Cortical neuronal and glial pathology in TgTauP301L transgenic mice: Neuronal degeneration, memory disturbance, and phenotypic variation

American Journal of Pathology

Volumn 169, Issue 4, 2006, Pages 1365-1375

  Murakami, Tetsuro ^a   Paitel, Erwan ^g   Kawarabayashi, Takeshi ^a   Ikeda, Masaki ^b   Chishti, M Azhar ^g   Janus, Christopher ^g   Matsubara, Etsuro ^c   Sasaki, Atsushi ^b   Kawarai, Toshitaka ^g   Phinney, Amie L ^g   Harigaya, Yasuo ^d   Horne, Patrick ^g   Egashira, Nobuaki ^e   Mishima, Kenichi ^e   Hanna, Amanda ^g   Yang, Jing ^g   Iwasaki, Katsunori ^e   Takahashi, Mitsuo ^e   Fujiwara, Michihiro ^e   Ishiguro, Koichi ^f   Bergeron, Catherine ^g   Carlson, George A ^h   Abe, Koji ^a   Westaway, David ^g,i   St George Hyslop, Peter ^g   Shoji, Mikio ^a   more..

^a OKAYAMA UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^d MAEBASHI RED CROSS HOSPITAL   (Japan)

^e FUKUOKA UNIVERSITY   (Japan)

^f MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^g UNIVERSITY OF TORONTO   (Canada)

^h MCLAUGHLIN RESEARCH INSTITUTE   (United States)

ⁱ UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TGTAU P301L; TAU PROTEIN; UNCLASSIFIED DRUG; TAURINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN CELL; CHROMOSOME 17; CHROMOSOME MUTATION; CONTROLLED STUDY; FRONTAL LOBE; GLIA CELL; MOUSE; NERVE DEGENERATION; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPINAL CORD; TEMPORAL LOBE; TRANSGENIC MOUSE; WORKING MEMORY; ANIMAL; BRAIN CORTEX; CHEMISTRY; DEGENERATIVE DISEASE; DEMENTIA; DISEASE MODEL; GENETICS; GLIA; GLIOSIS; HUMAN; MEMORY DISORDER; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE;

ANIMALS; CEREBRAL CORTEX; DEMENTIA; DISEASE MODELS, ANIMAL; GLIOSIS; HUMANS; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; MUTATION; NEURODEGENERATIVE DISEASES; NEUROGLIA; NEURONS; PHENOTYPE; TAURINE;

EID: 34447323183     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.051250     Document Type: Article

References (46)

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. Conference Participants. Ann Neurol 1997, 41:706-715
2. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B: Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 1998, 95:7737-7741
3. Mirra SS, Murrell JR, Gearing M, Spillantini MG, Goedert M, Crowther RA, Levey AI, Jones R, Green J, Shoffner JM, Wainer BH, Schmidt ML, Trojanowski JQ, Ghetti B: Tau pathology in a family with dementia and a P301L mutation in tau. J Neuropathol Exp Neurol 1999, 58:335-345
4. Lippa CF, Zhukareva V, Kawarai T, Uryu K, Shafiq M, Nee LE, Grafman J, Liang Y, St. George-Hyslop PH, Trojanowski JQ, Lee VM: Frontotemporal dementia with novel tau pathology and a Glu342Val tau mutation. Ann Neurol 2000, 48:850-858
5. Pickering-Brown SM, Richardson AM, Snowden JS, McDonagh AM, Burns A, Braude W, Baker M, Liu WK, Yen SH, Hardy J, Hutton M, Davies Y, Allsop D, Craufurd D, Neary D, Mann DM: Inherited frontotemporal dementia in nine British families associated with intronic mutations in the tau gene. Brain 2002, 125:732-751
6. Neumann M, Schulz-Schaeffer W, Crowther RA, Smith MJ, Spillantini MG, Goedert M, Kretzschmar HA: Pick's disease associated with the novel Tau gene mutation K369I. Ann Neurol 2001, 50:503-513
7. 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: Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol 1999, 58:667-677
8. Morris HR, Osaki Y, Holton J, Lees AJ, Wood NW, Revesz T, Quinn N: Tau exon 10 + 16 mutation FTDP-17 presenting clinically as sporadic young onset PSP. Neurology 2003, 61:102-104
9. Rizzu P, Joosse M, Ravid R, Hoogeveen A, Kamphorst W, van Swieten JC, Willemsen R, Heutink P: Mutation-dependent aggregation of tau protein and its selective depletion from the soluble fraction in brain of P301L FTDP-17 patients. Hum Mol Genet 2000, 9:3075-3082
10. Bird TD, Nochlin D, Poorkaj P, Cherrier M, Kaye J, Payami H, Peskind E, Lampe TH, Nemens E, Boyer PJ, Schellenberg GD: A clinical pathological comparison of three families with frontotemporal dementia and identical mutations in the tau gene (P301L). Brain 1999, 122:741-756
11. Nasreddine ZS, Loginov M, Clark LN, Lamarche J, Miller BL, Lamontagne A, Zhukareva V, Lee VM, Wilhelmsen KC, Geschwind DH: From genotype to phenotype: a clinical pathological, and biochemical investigation of frontotemporal dementia and parkinsonism (FTDP-17) caused by the P301L tau mutation. Ann Neurol 1999, 45:704-715
12. 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
13. Götz J, Chen F, Barmettler R, Nitsch RM: Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 2001, 276:529-534
14. 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
15. 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: Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481
16. 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: Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705
17. 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: 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 1998, 95:13103-13107
18. Poorkaj P, Grossman M, Steinbart E, Payami H, Sadovnick A, Nochlin D, Tabira T, Trojanowski JQ, Borson S, Galasko D, Reich S, Quinn B, Schellenberg G, Bird TD: Frequency of tau gene mutations in familial and sporadic cases of non-Alzheimer dementia. Arch Neurol 2001, 58:383-387
19. Kozak M: An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 1991, 115:887-903
20. Scott MR, Köhler R, Foster D, Prusiner SB: Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci 1992, 1:986-997
21. 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
22. Basler K, Oesch B, Scott M, Westaway D, Wälchli M, Groth DF, McKinley MP, Prusiner SB, Weissmann C: Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 1986, 46:417-428
23. Ikeda M, Shoji M, Kawarai T, Kawarabayashi T, Matsubara E, Murakami T, Sasaki A, Tomidokoro Y, Ikarashi Y, Kuribara H, Ishiguro K, Hasegawa M, Yen SH, Chishti MA, Harigaya Y, Abe K, Okamoto K, St. George-Hyslop P, Westaway D: Accumulation of filamentous tau in the cerebral cortex of human tau R406W transgenic mice. Am J Pathol 2005, 166:521-531
24. Weaver CL, Espinoza M, Kress Y, Davies P: Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Neurobiol Aging 2000, 21:719-727
25. Murakami T, Shoji M, Imai Y, Inoue H, Kawarabayashi T, Matsubara E, Harigaya Y, Sasaki A, Takahashi R, Abe K: Pael-R is accumulated in Lewy bodies of Parkinson's disease. Ann Neurol 2004, 55:439-442
26. 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: A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000, 408:979-982
27. Egashira N, Tanoue A, Higashihara F, Mishima K, Fukue Y, Takano Y, Tsujimoto G, Iwasaki K, Fujiwara M: V1a receptor knockout mice exhibit impairment of spatial memory in an eight-arm radial maze. Neurosci Lett 2004, 356:195-198
28. Pennanen L, Welzl H, D'Adamo P, Nitsch RM, Götz J: Accelerated extinction of conditioned taste aversion in P301L tau transgenic mice. Neurobiol Dis 2004, 15:500-509
29. Janus C, Welzl H, Hanna A, Lovasic L, Lane N, St. George-Hyslop P, Westaway D: Impaired conditioned taste aversion learning in APP transgenic mice. Neurobiol Aging 2004, 25:1213-1219
30. 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
31. Reed LA, Wszolek ZK, Hutton M: Phenotypic correlations in FTDP-17. Neurobiol Aging 2001, 22:89-107
32. Spillantini MG, Crowther RA, Kamphorst W, Heutink P, van Swieten JC: Tau pathology in two Dutch families with mutations in the microtubule-binding region of tau. Am J Pathol 1998, 153:1359-1363
33. van Swieten JC, Stevens M, Rosso SM, Rizzu P, Joosse M, de Koning I, Kamphorst W, Ravid R, Spillantini MG, Niermeijer, Heutink P: Phenotypic variation in hereditary frontotemporal dementia with tau mutations. Ann Neurol 1999, 46:617-626
34. Miyasaka T, Morishima-Kawashima M, Ravid R, Kamphorst W, Nagashima K, Ihara Y: Selective deposition of mutant tau in the FTDP-17 brain affected by the P301L mutation. J Neuropathol Exp Neurol 2001, 60:872-884
35. Feany MB, Dickson DW: Neurodegenerative disorders with extensive tau pathology: a comparative study and review. Ann Neurol 1996, 40:139-148
36. Feany MB, Mattiace LA, Dickson DW: Neuropathologic overlap of progressive supranuclear palsy, Pick's disease and corticobasal degeneration. J Neuropathol Exp Neurol 1996, 55:53-67
37. Komori T, Arai N, Oda M, Nakayama H, Mori H, Yagishita S, Takahashi T, Amano N, Murayama S, Murakami S, Shibata N, Kobayashi M, Sasaki S, Iwata M: Astrocytic plaques and tufts of abnormal fibers do not coexist in corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol (Berl) 1998, 96:401-408
38. Moser M, Colello RJ, Pott U, Oesch B: Developmental expression of the prion protein gene in glial cells. Neuron 1995, 14:509-517
39. 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, 162:213-238
40. Higuchi M, Ishihara T, Zhang B, Hong M, Andreadis A, Trojanowski J, Lee VM: Transgenic mouse model of tauopathies with glial pathology and nervous system degeneration. Neuron 2002, 35:433-446
41. Götz J, Tolnay M, Barmettler R, Chen F, Probst A, Nitsch RM: Oligodendroglial tau filament formation in transgenic mice expressing G272V tau. Eur J Neurosci 2001, 13:2131-2140
42. Lee VM, Goedert M, Trojanowski JQ: Neurodegenerative tauopathies. Annu Rev Neurosci 2001, 24:1121-1159
43. Goedert M, Hasegawa M, Jakes R, Lawler S, Cuenda A, Cohen P: Phosphorylation of microtubule-associated protein tau by stress-activated protein kinases. FEBS Lett 1997, 409:57-62
44. Okawa Y, Ishiguro K, Fujita SC: Stress-induced hyperphosphorylation of tau in the mouse brain. FEBS Lett 2003, 535:183-189
45. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, Barde YA, Duff K, Davies P: Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 2003, 86:582-590
46. 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: Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 2002, 22:9340-9351