Synuclein and neuronal cell death

Molecular Neurodegeneration

Volumn 4, Issue 1, 2009, Pages

  Cookson, Mark R ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; MUTANT PROTEIN;

ARTICLE; CELL LOSS; DOPAMINERGIC NERVE CELL; FAMILIAL DISEASE; HUMAN; LEWY BODY; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; SUBSTANTIA NIGRA;

EID: 61549111872     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-4-4     Document Type: Article

References (173)

1. The early diagnosis of Parkinson's disease. DJ Brooks, Ann Neurol 1998 44 S10 18 10.1002/ana.410440107 9749569
2. Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: Is this the target for Parkinson's disease? Y Chu JH Kordower, Neurobiol Dis 2007 25 134 149 10.1016/j.nbd.2006.08.021 17055279
3. Neurodegeneration in normal brain aging and disease. DR Thal K Del Tredici H Braak, Sci Aging Knowledge Environ 2004 2004 pe26 10.1126/sageke.2004. 23.pe26 15190177
4. Linking selective vulnerability to cell death mechanisms in Parkinson's disease. DW Dickson, Am J Pathol 2007 170 16 19 17200178 10.2353/ajpath.2007. 061011
5. Biochemistry of Parkinson's disease with special reference to the dopaminergic systems. EC Hirsch, Mol Neurobiol 1994 9 135 142 10.1007/BF02816113 7888089
6. Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. CY Chung H Seo KC Sonntag A Brooks L Lin O Isacson, Hum Mol Genet 2005 14 1709 1725 10.1093/hmg/ddi178 15888489
7. Calcium, ageing, and neuronal vulnerability in Parkinson's disease. DJ Surmeier, Lancet Neurol 2007 6 933 938 10.1016/S1474-4422(07)70246-6 17884683
8. The Parkinson's complex: parkinsonism is just the tip of the iceberg. JW Langston, Ann Neurol 2006 59 591 596 10.1002/ana.20834 16566021
9. Age-related loss of dorsal vagal neurons in Parkinson's disease. WP Gai PC Blumbergs LB Geffen WW Blessing, Neurology 1992 42 2106 2111 1436519
10. Post mortem studies in Parkinson's disease-is it possible to detect brain areas for specific symptoms? KA Jellinger, J Neural Transm Suppl 1999 56 1 29 10370901
11. In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin, and lipids in Lewy bodies. WP Gai HX Yuan XQ Li JT Power PC Blumbergs PH Jensen, Exp Neurol 2000 166 324 333 10.1006/exnr.2000.7527 11085897
12. Anti-ubiquitin immunocytochemistry is more sensitive than conventional techniques in the detection of diffuse Lewy body disease. G Lennox J Lowe K Morrell M Landon RJ Mayer, J Neurol Neurosurg Psychiatry 1989 52 67 71 2540286 10.1136/jnnp.52.1.67
13. Neuronal inclusions of Parkinson's disease. WR Gibb T Scott AJ Lees, Mov Disord 1991 6 2 11 10.1002/mds.870060103 1848677
14. Staging of brain pathology related to sporadic Parkinson's disease. H Braak K Del Tredici U Rub RA de Vos EN Jansen Steur E Braak, Neurobiol Aging 2003 24 197 211 10.1016/S0197-4580(02)00065-9 12498954
15. Where does parkinson disease pathology begin in the brain? K Del Tredici U Rub RA De Vos JR Bohl H Braak, J Neuropathol Exp Neurol 2002 61 413 426 12030260
16. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. AJ Hughes SE Daniel L Kilford AJ Lees, J Neurol Neurosurg Psychiatry 1992 55 181 184 1564476 10.1136/jnnp.55.3.181
17. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. L Maroteaux JT Campanelli RH Scheller, J Neurosci 1988 8 2804 2815 3411354
18. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. JM George H Jin WS Woods DF Clayton, Neuron 1995 15 361 372 10.1016/0896-6273(95)90040-3 7646890
19. The synucleins. JM George, Genome Biol 2002 3 REVIEWS3002 11806835
20. alpha-Synuclein A53T substitution associated with Parkinson disease also marks the divergence of Old World and New World primates. BA Hamilton, Genomics 2004 83 739 742 10.1016/j.ygeno.2003.09.016 15028296
21. Alpha-synuclein in blood and brain from familial Parkinson disease with SNCA locus triplication. DW Miller SM Hague J Clarimon M Baptista K Gwinn-Hardy MR Cookson AB Singleton, Neurology 2004 62 1835 1838 15159488
22. GATA transcription factors directly regulate the Parkinson's disease-linked gene alpha-synuclein. CR Scherzer JA Grass Z Liao I Pepivani B Zheng AC Eklund PA Ney J Ng M McGoldrick B Mollenhauer EH Bresnick MG Schlossmacher, Proc Natl Acad Sci USA 2008 105 10907 10912 18669654 10.1073/pnas.0802437105
23. alpha-Synuclein membrane interactions and lipid specificity. E Jo J McLaurin CM Yip P St George-Hyslop PE Fraser, J Biol Chem 2000 275 34328 34334 10.1074/jbc.M004345200 10915790
24. Delayed localization of synelfin (synuclein, NACP) to presynaptic terminals in cultured rat hippocampal neurons. GS Withers JM George GA Banker DF Clayton, Brain Res Dev Brain Res 1997 99 87 94 10.1016/S0165-3806(96)00210-6 9088569
25. Characterization of the precursor protein of the non-A beta component of senile plaques (NACP) in the human central nervous system. MC Irizarry TW Kim M McNamara RE Tanzi JM George DF Clayton BT Hyman, J Neuropathol Exp Neurol 1996 55 889 895 8759778
26. Lipid rafts mediate the synaptic localization of alpha-synuclein. DL Fortin MD Troyer K Nakamura S Kubo MD Anthony RH Edwards, J Neurosci 2004 24 6715 6723 10.1523/JNEUROSCI.1594-04.2004 15282274
27. Neural activity controls the synaptic accumulation of alpha-synuclein. DL Fortin VM Nemani SM Voglmaier MD Anthony TA Ryan RH Edwards, J Neurosci 2005 25 10913 10921 10.1523/JNEUROSCI.2922-05.2005 16306404
28. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. A Abeliovich Y Schmitz I Farinas D Choi-Lundberg WH Ho PE Castillo N Shinsky JM Verdugo M Armanini A Ryan M Hynes H Phillips D Sulzer A Rosenthal, Neuron 2000 25 239 252 10.1016/S0896-6273(00)80886-7 10707987
29. Altered short-term hippocampal synaptic plasticity in mutant alpha-synuclein transgenic mice. JV Steidl T Gomez-Isla A Mariash KH Ashe LM Boland, Neuroreport 2003 14 219 223 10.1097/00001756-200302100-00012 12598733
30. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. DE Cabin K Shimazu D Murphy NB Cole W Gottschalk KL McIlwain B Orrison A Chen CE Ellis R Paylor B Lu RL Nussbaum, J Neurosci 2002 22 8797 8807 12388586
31. Stressor-related impairment of synaptic transmission in hippocampal slices from alpha-synuclein knockout mice. ED Martin C Gonzalez-Garcia M Milan I Farinas V Cena, Eur J Neurosci 2004 20 3085 3091 10.1111/j.1460-9568.2004. 03801.x 15579163
32. alpha-Synuclein produces a long-lasting increase in neurotransmitter release. S Liu I Ninan I Antonova F Battaglia F Trinchese A Narasanna N Kolodilov W Dauer RD Hawkins O Arancio, Embo J 2004 23 4506 4516 15510220 10.1038/sj.emboj.7600451
33. Alpha-synuclein in Lewy bodies. MG Spillantini ML Schmidt VM Lee JQ Trojanowski R Jakes M Goedert, Nature 1997 388 839 840 10.1038/42166 9278044
34. Abnormal accumulation of NACP/alpha-synuclein in neurodegenerative disorders. A Takeda M Mallory M Sundsmo W Honer L Hansen E Masliah, Am J Pathol 1998 152 367 372 9466562
35. Characterisation of isolated alpha-synuclein filaments from substantia nigra of Parkinson's disease brain. RA Crowther SE Daniel M Goedert, Neurosci Lett 2000 292 128 130 10.1016/S0304-3940(00)01440-3 10998565
36. Selective insolubility of alpha-synuclein in human Lewy body diseases is recapitulated in a transgenic mouse model. PJ Kahle M Neumann L Ozmen V Muller S Odoy N Okamoto H Jacobsen T Iwatsubo JQ Trojanowski H Takahashi K Wakabayashi N Bogdanovic P Riederer HA Kretzschmar C Haass, Am J Pathol 2001 159 2215 2225 11733371
37. Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease. JP Anderson DE Walker JM Goldstein R de Laat K Banducci RJ Caccavello R Barbour J Huang K Kling M Lee L Diep PS Keim X Shen T Chataway MG Schlossmacher P Seubert D Schenk S Sinha WP Gai TJ Chilcote, J Biol Chem 2006 281 29739 29752 10.1074/jbc. M600933200 16847063
38. alpha-Synuclein is phosphorylated in synucleinopathy lesions. H Fujiwara M Hasegawa N Dohmae A Kawashima E Masliah MS Goldberg J Shen K Takio T Iwatsubo, Nat Cell Biol 2002 4 160 164 10.1038/ncb841 11813001
39. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. BI Giasson JE Duda IV Murray Q Chen JM Souza HI Hurtig H Ischiropoulos JQ Trojanowski VM Lee, Science 2000 290 985 989 10.1126/science.290.5493.985 11062131
40. Ubiquitination of alpha-synuclein in Lewy bodies is a pathological event not associated with impairment of proteasome function. GK Tofaris A Razzaq B Ghetti KS Lilley MG Spillantini, J Biol Chem 2003 278 44405 44411 10.1074/jbc.M308041200 12923179
41. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. JH Kordower Y Chu RA Hauser TB Freeman CW Olanow, Nat Med 2008 14 504 506 10.1038/nm1747 18391962
42. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. JY Li E Englund JL Holton D Soulet P Hagell AJ Lees T Lashley NP Quinn S Rehncrona A Bjorklund H Widner T Revesz O Lindvall P Brundin, Nat Med 2008 14 501 503 10.1038/nm1746 18391963
43. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. I Mendez A Vinuela A Astradsson K Mukhida P Hallett H Robertson T Tierney R Holness A Dagher JQ Trojanowski O Isacson, Nat Med 2008 14 507 509 10.1038/nm1752 18391961
44. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. MH Polymeropoulos C Lavedan E Leroy SE Ide A Dehejia A Dutra B Pike H Root J Rubenstein R Boyer ES Stenroos S Chandrasekharappa A Athanassiadou T Papapetropoulos WG Johnson AM Lazzarini RC Duvoisin G Di Iorio LI Golbe RL Nussbaum, Science 1997 276 2045 2047 10.1126/science.276.5321.2045 9197268
45. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. R Kruger W Kuhn T Muller D Woitalla M Graeber S Kosel H Przuntek JT Epplen L Schols O Riess, Nat Genet 1998 18 106 108 10.1038/ng0298-106 9462735
46. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. JJ Zarranz J Alegre JC Gomez-Esteban E Lezcano R Ros I Ampuero L Vidal J Hoenicka O Rodriguez B Atares V Llorens E Gomez Tortosa T del Ser DG Munoz JG de Yebenes, Ann Neurol 2004 55 164 173 10.1002/ana.10795 14755719
47. Concurrence of alpha-synuclein and tau brain pathology in the Contursi kindred. JE Duda BI Giasson ME Mabon DC Miller LI Golbe VM Lee JQ Trojanowski, Acta Neuropathol 2002 104 7 11 10.1007/s00401-002-0563-3 12070658
48. Abundant neuritic inclusions and microvacuolar changes in a case of diffuse Lewy body disease with the A53T mutation in the alpha-synuclein gene. K Yamaguchi EJ Cochran JR Murrell MH Polymeropoulos KM Shannon RA Crowther M Goedert B Ghetti, Acta Neuropathol 2005 110 298 305 10.1007/s00401-005-1042-4 15981014
49. Clinical, neuropathological and genotypic variability in SNCA A53T familial Parkinson's disease. Variability in familial Parkinson's disease. K Markopoulou DW Dickson RD McComb ZK Wszolek L Katechalidou L Avery MS Stansbury BA Chase, Acta Neuropathol 2008 116 25 35 10.1007/s00401-008-0372-4 18389263
50. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. MC Chartier-Harlin J Kachergus C Roumier V Mouroux X Douay S Lincoln C Levecque L Larvor J Andrieux M Hulihan N Waucquier L Defebvre P Amouyel M Farrer A Destee, Lancet 2004 364 1167 1169 10.1016/S0140-6736(04)17103-1 15451224
51. alpha-Synuclein locus triplication causes Parkinson's disease. AB Singleton M Farrer J Johnson A Singleton S Hague J Kachergus M Hulihan T Peuralinna A Dutra R Nussbaum S Lincoln A Crawley M Hanson D Maraganore C Adler MR Cookson M Muenter M Baptista D Miller J Blancato J Hardy K Gwinn-Hardy, Science 2003 302 841 10.1126/science.1090278 14593171
52. Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication. J Fuchs C Nilsson J Kachergus M Munz EM Larsson B Schule JW Langston FA Middleton OA Ross M Hulihan T Gasser MJ Farrer, Neurology 2007 68 916 922 10.1212/01.wnl.0000254458.17630.c5 17251522
53. Collaborative analysis of alpha-synuclein gene promoter variability and Parkinson disease. DM Maraganore M de Andrade A Elbaz MJ Farrer JP Ioannidis R Kruger WA Rocca NK Schneider TG Lesnick SJ Lincoln MM Hulihan JO Aasly T Ashizawa MC Chartier-Harlin H Checkoway C Ferrarese G Hadjigeorgiou N Hattori H Kawakami JC Lambert T Lynch GD Mellick S Papapetropoulos A Parsian A Quattrone O Riess EK Tan C Van Broeckhoven, JAMA 2006 296 661 670 10.1001/jama.296.6.661 16896109
54. Multiple regions of alpha-synuclein are associated with Parkinson's disease. JC Mueller J Fuchs A Hofer A Zimprich P Lichtner T Illig D Berg U Wullner T Meitinger T Gasser, Ann Neurol 2005 57 535 541 10.1002/ana.20438 15786467
55. The biochemistry of Parkinson's disease. MR Cookson, Annu Rev Biochem 2005 74 29 52 10.1146/annurev.biochem.74.082803.133400 15952880
56. alpha-Synuclein fission yeast model: concentration-dependent aggregation without plasma membrane localization or toxicity. KA Brandis IF Holmes SJ England N Sharma L Kukreja SK DebBurman, J Mol Neurosci 2006 28 179 191 10.1385/JMN:28:2:179 16679557
57. Functional mitochondria are required for alpha-synuclein toxicity in aging yeast. S Buttner A Bitto J Ring M Augsten P Zabrocki T Eisenberg H Jungwirth S Hutter D Carmona-Gutierrez G Kroemer J Winderickx F Madeo, J Biol Chem 2008 283 7554 7560 10.1074/jbc.M708477200 18192273
58. Alpha-synuclein targets the plasma membrane via the secretory pathway and induces toxicity in yeast. C Dixon N Mathias RM Zweig DA Davis DS Gross, Genetics 2005 170 47 59 15744056 10.1534/genetics.104.035493
59. Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson's disease. TR Flower LS Chesnokova CA Froelich C Dixon SN Witt, J Mol Biol 2005 351 1081 1100 10.1016/j.jmb.2005.06.060 16051265
60. Novel suppressors of alpha-synuclein toxicity identified using yeast. J Liang C Clark-Dixon S Wang TR Flower T Williams-Hart R Zweig LC Robinson K Tatchell SN Witt, Hum Mol Genet 2008 17 3784 3795 10.1093/hmg/ddn276 18772193
61. Yeast cells provide insight into alpha-synuclein biology and pathobiology. TF Outeiro S Lindquist, Science 2003 302 1772 1775 14657500 10.1126/science.1090439
62. alpha-Synuclein budding yeast model: toxicity enhanced by impaired proteasome and oxidative stress. N Sharma KA Brandis SK Herrera BE Johnson T Vaidya R Shrestha SK Debburman, J Mol Neurosci 2006 28 161 178 10.1385/JMN:28:2:161 16679556
63. Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. S Willingham TF Outeiro MJ DeVit SL Lindquist PJ Muchowski, Science 2003 302 1769 1772 10.1126/science.1090389 14657499
64. Phosphorylation, lipid raft interaction and traffic of alpha-synuclein in a yeast model for Parkinson. P Zabrocki I Bastiaens C Delay T Bammens R Ghillebert K Pellens C De Virgilio F Van Leuven J Winderickx, Biochim Biophys Acta 2008 1783 1767 1780 10.1016/j.bbamcr.2008.06.010 18634833
65. Characterization of alpha-synuclein aggregation and synergistic toxicity with protein tau in yeast. P Zabrocki K Pellens T Vanhelmont T Vandebroek G Griffioen S Wera F Van Leuven J Winderickx, FEBS J 2005 272 1386 1400 10.1111/j.1742-4658.2005.04571.x 15752356
66. Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. L Chen MB Feany, Nat Neurosci 2005 8 657 663 10.1038/nn1443 15834418
67. Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. PK Auluck HY Chan JQ Trojanowski VM Lee NM Bonini, Science 2002 295 865 868 10.1126/science.1067389 11823645
68. Selective loss of dopaminergic neurons and formation of Lewy body-like aggregations in alpha-synuclein transgenic fly neuronal cultures. SS Park D Lee, Eur J Neurosci 2006 23 2908 2914 10.1111/j.1460-9568.2006.04844.x 16819979
69. Mutant alpha-synuclein-induced degeneration is reduced by parkin in a fly model of Parkinson's disease. AF Haywood BE Staveley, Genome 2006 49 505 510 10.1139/G06-011 16767175
70. Aggregated alpha-synuclein mediates dopaminergic neurotoxicity in vivo. M Periquet T Fulga L Myllykangas MG Schlossmacher MB Feany, J Neurosci 2007 27 3338 3346 10.1523/JNEUROSCI.0285-07.2007 17376994
71. Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. E Kontopoulos JD Parvin MB Feany, Hum Mol Genet 2006 15 3012 3023 10.1093/hmg/ddl243 16959795
72. Pharmacological prevention of Parkinson disease in Drosophila. PK Auluck NM Bonini, Nat Med 2002 8 1185 1186 10.1038/nm1102-1185 12411925
73. A Drosophila model of Parkinson's disease. MB Feany WW Bender, Nature 2000 404 394 398 10.1038/35006074 10746727
74. Whole-mount analysis reveals normal numbers of dopaminergic neurons following misexpression of alpha-Synuclein in Drosophila. Y Pesah H Burgess B Middlebrooks K Ronningen J Prosser V Tirunagaru J Zysk G Mardon, Genesis 2005 41 154 159 10.1002/gene.20106 15789427
75. A systematic RNAi screen reveals involvement of endocytic pathway in neuronal dysfunction in alpha-synuclein transgenic C. elegans. T Kuwahara A Koyama S Koyama S Yoshina CH Ren T Kato S Mitani T Iwatsubo, Hum Mol Genet 2008 17 2997 3009 10.1093/hmg/ddn198 18617532
76. C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. TJ van Ham KL Thijssen R Breitling RM Hofstra RH Plasterk EA Nollen, PLoS Genet 2008 4 e1000027 18369446 10.1371/journal.pgen. 1000027
77. Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans. T Kuwahara A Koyama K Gengyo-Ando M Masuda H Kowa M Tsunoda S Mitani T Iwatsubo, J Biol Chem 2006 281 334 340 10.1074/jbc.M504860200 16260788
78. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. R Ved S Saha B Westlund C Perier L Burnam A Sluder M Hoener CM Rodrigues A Alfonso C Steer L Liu S Przedborski B Wolozin, J Biol Chem 2005 280 42655 42668 10.1074/jbc.M505910200 16239214
79. A Caenorhabditis elegans Parkin mutant with altered solubility couples alpha-synuclein aggregation to proteotoxic stress. W Springer T Hoppe E Schmidt R Baumeister, Hum Mol Genet 2005 14 3407 3423 10.1093/hmg/ddi371 16204351
80. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. M Lakso S Vartiainen AM Moilanen J Sirvio JH Thomas R Nass RD Blakely G Wong, J Neurochem 2003 86 165 172 10.1046/j.1471-4159.2003.01809.x 12807436
81. Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. L Petrucelli C O'Farrell PJ Lockhart M Baptista K Kehoe L Vink P Choi B Wolozin M Farrer J Hardy MR Cookson, Neuron 2002 36 1007 1019 10.1016/S0896-6273(02)01125-X 12495618
82. Predominant neuritic pathology induced by viral overexpression of alpha-synuclein in cell culture. S Zach H Bueler B Hengerer F Gillardon, Cell Mol Neurobiol 2007 27 505 515 10.1007/s10571-007-9141-5 17380380
83. Overexpression of human alpha-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalon-derived cells. W Zhou MS Hurlbert J Schaack KN Prasad CR Freed, Brain Res 2000 866 33 43 10.1016/S0006-8993(00)02215-0 10825478
84. Overexpression of human alpha-synuclein causes dopamine neuron death in primary human mesencephalic culture. W Zhou J Schaack WM Zawada CR Freed, Brain Res 2002 926 42 50 10.1016/S0006-8993(01)03292-9 11814405
85. DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity. W Zhou CR Freed, J Biol Chem 2005 280 43150 43158 10.1074/jbc.M507124200 16227205
86. Methionine sulfoxide reductase A protects dopaminergic cells from Parkinson's disease-related insults. F Liu J Hindupur JL Nguyen KJ Ruf J Zhu JL Schieler CC Bonham KV Wood VJ Davisson JC Rochet, Free Radic Biol Med 2008 45 242 255 10.1016/j.freeradbiomed.2008.03.022 18456002
87. Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. WW Smith H Jiang Z Pei Y Tanaka H Morita A Sawa VL Dawson TM Dawson CA Ross, Hum Mol Genet 2005 14 3801 3811 10.1093/hmg/ddi396 16239241
88. Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Y Tanaka S Engelender S Igarashi RK Rao T Wanner RE Tanzi A Sawa LD V TM Dawson CA Ross, Hum Mol Genet 2001 10 919 926 10.1093/hmg/10.9.919 11309365
89. Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. J Xu SY Kao FJ Lee W Song LW Jin BA Yankner, Nat Med 2002 8 600 606 10.1038/nm0602-600 12042811
90. Aggregates assembled from overexpression of wild-type alpha-synuclein are not toxic to human neuronal cells. LW Ko HH Ko WL Lin JG Kulathingal SH Yen, J Neuropathol Exp Neurol 2008 67 1084 1096 10.1097/NEN.0b013e31818c3618 18957893
91. Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. BI Giasson JE Duda SM Quinn B Zhang JQ Trojanowski VM Lee, Neuron 2002 34 521 533 10.1016/S0896-6273(02)00682-7 12062037
92. Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha -synuclein in human and transgenic mouse brain. PJ Kahle M Neumann L Ozmen V Muller H Jacobsen A Schindzielorz M Okochi U Leimer H van Der Putten A Probst E Kremmer HA Kretzschmar C Haass, J Neurosci 2000 20 6365 6373 10964942
93. Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53 - > Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice. MK Lee W Stirling Y Xu X Xu D Qui AS Mandir TM Dawson NG Copeland NA Jenkins DL Price, Proc Natl Acad Sci USA 2002 99 8968 8973 12084935 10.1073/pnas.132197599
94. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. E Masliah E Rockenstein I Veinbergs M Mallory M Hashimoto A Takeda Y Sagara A Sisk L Mucke, Science 2000 287 1265 1269 10.1126/science.287.5456.1265 10678833
95. Lack of nigral pathology in transgenic mice expressing human alpha-synuclein driven by the tyrosine hydroxylase promoter. Y Matsuoka M Vila S Lincoln A McCormack M Picciano J LaFrancois X Yu D Dickson WJ Langston E McGowan M Farrer J Hardy K Duff S Przedborski DA Di Monte, Neurobiol Dis 2001 8 535 539 10.1006/nbdi.2001.0392 11442360
96. Behavioral and neurochemical effects of wild-type and mutated human alpha-synuclein in transgenic mice. EK Richfield MJ Thiruchelvam DA Cory-Slechta C Wuertzer RR Gainetdinov MG Caron DA Di Monte HJ Federoff, Exp Neurol 2002 175 35 48 10.1006/exnr.2002.7882 12009758
97. Neuropathology in mice expressing human alpha-synuclein. H van der Putten KH Wiederhold A Probst S Barbieri C Mistl S Danner S Kauffmann K Hofele WP Spooren MA Ruegg S Lin P Caroni B Sommer M Tolnay G Bilbe, J Neurosci 2000 20 6021 6029 10934251
98. Hyperphosphorylation and insolubility of alpha-synuclein in transgenic mouse oligodendrocytes. PJ Kahle M Neumann L Ozmen V Muller H Jacobsen W Spooren B Fuss B Mallon WB Macklin H Fujiwara M Hasegawa T Iwatsubo HA Kretzschmar C Haass, EMBO Rep 2002 3 583 588 12034752 10.1093/embo-reports/kvf109
99. Exacerbated synucleinopathy in mice expressing A53T SNCA on a Snca null background. DE Cabin S Gispert-Sanchez D Murphy G Auburger RR Myers RL Nussbaum, Neurobiol Aging 2005 26 25 35 10.1016/j.neurobiolaging.2004.02.026 15585343
100. Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. HM Gao PT Kotzbauer K Uryu S Leight JQ Trojanowski VM Lee, J Neurosci 2008 28 7687 7698 10.1523/JNEUROSCI.0143-07.2008 18650345
101. Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alpha-synuclein(1-120) : implications for Lewy body disorders. GK Tofaris P Garcia Reitbock T Humby SL Lambourne M O'Connell B Ghetti H Gossage PC Emson LS Wilkinson M Goedert MG Spillantini, J Neurosci 2006 26 3942 3950 10.1523/JNEUROSCI.4965-05.2006 16611810
102. Dopaminergic neuron loss and up-regulation of chaperone protein mRNA induced by targeted over-expression of alpha-synuclein in mouse substantia nigra. JL St Martin J Klucken TF Outeiro P Nguyen C Keller-McGandy I Cantuti-Castelvetri TN Grammatopoulos DG Standaert BT Hyman PJ McLean, J Neurochem 2007 100 1449 1457 17241127
103. Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. D Kirik C Rosenblad C Burger C Lundberg TE Johansen N Muzyczka RJ Mandel A Bjorklund, J Neurosci 2002 22 2780 2791 11923443
104. Neuropathology and neurodegeneration in rodent brain induced by lentiviral vector-mediated overexpression of alpha-synuclein. E Lauwers Z Debyser J Van Dorpe B De Strooper B Nuttin V Baekelandt, Brain Pathol 2003 13 364 372 12946025
105. alpha -Synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. C Lo Bianco JL Ridet BL Schneider N Deglon P Aebischer, Proc Natl Acad Sci USA 2002 99 10813 10818 12122208 10.1073/pnas.152339799
106. Overexpression of alpha-synuclein in rat substantia nigra results in loss of dopaminergic neurons, phosphorylation of alpha-synuclein and activation of caspase-9: resemblance to pathogenetic changes in Parkinson's disease. M Yamada T Iwatsubo Y Mizuno H Mochizuki, J Neurochem 2004 91 451 461 10.1111/j.1471-4159.2004.02728.x 15447678
107. Long-term consequences of human alpha-synuclein overexpression in the primate ventral midbrain. A Eslamboli M Romero-Ramos C Burger T Bjorklund N Muzyczka RJ Mandel H Baker RM Ridley D Kirik, Brain 2007 130 799 815 10.1093/brain/awl382 17303591
108. Nigrostriatal alpha-synucleinopathy induced by viral vector-mediated overexpression of human alpha-synuclein: a new primate model of Parkinson's disease. D Kirik LE Annett C Burger N Muzyczka RJ Mandel A Bjorklund, Proc Natl Acad Sci USA 2003 100 2884 2889 12601150 10.1073/pnas.0536383100
109. Neuronal specificity of alpha-synuclein toxicity and effect of Parkin co-expression in primates. T Yasuda S Miyachi R Kitagawa K Wada T Nihira YR Ren Y Hirai N Ageyama K Terao T Shimada M Takada Y Mizuno H Mochizuki, Neuroscience 2007 144 743 753 10.1016/j.neuroscience.2006.09.052 17101231
110. A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. VN Uversky, J Biomol Struct Dyn 2003 21 211 234 12956606
111. Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. VN Uversky, J Neurochem 2007 103 17 37 17623039
112. Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. HJ Lee C Choi SJ Lee, J Biol Chem 2002 277 671 678 10.1074/jbc.M107045200 11679584
113. Oxidative Stress involvement in alpha-synuclein oligomerization in Parkinsons disease cybrids. AR Esteves DM Arduino RH Swerdlow CR Oliveira SM Cardoso, Antioxid Redox Signal 2008 18717628
114. Formation of toxic oligomeric alpha-synuclein species in living cells. TF Outeiro P Putcha JE Tetzlaff R Spoelgen M Koker F Carvalho BT Hyman PJ McLean, PLoS ONE 2008 3 e1867 18382657 10.1371/journal.pone.0001867
115. The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. R Sharon I Bar-Joseph MP Frosch DM Walsh JA Hamilton DJ Selkoe, Neuron 2003 37 583 595 10.1016/S0896-6273(03)00024-2 12597857
116. Characterization of cytoplasmic alpha-synuclein aggregates. Fibril formation is tightly linked to the inclusion-forming process in cells. HJ Lee SJ Lee, J Biol Chem 2002 277 48976 48983 10.1074/jbc.M208192200 12351642
117. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. N Ostrerova-Golts L Petrucelli J Hardy JM Lee M Farer B Wolozin, J Neurosci 2000 20 6048 6054 10934254
118. Different species of alpha-synuclein oligomers induce calcium influx and seeding. KM Danzer D Haasen AR Karow S Moussaud M Habeck A Giese H Kretzschmar B Hengerer M Kostka, J Neurosci 2007 27 9220 9232 10.1523/JNEUROSCI.2617-07.2007 17715357
119. Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. HJ Lee S Patel SJ Lee, J Neurosci 2005 25 6016 6024 10.1523/JNEUROSCI.0692-05.2005 15976091
120. Detection of novel intracellular alpha-synuclein oligomeric species by fluorescence lifetime imaging. J Klucken TF Outeiro P Nguyen PJ McLean BT Hyman, Faseb J 2006 20 2050 2057 10.1096/fj.05-5422com 17012257
121. Impairment of redox state and dopamine level induced by alpha-synuclein aggregation and the prevention effect of hsp70. F Yu H Xu M Zhuo L Sun A Dong X Liu, Biochem Biophys Res Commun 2005 331 278 284 10.1016/j.bbrc.2005.03.148 15845390
122. Isolation of a human single chain antibody fragment against oligomeric alpha-synuclein that inhibits aggregation and prevents alpha-synuclein-induced toxicity. S Emadi H Barkhordarian MS Wang P Schulz MR Sierks, J Mol Biol 2007 368 1132 1144 17391701 10.1016/j.jmb.2007.02.089
123. Inhibiting aggregation of alpha-synuclein with human single chain antibody fragments. S Emadi R Liu B Yuan P Schulz C McAllister Y Lyubchenko A Messer MR Sierks, Biochemistry 2004 43 2871 2878 10.1021/bi036281f 15005622
124. The phosphorylation state of Ser-129 in human alpha-synuclein determines neurodegeneration in a rat model of Parkinson disease. OS Gorbatyuk S Li LF Sullivan W Chen G Kondrikova FP Manfredsson RJ Mandel N Muzyczka, Proc Natl Acad Sci USA 2008 105 763 768 18178617 10.1073/pnas.0711053105
125. Alpha-synuclein phosphorylation enhances eosinophilic cytoplasmic inclusion formation in SH-SY5Y cells. WW Smith RL Margolis X Li JC Troncoso MK Lee VL Dawson TM Dawson T Iwatsubo CA Ross, J Neurosci 2005 25 5544 5552 10.1523/JNEUROSCI.0482-05.2005 15944382
126. Phosphorylation at Ser-129 but not the phosphomimics S129E/D inhibits the fibrillation of alpha-synuclein. KE Paleologou AW Schmid CC Rospigliosi HY Kim GR Lamberto RA Fredenburg PT Lansbury Jr CO Fernandez D Eliezer M Zweckstetter HA Lashuel, J Biol Chem 2008 283 16895 16905 10.1074/jbc.M800747200 18343814
127. Polo-like kinase 2 (PLK2) phosphorylates alpha-synuclein at serine 129 in central nervous system. KJ Inglis D Chereau EF Brigham SS Chiou S Schobel NL Frigon M Yu RJ Caccavello S Nelson R Motter S Wright D Chian P Santiago F Soriano C Ramos K Powell JM Goldstein M Babcock T Yednock F Bard GS Basi H Sham TJ Chilcote L McConlogue I Griswold-Prenner JP Anderson, J Biol Chem 2008 19004816
128. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. DP Seeburg M Feliu-Mojer J Gaiottino DT Pak M Sheng, Neuron 2008 58 571 583 18498738 10.1016/j.neuron.2008.03.021
129. Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro. W Hoyer D Cherny V Subramaniam TM Jovin, Biochemistry 2004 43 16233 16242 10.1021/bi048453u 15610017
130. Aggregation promoting C-terminal truncation of alpha-synuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations. W Li N West E Colla O Pletnikova JC Troncoso L Marsh TM Dawson P Jakala T Hartmann DL Price MK Lee, Proc Natl Acad Sci USA 2005 102 2162 2167 15684072 10.1073/pnas.0406976102
131. A precipitating role for truncated alpha-synuclein and the proteasome in alpha-synuclein aggregation: implications for pathogenesis of Parkinson disease.
132. Selective loss of nigral dopamine neurons induced by overexpression of truncated human alpha-synuclein in mice. M Wakamatsu A Ishii S Iwata J Sakagami Y Ukai M Ono D Kanbe S Muramatsu K Kobayashi T Iwatsubo M Yoshimoto, Neurobiol Aging 2008 29 574 585 10.1016/j.neurobiolaging.2006.11.017 17174013
133. Induction of alpha-synuclein aggregation by intracellular nitrative insult. E Paxinou Q Chen M Weisse BI Giasson EH Norris SM Rueter JQ Trojanowski VM Lee H Ischiropoulos, J Neurosci 2001 21 8053 8061 11588178
134. Alpha-Synuclein is degraded by both autophagy and the proteasome. JL Webb B Ravikumar J Atkins JN Skepper DC Rubinsztein, J Biol Chem 2003 278 25009 25013 10.1074/jbc.M300227200 12719433
135. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. AM Cuervo L Stefanis R Fredenburg PT Lansbury D Sulzer, Science 2004 305 1292 1295 10.1126/science.1101738 15333840
136. Calpain-cleavage of alpha-synuclein: connecting proteolytic processing to disease-linked aggregation. BM Dufty LR Warner ST Hou SX Jiang T Gomez-Isla KM Leenhouts JT Oxford MB Feany E Masliah TT Rohn, Am J Pathol 2007 170 1725 1738 17456777 10.2353/ajpath.2007.061232
137. Calpain-resistant fragment(s) of alpha-synuclein regulates the synuclein-cleaving activity of 20S proteasome. HJ Kim D Lee CH Lee KC Chung J Kim SR Paik, Arch Biochem Biophys 2006 455 40 47 10.1016/j.abb.2006.08.019 17005155
138. Distinct cleavage patterns of normal and pathologic forms of alpha-synuclein by calpain I in vitro. AJ Mishizen-Eberz RP Guttmann BI Giasson GA Day 3rd R Hodara H Ischiropoulos VM Lee JQ Trojanowski DR Lynch, J Neurochem 2003 86 836 847 10.1046/j.1471-4159.2003.01878.x 12887682
139. Cleavage of alpha-synuclein by calpain: potential role in degradation of fibrillized and nitrated species of alpha-synuclein. AJ Mishizen-Eberz EH Norris BI Giasson R Hodara H Ischiropoulos VM Lee JQ Trojanowski DR Lynch, Biochemistry 2005 44 7818 7829 10.1021/bi047846q 15909996
140. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. R Cappai SL Leck DJ Tew NA Williamson DP Smith D Galatis RA Sharples CC Curtain FE Ali RA Cherny JG Culvenor SP Bottomley CL Masters KJ Barnham AF Hill, Faseb J 2005 19 1377 1379 15946991
141. Parkinson's disease genetic mutations increase cell susceptibility to stress: Mutant alpha-synuclein enhances H(2)O(2)- and Sin-1-induced cell death. H Jiang YC Wu M Nakamura Y Liang Y Tanaka S Holmes VL Dawson TM Dawson CA Ross WW Smith, Neurobiol Aging 2006
142. Overexpression of alpha-synuclein decreased viability and enhanced sensitivity to prostaglandin E(2), hydrogen peroxide, and a nitric oxide donor in differentiated neuroblastoma cells. JE Prasad B Kumar C Andreatta P Nahreini AJ Hanson XD Yan KN Prasad, J Neurosci Res 2004 76 415 422 10.1002/jnr.20058 15079871
143. Alpha-synuclein is upregulated in neurones in response to chronic oxidative stress and is associated with neuroprotection. MC Quilty AE King WP Gai DL Pountney AK West JC Vickers TC Dickson, Exp Neurol 2006 199 249 256 10.1016/j.expneurol.2005.10.018 16310772
144. Cell systems and the toxic mechanism(s) of alpha-synuclein. MR Cookson M van der Brug, Exp Neurol 2008 209 5 11 17603039 10.1016/j.expneurol.2007.05.022
145. The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. M Zhu J Li AL Fink, J Biol Chem 2003 278 40186 40197 10.1074/jbc.M305326200 12885775
146. Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. MJ Volles PT Lansbury Jr, Biochemistry 2002 41 4595 4602 10.1021/bi0121353 11926821
147. Annular alpha-synuclein species from purified multiple system atrophy inclusions. DL Pountney R Lowe M Quilty JC Vickers NH Voelcker WP Gai, J Neurochem 2004 90 502 512 10.1111/j.1471-4159.2004.02533.x 15228606
148. Plasma membrane ion permeability induced by mutant alpha-synuclein contributes to the degeneration of neural cells. K Furukawa M Matsuzaki-Kobayashi T Hasegawa A Kikuchi N Sugeno Y Itoyama Y Wang PJ Yao I Bushlin A Takeda, J Neurochem 2006 97 1071 1077 10.1111/j.1471-4159.2006.03803.x 16606366
149. Alpha-synuclein overexpression increases cytosolic catecholamine concentration. EV Mosharov RG Staal J Bove D Prou A Hananiya D Markov N Poulsen KE Larsen CM Moore MD Troyer RH Edwards S Przedborski D Sulzer, J Neurosci 2006 26 9304 9311 10.1523/JNEUROSCI.0519-06.2006 16957086
150. Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis. KE Larsen Y Schmitz MD Troyer E Mosharov P Dietrich AZ Quazi M Savalle V Nemani FA Chaudhry RH Edwards L Stefanis D Sulzer, J Neurosci 2006 26 11915 11922 10.1523/JNEUROSCI.3821-06.2006 17108165
151. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. AA Cooper AD Gitler A Cashikar CM Haynes KJ Hill B Bhullar K Liu K Xu KE Strathearn F Liu S Cao KA Caldwell GA Caldwell G Marsischky RD Kolodner J Labaer JC Rochet NM Bonini S Lindquist, Science 2006 313 324 328 16794039 10.1126/science.1129462
152. Golgi fragmentation occurs in the cells with prefibrillar alpha-synuclein aggregates and precedes the formation of fibrillar inclusion. N Gosavi HJ Lee JS Lee S Patel SJ Lee, J Biol Chem 2002 277 48984 48992 10.1074/jbc.M208194200 12351643
153. alpha-synuclein promotes mitochondrial deficit and oxidative stress. LJ Hsu Y Sagara A Arroyo E Rockenstein A Sisk M Mallory J Wong T Takenouchi M Hashimoto E Masliah, Am J Pathol 2000 157 401 410 10934145
154. Localization of alpha-synuclein to mitochondria within midbrain of mice. WW Li R Yang JC Guo HM Ren XL Zha JS Cheng DF Cai, Neuroreport 2007 18 1543 1546 17885598
155. Mitochondrial translocation of alpha-synuclein is promoted by intracellular acidification. NB Cole D Dieuliis P Leo DC Mitchell RL Nussbaum, Exp Cell Res 2008 314 2076 2089 10.1016/j.yexcr.2008.03.012 18440504
156. Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria. K Nakamura VM Nemani EK Wallender K Kaehlcke M Ott RH Edwards, J Neurosci 2008 28 12305 12317 10.1523/JNEUROSCI. 3088-08.2008 19020024
157. Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. L Devi V Raghavendran BM Prabhu NG Avadhani HK Anandatheerthavarada, J Biol Chem 2008 283 9089 9100 10.1074/jbc.M710012200 18245082
158. Alpha-synuclein expression in HEK293 cells enhances the mitochondrial sensitivity to rotenone. M Orth SJ Tabrizi AH Schapira JM Cooper, Neurosci Lett 2003 351 29 32 10.1016/S0304-3940(03)00941-8 14550906
159. Induction of neuronal death by alpha-synuclein. AR Saha NN Ninkina DP Hanger BH Anderton AM Davies VL Buchman, Eur J Neurosci 2000 12 3073 3077 10.1046/j.1460-9568.2000.00210.x 10971650
160. Glial cell death induced by overexpression of alpha-synuclein. N Stefanova L Klimaschewski W Poewe GK Wenning M Reindl, J Neurosci Res 2001 65 432 438 10.1002/jnr.1171 11536327
161. Alpha-synuclein induces apoptosis by altered expression in human peripheral lymphocyte in Parkinson's disease. S Kim BS Jeon C Heo PS Im TB Ahn JH Seo HS Kim CH Park SH Choi SH Cho WJ Lee YH Suh, Faseb J 2004 18 1615 1617 10.1096/fj.03-1391com 15289452
162. Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. LJ Martin Y Pan AC Price W Sterling NG Copeland NA Jenkins DL Price MK Lee, J Neurosci 2006 26 41 50 10.1523/JNEUROSCI.4308-05.2006 16399671
163. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. L Stefanis KE Larsen HJ Rideout D Sulzer LA Greene, J Neurosci 2001 21 9549 9560 11739566
164. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Q Yang H She M Gearing E Colla M Lee JJ Shacka Z Mao, Science 2009 323 124 127 10.1126/science.1166088 19119233
165. Aggregated and monomeric alpha-synuclein bind to the S6' proteasomal protein and inhibit proteasomal function. H Snyder K Mensah C Theisler J Lee A Matouschek B Wolozin, J Biol Chem 2003 278 11753 11759 10.1074/jbc.M208641200 12551928
166. Proteasomal inhibition by alpha-synuclein filaments and oligomers. E Lindersson R Beedholm P Hojrup T Moos W Gai KB Hendil PH Jensen, J Biol Chem 2004 279 12924 12934 10.1074/jbc.M306390200 14711827
167. Cell-produced alpha-synuclein oligomers are targeted to, and impair, the 26S proteasome. E Emmanouilidou L Stefanis K Vekrellis, Neurobiol Aging 2008 18715677
168. Proteasome dysfunction in aged human alpha-synuclein transgenic mice. L Chen MJ Thiruchelvam K Madura EK Richfield, Neurobiol Dis 2006 23 120 126 10.1016/j.nbd.2006.02.004 16713278
169. Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein. NB Cole DD Murphy T Grider S Rueter D Brasaemle RL Nussbaum, J Biol Chem 2002 277 6344 6352 10.1074/jbc.M108414200 11744721
170. Trehalose, a Novel mTOR-independent Autophagy Enhancer, Accelerates the Clearance of Mutant Huntingtin and {alpha}-Synuclein. S Sarkar JE Davies Z Huang A Tunnacliffe DC Rubinsztein, J Biol Chem 2007 282 5641 5652 10.1074/jbc.M609532200 17182613
171. Silencing of human alpha-synuclein in vitro and in rat brain using lentiviral-mediated RNAi. MK Sapru JW Yates S Hogan L Jiang J Halter MC Bohn, Exp Neurol 2006 198 382 390 10.1016/j.expneurol.2005.12.024 16455076
172. In vivo silencing of alpha-synuclein using naked siRNA. J Lewis H Melrose D Bumcrot A Hope C Zehr S Lincoln A Braithwaite Z He S Ogholikhan K Hinkle C Kent I Toudjarska K Charisse R Braich RK Pandey M Heckman DM Maraganore J Crook MJ Farrer, Mol Neurodegener 2008 3 19 18976489 10.1186/1750-1326-3-19
173. The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. AD Gitler BJ Bevis J Shorter KE Strathearn S Hamamichi LJ Su KA Caldwell GA Caldwell JC Rochet JM McCaffery C Barlowe S Lindquist, Proc Natl Acad Sci USA 2008 105 145 150 18162536 10.1073/pnas.0710685105