Parkinson's disease transgenic mitochondrial cybrids generate Lewy inclusion bodies

Journal of Neurochemistry

Volumn 88, Issue 4, 2004, Pages 800-812

  Trimmer, Patricia A ^a   Borland, M Kathleen ^a   Keeney, Paula M ^a   Bennett Jr , James P ^a   Parker Jr , W Davis ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Immunoprecipitation; Lewy bodies; Mitochondrial DNA; Nitrotyrosine; Ubiquitin; synuclein

Indexed keywords

3 NITROTYROSINE; 3-NITROTYROSINE; ALPHA SYNUCLEIN; ANTIBODY; BETA TUBULIN; CARRIER PROTEIN; CYSTEINE PROTEINASE; CYTOCHROME C; DRUG DERIVATIVE; EOSIN; MITOCHONDRIAL DNA; MULTIENZYME COMPLEX; NERVE PROTEIN; NEUROFILAMENT PROTEIN; PARKIN; PROTEASOME; PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SYNPHILIN 1; SYNPHILIN-1; SYNUCLEIN; THIOFLAVINE; TUBULIN; TYROSINE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BRAIN TISSUE; CASE CONTROL STUDY; CELL INCLUSION; CELL LINE; CELL STRUCTURE; CELL VACUOLE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYBRID; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; FEMALE; GENETIC CODE; GENETICS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LEWY BODY; MALE; METABOLISM; METHODOLOGY; MITOCHONDRION; NERVE CELL; NERVE CELL CULTURE; NEUROBLASTOMA; NEUROFILAMENT; PARKINSON DISEASE; PATHOGENESIS; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; SERODIAGNOSIS; STAINING; TRANSGENE; ULTRASTRUCTURE; WESTERN BLOTTING;

EID: 1042301278     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02168.x     Document Type: Article

References (76)

1. Alim M. A., Hossain M. S., Arima K. et al. (2002) Tubulin seeds α-synuclein fibril formation. J. Biol. Chem. 277, 2112-2117.
2. Arai H., Lee V. M., Hill W. D., Greenberg B. D. and Trojanowski J. Q. (1992) Lewy bodies contain β-amyloid precursor proteins of Alzheimer's disease. Brain Res. 585, 386-390.
3. Arima K., Ueda K., Sunohara N., Hirai S., Izumiyama Y., Tonozuka-Uehara H. and Kawai M. (1998) Immunoelectron-microscopic demonstration of NACP/α-synuclein-epitopes on the filamentous component of Lewy bodies in Parkinson's disease and in dementia with Lewy bodies. Brain Res. 808, 93-100.
4. Arima K., Mizutani T., Alim M. A., Tonozuka-Uehara H., Izumiyama Y., Hirai S. and Ueda K. (2000) NACP/α-synuclein and tau constitute two distinctive subsets of filaments in the same neuronal inclusions in brains from a family of parkinsonism and dementia with Lewy bodies: double-immunolabeling fluorescence and electron microscopic studies. Acta Neuropathol. 100, 115-121.
5. Baba M., Nakajo S., Tu P. H., Tomita T., Lee V. M., Torjanowski J. Q. and Iwatsubo T. (1998) Aggregation of α-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152, 879-884.
6. Bahr B. A. and Bendiske J. (2002) The neuropathogenic contributions of lysosomal dysfunction. J. Neurochem. 83, 481-489.
7. Barrientos A. and Moraes C. T. (1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 274, 16188-16197.
8. Betarbet R., Sherer T. B. and Greenamyre J. T. (2002) Animal models of Parkinson's disease. Bioessays 24, 308-318.
9. Braak E., Sandmann-Keil D., Rub U., Gai W. P., de Vos R. A., Steur E. N., Arai K. and Braak H. (2001) α-synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol. 101, 195-201.
10. Brion J. P. and Couck A. M. (1995) Cortical and brainstem-type Lewy bodies are immunoreactive for the cyclin-dependent kinase 5. Am. J. Pathol. 147, 1465-1476.
11. Cassarino D. S. and Bennett J. P. Jr (1999) An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Brain Res. Rev. 29, 1-25.
12. Cassarino D. S., Halvorsen E. M., Swerdlow R. H., Abramova N. N., Parker W. D. Jr, Sturgill T. W. and Bennett J. P. Jr (2000) Interaction among mitochondria, mitogen-activated protein kinases, and nuclear factor-κβ in cellular models of Parkinson's disease. J. Neurochem. 74, 1384-1392.
13. Castellani R., Smith M. A., Richey P. L. and Perry G. (1996) Glycoxidation and oxidative stress in Parkinson disease and diffuse Lewy body disease. Brain Res. 737, 195-200.
14. Castellani R. J., Perry G., Siedlak S. L., Nunomura A., Shimohama S., Zhang J., Montine T., Sayre L. M. and Smith M. A. (2002) Hydroxynonenal adducts indicate a role for lipid peroxidation in neocortical and brainstem Lewy bodies in humans. Neurosci. Lett. 319, 25-28.
15. Conway K. A., Harper J. D. and Lansbury P. T. (1998) Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease. Nat. Med. 4, 1318-1320.
16. D'Andrea M. R., Ilyin S. and Plata-Salaman C. R. (2001) Abnormal patterns of microtubule-associated protein-2 (MAP-2) immunolabeling in neuronal nuclei and Lewy bodies in Parkinson's disease substantia nigra brain tissues. Neurosci. Lett. 306, 137-140.
17. Dickson D. W. (2001) α-synuclein and the Lewy body disorders. Curr. Opin. Neurol. 14, 423-432.
18. Foley P. and Riederer P. (2000) Influence of neurotoxins and oxidative stress on the onset and progression of Parkinson's disease. J. Neurol. 247, 1182-1194.
19. Foltynie T., Brayne C. and Barker R. A. (2002) The heterogeneity of idiopathic Parkinson's disease. J. Neurol. 249, 138-145.
20. Forno L. S. (1996) Neuropathology of Parkinson's disease. J. Neuropathol. Exp. Neurol. 55, 259-272.
21. Gai W. P., Blumbergs P. C. and Blessing W. W. (1996) Microtubule-associated protein 5 is a component of Lewy bodies and Lewy neurites in the brainstem and forebrain regions affected in Parkinson's disease. Acta Neuropathol. 91, 78-81.
22. Gai W. P., Yuan H. X., Li X. Q., Power J. T., Blumbergs P. C. and Jensen P. H. (2000) In situ and in vitro study of colocalization and segregation of α-synuclein, ubiquitin, and lipids in Lewy bodies. Exp. Neurol. 166, 324-333.
23. Galloway P. G., Mulvihill P. and Perry G. (1992) Filaments of Lewy bodies contain insoluble cytoskeletal elements. Am. J. Pathol. 140, 809-822.
24. Ghosh S. S., Swerdlow R. H., Miller S. W., Sheeman B., Parker W. D. Jr and Davis R. E. (1999) Use of cytoplasmic hybrid cell lines for elucidating the role of mitochondrial dysfunction in Alzheimer's disease and Parkinson's disease. Ann. NY Acad. Sci. 893, 176-191.
25. Giasson B. I., Duda J. E., Murray I. V., Chen Q., Souza J. M., Hurtig H. I., Ischiropoulos H., Trojanowski J. Q. and Lee V. M. (2000) Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions. Science 290, 985-989.
26. Goedert M. (2001) α-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2, 492-501.
27. Gosavi N., Lee H. J., Lee J. S., Patel S. and Lee S. J. (2002) Golgi fragmentation occurs in the cells with prefibrillar α-synuclein aggregates and precedes the formation of fibrillar inclusion. J. Biol. Chem. 277, 48984-48992.
28. Graham D. I. and Lantos P. L., eds. (2002) Greenfields's Neuropathology, 7th edn, pp. 237-238. Oxford University Press, London.
29. Hashimoto M., Hsu L. J., Sisk A., Xia Y., Takeda A., Sundsmo M. and Masliah E. (1998) Human recombinant NACP/α-synuclein is aggregated and fibrillated in vitro: relevance for Lewy body disease. Brain Res. 799, 301-306.
30. Hashimoto M., Takeda A., Hsu L. J., Takenouchi T. and Masliah E. (1999) Role of cytochrome c as a stimulator of α-synuclein aggregation in Lewy body disease. J. Biol. Chem. 274, 28849-28852.
31. Hashimoto M., Rockenstein E., Mante M., Mallory M. and Masliah E. (2001) β-Synuclein inhibits α-synuclein aggregation: a possible role as an anti-parkinsonian factor. Neuron 32, 213-223.
32. Hill W. D., Lee V. M., Hurtig H. I., Murray J. M. and Trojanowski J. Q. (1991) Epitopes located in spatially separate domains of each neurofilament subunit are present in Parkinson's disease Lewy bodies. J. Comp. Neurol. 309, 150-160.
33. Hishikawa N., Hashizume Y., Yoshida M. and Sobue G. (2003) Clinical and neuropathological correlates of Lewy body disease. Acta Neuropathol. 105, 341-350.
34. Hoehn M. M. and Yahr M. D. (1967) Parkinsonism: onset, progression, and mortality 1967. Neurology 57, S11-S26.
35. Ii K., Ito H., Tanaka K. and Hirano A. (1997) Immunocytochemical co-localization of the proteasome in ubiquitinated structures in neurodegenerative diseases and the elderly. J. Neuropathol. Exp. Neurol. 56, 125-131.
36. Ishizawa T., Mattila P., Davies P., Wang D. and Dickson D. W. (2003) Colocalization of tau and α-synuclein epitopes in Lewy bodies. J. Neuropathol. Exp. Neurol. 62, 389-397.
37. Iwatsubo T., Nakano I., Fukunaga K. and Miyamoto E. (1991) Ca2+/calmodulin-dependent protein kinase II immunoreactivity in Lewy bodies. Acta Neuropathol. 82, 159-163.
38. Jellinger K. A. (2001) The pathology of Parkinson's disease. Adv. Neurol. 86, 55-72.
39. Kahle P. J., Neumann M., Ozmen L. and Haass C. (2000) Physiology and pathophysiology of α-synuclein. Cell culture and transgenic animal models based on a Parkinson's disease-associated protein. Ann. NY Acad. Sci. 920, 33-41.
40. Kovari E., Gold G., Herrmann F. R., Canuto A., Hof P. R., Bouras C. and Giannakopoulos P. (2003) Lewy body densities in the entorhinal and anterior cingulate cortex predict cognitive deficits in Parkinson's disease. Acta Neuropathol. 106, 83-88.
41. Lee H. J. and Lee S. J. (2002) Characterization of cytoplasmic α-synuclein aggregates. Fibril formation is tightly linked to the inclusion-forming process in cells. J. Biol. Chem. 277, 48976-48983.
42. Lee H. J., Shin S. Y., Choi C., Lee Y. H. and Lee S. J. (2002) Formation and removal of α-synuclein aggregates in cells exposed to mitochondrial inhibitors. J. Biol. Chem. 277, 5411-5417.
43. Lowe J., McDermott H., Landon M., Mayer R. J. and Wilkinson K. D. (1990) Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J. Pathol. 161, 153-160.
44. McLean P. J., Kawamata H., Shariff S., Hewett J., Sharma N., Ueda K., Breakefield X. O. and Hyman B. T. (2002) TorsinA and heat shock proteins act as molecular chaperones: suppression of α-synuclein aggregation. J. Neurochem. 83, 846-854.
45. McNaught K. S. and Olanow C. W. (2003) Proteolytic stress: a unifying concept for the etiopathogenesis of Parkinson's disease. Ann. Neurol. 53, S73-S86.
46. McNaught K. S., Belizaire R., Jenner P., Olanow C. W. and Isacson O. (2002a) Selective loss of 20S proteasome α-subunits in the substantia nigra pars compacta in Parkinson's disease. Neurosci. Lett. 326, 155-158.
47. McNaught K. S., Mytilineou C., Jnobaptiste R., Yabut J., Shashidharan P., Jennert P. and Olanow C. W. (2002b) Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J. Neurochem. 81, 301-306.
48. McNaught K. S., Shashidharan P., Perl D. P., Jenner P. and Olanow C. W. (2002c) Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci. 16, 2136-2148.
49. Miller S. W., Trimmer P. A., Parker W. D. Jr and Davis R. E. (1996) Creation and characterization of mitochondrial DNA-depleted cell lines with 'neuronal-like' properties. J. Neurochem. 67, 1897-1907.
50. Mochizuki A., Komatsuzaki Y. and Shoji S. (2002) Association of Lewy bodies and glial cytoplasmic inclusions in the brain of Parkinson's disease. Acta Neuropathol. 104, 534-537.
51. Murray I. J., Medford M. A., Guan H. P., Rueter S. M., Trojanowski J. Q. and Lee V. M. (2003) Synphilin in normal human brains and in synucleinopathies: studies with new antibodies. Acta Neuropathol. 105, 177-184.
52. Nakashima S. and Ikuta F. (1984) Tyrosine hydroxylase protein in Lewy bodies of parkinsonian and senile brains. J. Neurol. Sci. 66, 91-96.
53. Nishiyama K., Murayama S., Shimizu J., Ohya Y., Kwak S., Asayama K. and Kanazawa I. (1995) Cu/Zn superoxide dismutase-like immunoreactivity is present in Lewy bodies from Parkinson disease: a light and electron microscopic immunocytochemical study. Acta Neuropathol. 89, 471-474.
54. Park J. Y. and Lansbury P. T. Jr (2003) β-synuclein inhibits formation of α-synuclein protofibrils: a possible therapeutic strategy against Parkinson's disease. Biochemistry 42, 3696-3700.
55. Parker W. D. Jr and Swerdlow R. H. (1998) Mitochondrial dysfunction in idiopathic Parkinson disease. Am. J. Hum. Genet. 62, 758-762.
56. Pollanen M. S., Dickson D. W. and Bergeron C. (1993) Pathology and biology of the Lewy body. J. Neuropathol. Exp. Neurol. 52, 183-191.
57. Sakamoto M., Uchihara T., Hayashi M., Nakamura A., Kikuchi E., Mizutani T., Mizusawa H. and Hirai S. (2002) Heterogeneity of nigral and cortical Lewy bodies differentiated by amplified triple-labeling for α-synuclein, ubiquitin, and thiazin red. Exp. Neurol. 177, 88-94.
58. Schapira A. H., Gu M., Taanman J. W., Tabrizi S. J., Seaton T., Cleeter M. and Cooper J. M. (1998) Mitochondria in the etiology and pathogenesis of Parkinson's disease. Ann. Neurol. 44, S89-S98.
59. Schipper H. M., Liberman A. and Stopa E. G. (1998) Neural heme oxygenase-1 expression in idiopathic Parkinson's disease. Exp. Neurol. 150, 60-68.
60. Schlossmacher M. G., Frosch M. P., Gai W. P. et al. (2002) Parkin localizes to the Lewy bodies of Parkinson disease and dementia with Lewy bodies. Am. J. Pathol. 160, 1655-1667.
61. Schneider J. A., Bienias J. L., Gilley D. W., Kvamberg D. E., Mufson E. J. and Bennett D. A. (2002) Improved detection of substantia nigra pathology in Alzheimer's disease. J. Histochem. Cytochem. 50, 99-106.
62. Sheehan J. P., Swerdlow R. H., Parker W. D., Miller S. W., Davis R. E. and Tuttle J. B. (1997) Altered calcium homeostasis in cells transformed by mitochondria from individuals with Parkinson's disease. J. Neurochem. 68, 1221-1233.
63. Sherer T. B., Betarbet R., Stout A. K., Lund S., Baptista M., Panov A. V., Cookson M. R. and Greenamyre J. T. (2002) An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered α-synuclein metabolism and oxidative damage. J. Neurosci. 22, 7006-7015.
64. Swerdlow R. H., Parks J. K., Miller S. W. et al. (1996) Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 40, 663-671.
65. Swerdlow R. H., Parks J. K., Davis J. N. et al. (1998) Matrilineal inheritance of complex I dysfunction in a multigenerational Parkinson's disease family. Ann. Neurol. 44, 873-881.
66. Swerdlow R. H., Parks J. K., Cassarino D. S., Shilling A. T., Bennett J. P. Jr, Harrison M. B. and Parker W. D. Jr (1999) Characterization of cybrid cell lines containing mtDNA from Huntington's disease patients. Biochem. Biophys. Res. Commun. 261, 701-704.
67. Swerdlow R. H., Parks J. K., Cassarino D. S., Binder D. R., Bennett J. P. Jr, Di Iorio G., Golbe L. I. and Parker W. D. Jr (2001) Biochemical analysis of cybrids expressing mitochondrial DNA from Contursi kindred Parkinson's subjects. Exp. Neurol. 169, 479-485.
68. Tabrizi S. J., Cooper J. M. and Schapira A. H. (1998) Mitochondrial DNA in focal dystonia: a cybrid analysis. Ann. Neurol. 44, 258-261.
69. Takahashi H. and Wakabayashi K. (2001) The cellular pathology of Parkinson's disease. Neuropathology 21, 315-322.
70. Terry R. D. (2000) Do neuronal inclusions kill the cell? J. Neural Transm. Suppl. 59, 91-93.
71. Tofaris G. K., Layfield R. and Spillantini M. G. (2001) α-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett. 509, 22-26.
72. Tompkins M. M. and Hill W. D. (1997) Contribution of somal Lewy bodies to neuronal death. Brain Res. 775, 24-29.
73. Trimmer P. A., Swerdlow R. H., Parks J. K., Keeney P., Bennett J. P. Jr, Miller S. W., Davis R. E. and Parker W. D. Jr (2000) Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp. Neurol. 162, 37-50.
74. Trojanowski J. Q. and Lee V. M. (2002) Parkinson's disease and related synucleinopathies are a new class of nervous system amyloidoses. Neurotoxicology 23, 457-460.
75. Veech G. A., Dennis J., Keeney P. M., Fall C. P., Swerdlow R. H., Parker W. D. Jr and Bennett J. P. Jr (2000) Disrupted mitochondrial electron transport function increases expression of anti-apoptotic bcl-2 and bcl-X (L) proteins in SH-SY5Y neuroblastoma and in Parkinson disease cybrid cells through oxidative stress. J. Neurosci. Res. 61, 693-700.
76. Wooten G. F., Currie L. J., Bennett J. P., Harrison M. B., Trugman J. M. and Parker W. D. Jr (1997) Maternal inheritance in Parkinson's disease. Ann. Neurol. 41, 265-268.