ^g   Kuribara, Hisashi ^h   Ishiguro, Koichi ^e   Hasegawa, Masato ^f   Yen, Shu Hui ⁱ   Chishti, M Azhar ^c   Harigaya, Yasuo ^d   Abe, Koji ^b   Okamoto, Koichi ^a   St George Hyslop, Peter ^c   Westaway, David ^c  

^a GUNMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c UNIVERSITY OF TORONTO   (Canada)

^d MAEBASHI RED CROSS HOSPITAL   (Japan)

^e MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^f TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^g TSUMURA AND CO   (Japan)

^h Wakanyaku Medical Institute Ltd   (Japan)

ⁱ MAYO CLINIC   (United States)

^j GUNMA UNIVERSITY   (Japan)

^k NONE

more..

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN; TAU PROTEIN;

AMNESIA; ANIMAL MODEL; ANIMAL TISSUE; ARGYROPHILIA; ARTICLE; ASTROCYTOSIS; BRAIN CORTEX; CELL LOSS; CHROMOSOME 17; CONTROLLED STUDY; ELECTRON MICROSCOPY; FRONTOTEMPORAL DEMENTIA; GENE VECTOR; HAMSTER; HUMAN; MISSENSE MUTATION; MOTOR DYSFUNCTION; MOUSE; NEUROFIBRILLARY TANGLE; NONHUMAN; PARKINSONISM; PERSONALITY DISORDER; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TAUOPATHY; TRANSGENIC MOUSE; UBIQUITINATION;

EID: 19944432508     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)62274-2     Document Type: Article

References (50)

1. Foster NL, Wilhelmsen K, Sima AA, Jones MZ, D'Amato CJ, Gilman S: Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Ann Neurol 1997, 41:706-715
2. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD: Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 1998, 43:815-825
3. 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, Heutink P, et al: Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705
4. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B: Mutation in the tau gene in familial multiple system tauopathy with presence dementia. Proc Natl Acad Sci USA 1998, 95:7737-7741
5. Reed LA, Wszolek ZK, Hutton M: Phenotypic correlations in FTDP-17. Neurobiol Aging 2001, 22:89-107
6. Hasegawa M, Smith MJ, Goedert M: Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 1998, 437:207-210
7. Spillantini MG, Goedert M, Crowther RA, Murrell JR, Farlow MR, Ghetti B: Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments. Proc Natl Acad Sci USA 1997, 94:4113-4118
8. Spillantini MG, Goedert M: Tau protein pathology in neurodegenerative diseases. Trends Neurosci 1998, 21:428-433
9. Reed LA, Grabowski TJ, Schmidt ML, Morris JC, Goate A, Solodkin A, Van Hoesen GW, Schelper RL, Talbot CJ, Wragg MA, Trojanowski JQ: Autosomal dominant dementia with widespread neurofibrillary tangles. Ann Neurol 1997, 42:564-572
10. van Swieten JC, Stevens M, Rosso SM, Rizzu P, Joosse M, de Koning I, Kamphorst W, Ravid R, Spillantini MG, Niermeijer MF, Heutink P: Phenotypic variation in hereditary frontotemporal dementia with tau mutations. Ann Neurol 1999, 46:617-626
11. Saito Y, Geyer A, Sasaki R, Kuzuhara S, Nanba E, Miyasaka T, Suzuki K, Murayama S: Early-onset, rapidly progressive familial tauopathy with R406W mutation. Neurology 2002, 58:811-813
12. Matsumura N, Yamazaki T, Ihara Y: Stable expression in Chinese hamster ovary cells of mutated tau genes causing frontotemporal dementia and parkinsonism linked to chromosome 17 (FTDP-17). Am J Pathol 1999, 154:1649-1656
13. Miyasaka T, Morishima-Kawashima M, Ravid R, Heutink P, van Swieten JC, Nagashima K, Ihara Y: Molecular analysis of mutant and wild-type tau deposited in the brain affected by the FTDP-17 R406W mutation. Am J Pathol 2001, 158:373-379
14. Kozak M: Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 1984, 12:857-872
15. Kozak M: An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 1991, 115:887-903
16. Scott MR, Kohler R, Foster D, Prusiner SB: Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci 1992, 1:986-997
17. Citron M, Westaway D, Xia W, Carlson G, Diehl T, Levesque G, Johnson-Wood K, Lee M, Seubert P, Davis A, Kholodenko D, Motter R, Sherrington R, Perry B, Yao H, Strome R, Lieberburg I, Rommens J, Kim S, Schenk D, Fraser P, St. George Hyslop P, Selkoe DJ: Mutant presenilins of Alzheimer's disease increase production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat Med 1997, 3:67-72
18. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D: Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 2001, 276:21562-21570
19. Duff K, Knight H, Refolo LM, Sanders S, Yu X, Picciano M, Malester B, Hutton M, Adamson J, Goedert M, Burki K, Davies P: Characterization of pathology in transgenic mice overexpressing human genomic and cDNA tau transgenes. Neurobiol Dis 2000, 7:87-98
20. Elliott JL: Cytokine upregulation in a murine model of familial amyotrophic lateral sclerosis. Brain Res Mol Brain Res 2001, 95:172-178
21. Crowe A, Ksiezak-Reding H, Liu WK, Dickson DW, Yen SH: The N terminal region of human tau is present in Alzheimer's disease protein A68 and is incorporated into paired helical filaments. Am J Pathol 1991, 139:1463-1470
22. Greenberg SG, Davies P, Schein JD, Binder LI: Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 1992, 267:564-569
23. Yamaguchi H, Ishiguro K, Uchida T, Takashima A, Lemere CA, Imahori K: Preferential labeling of Alzheimer's neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3β and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol (Berl) 1996, 92:232-241
24. Wolozin BL, Pruchnicki A, Dickson DW, Davies P: A neuronal antigen in the brains of Alzheimer patients. Science 1986, 232:648-650
25. Tomidokoro Y, Ishiguro K, Harigaya Y, Matsubara E, Ikeda M, Park J-M, Yasutake K, Kawarabayashi T, Okamoto K, Shoji M: Aβ amyloidosis induces the initial stage of tau accumulation in APPsw mice. Neurosci Lett 2001, 299:169-172
26. Ishiguro K, Sato K, Takamatsu M, Park J, Uchida T, Imahori K: Analysis of phosphorylation of tau with antibodies specific for phosphorylation sites. Neurosci Lett 1995, 202:81-84
27. Jicha GA, Berenfeld B, Davies P: Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease. J Neurosci Res 1999, 55:713-723
28. Goedert M, Jakes R, Vanmechelen E: Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 1995, 189:167-169
29. Planel E, Yasutake K, Fujita SC, Ishiguro K: 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 2001, 276:34298-34306
30. Paxinos G, Franklin KB: The Mouse Brain in Stereotaxic Coordinates, ed 2. Edited by Paxinos G, Franklin KB. San Diego, Academic Press, 2001
31. Ikarashi Y, Kuribara H, Shiobara T, Takahashi A, Ishimaru H, Maruyama Y: Learning and memory in mice treated with choline oxidase, a hydrolytic enzyme for choline. Pharmacol Biochem Behav 2000, 65:519-522
32. Ikarashi Y, Harigaya Y, Tomidokoro Y, Kanai M, Ikeda M, Matsubara E, Kawarabayashi T, Kuribara H, Younkin SG, Maruyama Y, Shoji M: Decreased level of brain acetylcholine and memory disturbance in APPsw mice. Neurobiol Aging 2004, 25:483-490
33. Goedert M, Spillantini MG, Cairns NJ, Crowther RA: Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 1992, 8:159-168
34. Goedert M, Jakes R: Expression of separate isoforms of human tau protein: correlation of the tau pattern in brain and effects on tubulin polymerazation. EMBO J 1990, 9:4225-4230
35. Gotz J, Probst A, Spillantini MG, Schafer T, Jakes R, Burki K, Goedert M: Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO J 1995, 14:1304-1313
36. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, Lee VM: Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999, 24:751-762
37. Ishihara T, Zhang B, Higuchi M, Yoshiyama Y, Trojanowski JQ, Lee VM: Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mic. Am J Pathol 2001, 158:555-562
38. 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: Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 1999, 155:2153-2165
39. Probst A, Gotz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, Hong M, Ishihara T, Lee VM, Trojanowski JQ, Jakes R, Crowther RA, Spillantini MG, Burki K, Goedert M: Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol (Berl) 2000, 99:469-481
40. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M: Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000, 25:402-405
41. Gotz J, Chen F, Barmettler R, Nitsch RM: Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 2001, 276:529-534
42. Tanemura K, Murayama M, Akagi T, Hashikawa T, Tominaga T, Ichikawa M, Yamaguchi H, Takashima A: Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 2002, 22:133-141
43. Allen B, Ingram E, Takao M, Smith MJ, Jakes R: Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 2002, 22:9340-9351
44. 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: Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci USA 2002, 99:13896-13901
45. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Titani K, Ihara Y: Praline-directed and non-proline-directed phosphoryiation of PHF-tau. J Biol Chem 1995, 270:823-829
46. Krishnamurthy PK, Johnson GV: Mutant (R406W) human tau is hyperphosphorylated and does not efficiently bind microtubules in a neuronal cortical cell model. J Biol Chem 2004, 279:7893-7900
47. Ferrer I, Barrachina M, Puig B: Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy, and corticobasal degeneration. Acta Neuropathol (Berl) 2002, 104:583-591
48. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW: Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation. Am J Pathol 2003, 162:213-218
49. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M, McGowan E: Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491
50. Gotz J, Chen F, van Dorpe J, Nitsch RM: Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Abeta 42 fibrils. Science 2001, 293:1491-1495