Progressive accumulation of ubiquitin and disappearance of α-synuclein epitope in multiple system atrophy-associated glial cytoplasmic inclusions: Triple fluorescence study combined with Gallyas-Braak method

Acta Neuropathologica

Volumn 110, Issue 4, 2005, Pages 417-425

  Sakamoto, Masaki ^a,b,c   Uchihara, Toshiki ^b   Nakamura, Ayako ^b   Mizutani, Toshio ^a   Mizusawa, Hidehiro ^c  

^a TOKYO METROPOLITAN NEUROLOGICAL HOSPITAL   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

CARD; Confocal laser microscope; Gallyas Braak; Thiazin red; Triple labeling

Indexed keywords

ALPHA SYNUCLEIN; EPITOPE; UBIQUITIN;

ADULT; AGED; ARTICLE; BRAIN REGION; CASE REPORT; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; DISEASE DURATION; DISEASE SEVERITY; FEMALE; FLUORESCENCE ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEWY BODY; MALE; MOTOR CORTEX; NERVE CELL MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PUTAMEN; SHY DRAGER SYNDROME; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; WHITE MATTER;

AGED; ALPHA-SYNUCLEIN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INCLUSION BODIES; MALE; MIDDLE AGED; MULTIPLE SYSTEM ATROPHY; NEUROGLIA; REGRESSION ANALYSIS; SEVERITY OF ILLNESS INDEX; STAINING AND LABELING; UBIQUITIN;

EID: 27944487985     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-005-1066-9     Document Type: Article

References (39)

1. Adams JC (1992) Biotin amplification of biotin and horseradish peroxidase signals in histochemical stains. J Histochem Cytochem 40:1457-1463 1527370
2. Baba M, Nakajo S, Tu PH, Tomita T, Nakaya K, Lee VM, Trojanowski JQ, Iwatsubo T (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 152:879-884 9546347
3. Braak H, Braak E, Ohm T, Bohl J (1988) Silver impregnation of Alzheimer's neurofibrillary changes counterstained for basophilic material and lipofuscin pigment. Stain Technol 63:197-200 2464205
4. Conway KA, Harper JD, Lansbury PT Jr (1998) Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat Med 11:1318-1320 10.1038/3311
5. Duda JE, Giasson BI, Gur TL, Montine TJ, Robertson D, Biaggioni I, Hurtig HI, Stern MB, Gollomp SM, Grossman M, Lee VM, Trojanowski JQ (2000) Immunohistochemical and biochemical studies demonstrate a distinct profile of alpha-synuclein permutations in multiple system atrophy. J Neuropathol Exp Neurol 59:830-841 11005264
6. Fujita T, Doi M, Ogata T, Kanazawa I, Mizusawa H (1993) Cerebral cortical pathology of sporadic olivopontocerebellar atrophy. J Neurol Sci 116:41-46 8251013
7. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, Iwatsubo T (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4:160-164 10.1038/ncb841
8. Gai WP, Power JH, Blumbergs PC, Culvenor JG, Jensen PH (1999) Alpha-synuclein immunoisolation of glial inclusions from multiple system atrophy brain tissue reveals multiprotein components. J Neurochem 73:2093-2100 10537069
9. Gai WP, Pountney DL, Power JHT, Li QX, Culvenor JG, McLean CA, Jensen PH, Blumbergs PC (2003) α-Synuclein fibrils constitute the central core of oligodendroglial inclusion filaments in multiple system atrophy. Exp Neurol 181:68-78 10.1016/S0014-4886(03)00004-9
10. Giasson BI, Uryu K, Trojanowski JQ, Lee VM (1999) Mutant and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro. J Biol Chem 19:7619-7622 10.1074/jbc.274.12.7619
11. Goedert M (2001) Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2:492-501 10.1038/35081564
12. Gomez-Tortosa E, Gonzalo I, Newell K, Garcia YJ, Vonsattel P, Hyman BT (2002) Patterns of protein nitration in dementia with Lewy bodies and striatonigral degeneration. Acta Neuropathol 103:495-500 10.1007/ s00401-001-0495-3
13. Hasegawa M, Fujiwara H, Nonaka T, Wakabayashi K, Takahashi H, Lee VM, Trojanowski JQ, Mann D, Iwatsubo T (2002) Phosphorylated alpha-synuclein is ubiquitinated in alpha-synucleinopathy lesions. J Biol Chem 13:49071-49076 10.1074/jbc.M208046200
14. Honjyo Y, Kawamoto Y, Nakamura S, Nakano S, Akiguchi I (2001) P39 immunoreactivity in glial cytoplasmic inclusions in brains with multiple system atrophy. Acta Neuropathol 101:190-194 11307616
15. Inoue M, Yagishita S, Ryo M, Hasegawa K, Amano N, Matsushita M (1997) The distribution and dynamic density of oligodendroglial cytoplasmic inclusions (GCIs) in multiple system atrophy: A correlation between the density of GCIs and the degree of involvement of striatonigral and olivopontocerebellar systems. Acta Neuropathol 93:585-591 10.1007/ s004010050655
16. Irizarry MC, Growdon W, Gomez-Isla T, Newell K, George JM, Clayton DF, Hyman BT (1998) Nigral and cortical Lewy bodies and dystrophic nigral neurites in Parkinson's disease and cortical Lewy body disease contain alpha-synuclein immunoreactivity. J Neuropathol Exp Neurol 57:334-337 9600226
17. Iwabuchi K, Kosaka K, Haga C, Tuchiya K, Amano N, Itoh K, Yagishita S, Mizutani Y (1991) Study on argyrophilic inclusions of multisystem atrophy. No To Shinkei 43:561-568 1654964
18. Iwai A, Masliah E, Yoshimoto M, Ge N, Flanagan L, Silva HA de, Kittel A, Saitoh T (1995) The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14:467-475 10.1016/0896-6273(95)90302-X
19. Iwatsubo T, Yamaguchi H, Fujimuro M, Yokosawa H, Ihara Y, Trojanowski JQ, Lee VM (1996) Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. Am J Pathol 148:1517-1529 8623921
20. Jakes R, Crowther RA, Lee VM-Y, Trojanowski JQ, Iwatsubo T, Goedert M (1999) Epitope mapping of LB509, a monoclonal antibody directed against human alpha-synuclein. Neurosci Lett 269:13-16 10.1016/ S0304-3940(99)00411-5
21. Lantos PL (1998) The definition of multiple system atrophy: A review of recent developments. J Neuropathol Exp Neurol 57:1099-1111 9862632
22. Miake H, Mizusawa H, Iwatsubo T, Hasegawa M (2002) Biochemical characterization of the core structure of alpha-synuclein filaments. J Biol Chem 277:19213-19219. 10.1074/jbc.M110551200
23. Nakazato Y, Yamazaki H, Hirato J, Ishida Y, Yamaguchi H (1990) Oligodendroglial microtubular tangles in olivopontocerebellar atrophy. J Neuropathol Exp Neurol 49:521-530 1703225
24. Narhi L, Wood SJ, Steavenson S, Jiang Y, Wu GM, Anafi D, Kaufman SA, Martin F, Sitney K, Denis P, Louis JC, Wypych J, Biere AL, Citron M, (1999) Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J Biol Chem 2:9843-9846 10.1074/ jbc.274.14.9843
25. Nishie M, Mori F, Fujiwara H, Hasegawa M, Yoshimoto M, Iwatsubo T, Takahashi H, Wakabayashi K (2004) Accumulation of phosphorylated alpha-synuclein in the brain and peripheral ganglia of patients with multiple system atrophy. Acta Neuropathol 107:292-298 10.1007/ s00401-003-0811-1
26. Papp MI, Lantos PL (1994) The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. Brain 117:235-243 8186951
27. Papp MI, Kahn JE, Lantos PL (1989) Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94:79-100 10.1016/0022-510X(89)90219-0
28. Piao YS, Hayashi S, Hasegawa M, Wakabayashi K, Yamada M, Yoshimoto M, Ishikawa A, Iwatsubo T, Takahashi H (2001) Co-localization of alpha-synuclein and phosphorylated tau in neuronal and glial cytoplasmic inclusions in a patient with multiple system atrophy of long duration. Acta Neuropathol 101:285-293 11307630
29. Sakamoto M, Uchihara T, Hayashi M, Nakamura A, Kikuchi E, Mizutani T, Mizusawa H, Hirai S (2002) Heterogeneity of nigral and cortical Lewy bodies differentiated by amplified triple-labeling for alpha-synuclein, ubiquitin, and thiazin red. Exp Neurol 177:88-94 10.1006/exnr.2002.7961
30. Shibuya K, Uchihara T, Nakamura A, Ishiyama M, Yamaoka K, Yagishita S, Iwabuchi K, Kosaka K (2003) Reversible conformational change of tau2 epitope on exposure to detergent in glial cytoplasmic inclusions of multiple system atrophy. Acta Neuropathol 105:508-514 12677452
31. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 28:839-840 10.1038/42166
32. Spillantini MG, Crowther RA, Jakes R, Cairns NJ, Lantos PL, Goedert M (1998) Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci Lett 251:205-208 10.1016/S0304-3940(98)00504-7
33. Takahashi M, Iseki E, Kosaka K (2000) Cyclin-dependent kinase 5 (Cdk5) associated with Lewy bodies in diffuse Lewy body disease. Brain Res 862:253-256 10.1016/S0006-8993(00)02086-2
34. Tu PH, Galvin JE, Baba M, Giasson B, Tomita T, Leight S, Nakajo S, Iwatsubo T, Trojanowski JQ, Lee VM (1998) Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann Neurol 44:415-422 10.1002/ ana.410440324
35. Uchihara T, Nakamura A, Nagaoka U, Yamazaki M, Mori O (2000) Dual enhancement of double immunofluorescent signals by CARD: Participation of ubiquitin during formation of neurofibrillary tangles. Histochem Cell Biol 114:447-451 11201605
36. Uchihara T, Nakamura A, Yamazaki M, Mori O (2000) Tau-positive neurons in corticobasal degeneration and Alzheimer's disease-distinction by thiazin red and silver impregnations. Acta Neuropathol 100:385-389 10.1007/s004010000186
37. Uchihara T, Nakamura A, Nakayama H, Arima K, Ishizuka N, Mori H, Mizushima S (2003) Triple immunofluorolabeling with two rabbit polyclonal antibodies and a mouse monoclonal antibody allowing three-dimensional analysis of cotton wool plaques in Alzheimer disease. J Histochem Cytochem 51:1201-1206 12923245
38. Wakabayashi K, Hayashi S, Kakita A, Yamada M, Toyoshima Y, Yoshimoto M, Takahashi H (1998) Accumulation of alpha-synuclein/NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy. Acta Neuropathol 96:445-452 10.1007/s004010050918
39. Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H, (1998) Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 19:180-182 10.1016/S0304-3940(98)00407-8