The role of transcriptional control in multiple system atrophy

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 394-400

  Chen, Jieqiong ^a   Mills, James D ^a   Halliday, Glenda M ^a,b   Janitz, Michael ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

Author keywords

Gene regulation; Multiple system atrophy; Neurodegenerative diseases; Transcriptome; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; COENZYME Q2; LONG UNTRANSLATED RNA; MICRORNA; TRANSCRIPTOME; UBIDECARENONE; UBIQUINONE; UNCLASSIFIED DRUG; MESSENGER RNA; UNTRANSLATED RNA;

ALPHA SYNUCLEINOPATHY; ALTERNATIVE RNA SPLICING; DEGENERATIVE DISEASE; FAMILIAL DISEASE; GENE EXPRESSION; GENE MUTATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; GLIA CELL; HUMAN; MOLECULAR PATHOLOGY; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; REVIEW; SHY DRAGER SYNDROME; BRAIN; GENETICS; METABOLISM; PATHOLOGY;

ALPHA-SYNUCLEIN; BRAIN; GENE EXPRESSION; HUMANS; MULTIPLE SYSTEM ATROPHY; OLIGODENDROGLIA; RNA, MESSENGER; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 84920597030     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.08.015     Document Type: Review

References (106)

1. Ahtiainen L., Kolikova J., Mutka A.L., Luiro K., Gentile M., Ikonen E., Khiroug L., Jalanko A., Kopra O. Palmitoyl protein thioesterase 1 (Ppt1)-deficient mouse neurons show alterations in cholesterol metabolism and calcium homeostasis prior to synaptic dysfunction. Neurobiol. Dis. 2007, 28:52-64.
2. Asi Y.T., Simpson J.E., Heath P.R., Wharton S.B., Lees A.J., Revesz T., Houlden H., Holton J.L. Alpha-synuclein mRNA expression in oligodendrocytes in MSA. Glia 2014, 62:964-970.
3. Bartels T., Choi J.G., Selkoe D.J. alpha-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 2011, 477:107-110.
4. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005, 58:495-505.
5. Beyer K. Alpha-synuclein structure, posttranslational modification and alternative splicing as aggregation enhancers. Acta Neuropathol. 2006, 112:237-251.
6. Beyer K., Ariza A. alpha-Synuclein posttranslational modification and alternative splicing as a trigger for neurodegeneration. Mol. Neurobiol. 2013, 47:509-524.
7. Beyer K., Domingo-Sabat M., Humbert J., Carrato C., Ferrer I., Ariza A. Differential expression of alpha-synuclein, parkin, and synphilin-1 isoforms in Lewy body disease. Neurogenetics 2008, 9:163-172.
8. Bisaglia M., Mammi S., Bubacco L. Structural insights on physiological functions and pathological effects of alpha-synuclein. FASEB J. 2009, 23:329-340.
9. Bleasel J.M., Wong J.H., Halliday G.M., Kim W.S. Lipid dysfunction and pathogenesis of multiple system atrophy. Acta Neuropathol. Commun. 2014, 2:15.
10. Braak H., Sastre M., Del Tredici K. Development of alpha-synuclein immunoreactive astrocytes in the forebrain parallels stages of intraneuronal pathology in sporadic Parkinson's disease. Acta Neuropathol. 2007, 114:231-241.
11. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., Thompson W.J., Barres B.A. Atranscriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J.Neurosci. 2008, 28:264-278.
12. Campion D., Martin C., Heilig R., Charbonnier F., Moreau V., Flaman J.M., Petit J.L., Hannequin D., Brice A., Frebourg T. The NACP/synuclein gene: chromosomal assignment and screening for alterations in Alzheimer disease. Genomics 1995, 26:254-257.
13. Castagnet P.I., Golovko M.Y., Barcelo-Coblijn G.C., Nussbaum R.L., Murphy E.J. Fatty acid incorporation is decreased in astrocytes cultured from alpha-synuclein gene-ablated mice. J.Neurochem. 2005, 94:839-849.
14. Chiba M., Kiyosawa H., Hiraiwa N., Ohkohchi N., Yasue H. Existence of Pink1 antisense RNAs in mouse and their localization. Cytogenet. Genome Res. 2009, 126:259-270.
15. Cho M.K., Nodet G., Kim H.Y., Jensen M.R., Bernado P., Fernandez C.O., Becker S., Blackledge M., Zweckstetter M. Structural characterization of alpha-synuclein in an aggregation prone state. Protein Sci. 2009, 18:1840-1846.
16. Clayton D.F., George J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J.Neurosci. Res. 1999, 58:120-129.
17. Dean J.M., Wang X., Kaindl A.M., Gressens P., Fleiss B., Hagberg H., Mallard C. Microglial MyD88 signaling regulates acute neuronal toxicity of LPS-stimulated microglia invitro. Brain Behav. Immun. 2010, 24:776-783.
18. Deshpande M., Zheng J., Borgmann K., Persidsky R., Wu L., Schellpeper C., Ghorpade A. Role of activated astrocytes in neuronal damage: potential links to HIV-1-associated dementia. Neurotox. Res. 2005, 7:183-192.
19. Dickson D.W., Lin W., Liu W.K., Yen S.H. Multiple system atrophy: a sporadic synucleinopathy. Brain Pathol. 1999, 9:721-732.
20. Donadio V., Cortelli P., Elam M., Di Stasi V., Montagna P., Holmberg B., Giannoccaro M.P., Bugiardini E., Avoni P., Baruzzi A., Liguori R. Autonomic innervation in multiple system atrophy and pure autonomic failure. J.Neurol. Neurosurg. Psychiatry 2010, 81:1327-1335.
21. Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12:861-874.
22. Faghihi M.A., Modarresi F., Khalil A.M., Wood D.E., Sahagan B.G., Morgan T.E., Finch C.E., St Laurent G., Kenny P.J., Wahlestedt C. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat. Med. 2008, 14:723-730.
23. Fellner L., Jellinger K.A., Wenning G.K., Stefanova N. Glial dysfunction in the pathogenesis of alpha-synucleinopathies: emerging concepts. Acta Neuropathol. 2011, 121:675-693.
24. Fellner L., Stefanova N. The role of glia in alpha-synucleinopathies. Mol. Neurobiol. 2013, 47:575-586.
25. Ferrante K.L., Shefner J., Zhang H., Betensky R., O'Brien M., Yu H., Fantasia M., Taft J., Beal M.F., Traynor B., Newhall K., Donofrio P., Caress J., Ashburn C., Freiberg B., O'Neill C., Paladenech C., Walker T., Pestronk A., Abrams B., Florence J., Renna R., Schierbecker J., Malkus B., Cudkowicz M. Tolerance of high-dose (3,000 mg/day) coenzyme Q10 in ALS. Neurology 2005, 65:1834-1836.
26. Ferrer I. [Alpha-synucleinopathies]. Neurologia 2001, 16:163-170.
27. Frisardi V., Solfrizzi V., Imbimbo P.B., Capurso C., D'Introno A., Colacicco A.M., Vendemiale G., Seripa D., Pilotto A., Capurso A., Panza F. Towards disease-modifying treatment of Alzheimer's disease: drugs targeting beta-amyloid. Curr. Alzheimer Res. 2010, 7:40-55.
28. Fujiwara H., Hasegawa M., Dohmae N., Kawashima A., Masliah E., Goldberg M.S., Shen J., Takio K., Iwatsubo T. alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat. Cell. Biol. 2002, 4:160-164.
29. Gai W.P., Power J.H., Blumbergs P.C., Blessing W.W. Multiple-system atrophy: a new alpha-synuclein disease?. Lancet 1998, 352:547-548.
30. Gawel M., Jamrozik Z., Szmidt-Salkowska E., Slawek J., Rowinska-Marcinska K. Is peripheral neuron degeneration involved in multiple system atrophy? A clinical and electrophysiological study. J.Neurol. Sci. 2012, 319:81-85.
31. Gilman S., Wenning G.K., Low P.A., Brooks D.J., Mathias C.J., Trojanowski J.Q., Wood N.W., Colosimo C., Durr A., Fowler C.J., Kaufmann H., Klockgether T., Lees A., Poewe W., Quinn N., Revesz T., Robertson D., Sandroni P., Seppi K., Vidailhet M. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 2008, 71:670-676.
32. Golovko M.Y., Faergeman N.J., Cole N.B., Castagnet P.I., Nussbaum R.L., Murphy E.J. Alpha-synuclein gene deletion decreases brain palmitate uptake and alters the palmitate metabolism in the absence of alpha-synuclein palmitate binding. Biochemistry 2005, 44:8251-8259.
33. Halliday G.M., Holton J.L., Revesz T., Dickson D.W. Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol. 2011, 122:187-204.
34. Halliday G.M., Stevens C.H. Glia: initiators and progressors of pathology in Parkinson's disease. Mov. Disord. 2011, 26:6-17.
35. Hyson H.C., Kieburtz K., Shoulson I., McDermott M., Ravina B., de Blieck E.A., Cudkowicz M.E., Ferrante R.J., Como P., Frank S., Zimmerman C., Cudkowicz M.E., Ferrante K., Newhall K., Jennings D., Kelsey T., Walker F., Hunt V., Daigneault S., Goldstein M., Weber J., Watts A., Beal M.F., Browne S.E., Metakis L.J. Safety and tolerability of high-dosage coenzyme Q10 in Huntington's disease and healthy subjects. Mov. Disord. 2010, 25:1924-1928. Huntington Study Group Pre2CARE Investigators.
36. Ide C.F., Scripter J.L., Coltman B.W., Dotson R.S., Snyder D.C., Jelaso A. Cellular and molecular correlates to plasticity during recovery from injury in the developing mammalian brain. Prog. Brain Res. 1996, 108:365-377.
37. Ischiropoulos H., Beckman J.S. Oxidative stress and nitration in neurodegeneration: cause, effect, or association?. J.Clin. Invest. 2003, 111:163-169.
38. Ishizawa K., Komori T., Sasaki S., Arai N., Mizutani T., Hirose T. Microglial activation parallels system degeneration in multiple system atrophy. J.Neuropathol. Exp. Neurol. 2004, 63:43-52.
39. Jellinger K.A. Neuropathological spectrum of synucleinopathies. Mov. Disord. 2003, 18(Suppl 6):S2-S12.
40. Jin H., Ishikawa K., Tsunemi T., Ishiguro T., Amino T., Mizusawa H. Analyses of copy number and mRNA expression level of the alpha-synuclein gene in multiple system atrophy. J.Med. Dent. Sci. 2008, 55:145-153.
41. Kalivendi S.V., Yedlapudi D., Hillard C.J., Kalyanaraman B. Oxidants induce alternative splicing of alpha-synuclein: Implications for Parkinson's disease. Free Radic. Biol. Med. 2010, 48:377-383.
42. Kawai Y., Suenaga M., Takeda A., Ito M., Watanabe H., Tanaka F., Kato K., Fukatsu H., Naganawa S., Kato T., Ito K., Sobue G. Cognitive impairments in multiple system atrophy: MSA-C vs MSA-P. Neurology 2008, 70(16 Pt 2):1390-1396.
43. Keller J.N., Hanni K.B., Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J.Neurochem. 2000, 75:436-439.
44. Kiely A.P., Asi Y.T., Kara E., Limousin P., Ling H., Lewis P., Proukakis C., Quinn N., Lees A.J., Hardy J., Revesz T., Houlden H., Holton J.L. alpha-Synucleinopathy associated with G51D SNCA mutation: a link between Parkinson's disease and multiple system atrophy?. Acta Neuropathol. 2013, 125:753-769.
45. Kohler W. Leukodystrophies with late disease onset: an update. Curr. Opin. Neurol. 2010, 23:234-241.
46. Kosaka K. Lewy bodies in cerebral cortex, report of three cases. Acta Neuropathol. 1978, 42:127-134.
47. Langerveld A.J., Mihalko D., DeLong C., Walburn J., Ide C.F. Gene expression changes in postmortem tissue from the rostral pons of multiple system atrophy patients. Mov. Disord. 2007, 22:766-777.
48. Lavedan C. The synuclein family. Genome Res. 1998, 8:871-880.
49. Lee H.J., Choi C., Lee S.J. Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J.Biol. Chem. 2002, 277:671-678.
50. Lesage S., Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum. Mol. Genet. 2009, 18(R1):R48-R59.
51. Li J., Uversky V.N., Fink A.L. Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry 2001, 40:11604-11613.
52. Lin S.T., Fu Y.H. miR-23 regulation of lamin B1 is crucial for oligodendrocyte development and myelination. Dis. Model Mech. 2009, 2:178-188.
53. Lin S.T., Huang Y., Zhang L., Heng M.Y., Ptacek L.J., Fu Y.H. MicroRNA-23a promotes myelination in the central nervous system. Proc. Natl. Acad. Sci. U.S.A 2013, 110:17468-17473.
54. Lu C.F., Soong B.W., Wu H.M., Teng S., Wang P.S., Wu Y.T. Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy. Mov. Disord. 2013, 28:362-369.
55. Ma K.L., Song L.K., Long W.A., Yuan Y.H., Zhang Y., Song X.Y., Niu F., Han N., Chen N.H. Deletion in exon 5 of the SNCA gene and exposure to rotenone leads to oligomerization of alpha-synuclein and toxicity to PC12 cells. Brain Res. Bull. 2013, 90:127-131.
56. Matsuo A., Akiguchi I., Lee G.C., McGeer E.G., McGeer P.L., Kimura J. Myelin degeneration in multiple system atrophy detected by unique antibodies. Am. J. Pathol. 1998, 153:735-744.
57. Mattick J.S. The central role of RNA in human development and cognition. FEBS Lett. 2011, 585:1600-1616.
58. May V.E., Ettle B., Poehler A.M., Nuber S., Ubhi K., Rockenstein E., Winner B., Wegner M., Masliah E., Winkler J. alpha-Synuclein impairs oligodendrocyte progenitor maturation in multiple system atrophy. Neurobiol. Aging 2014, 35:2357-2368.
59. McLean P.J., Kawamata H., Ribich S., Hyman B.T. Membrane association and protein conformation of alpha-synuclein in intact neurons. Effect of Parkinson's disease-linked mutations. J.Biol. Chem. 2000, 275:8812-8816.
60. McNaught K.S., Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci. Lett. 2001, 297:191-194.
61. Mercer T.R., Dinger M.E., Mattick J.S. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 2009, 10:155-159.
62. Miller D.W., Johnson J.M., Solano S.M., Hollingsworth Z.R., Standaert D.G., Young A.B. Absence of alpha-synuclein mRNA expression in normal and multiple system atrophy oligodendroglia. J.Neural Transm. 2005, 112:1613-1624.
63. Mills J.D., Janitz M. Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol. Aging 2012, 33:1012.e11-1012.e24.
64. Mills J.D., Kavanagh T., Kim W.S., Chen B.J., Kawahara Y., Halliday G.M., Janitz M. Unique transcriptome patterns of the white and grey matter corroborate structural and functional heterogeneity in the human frontal lobe. PLoS One 2013, 8:e78480.
65. Minnerop M., Luders E., Specht K., Ruhlmann J., Schimke N., Thompson P.M., Chou Y.Y., Toga A.W., Abele M., Wullner U., Klockgether T. Callosal tissue loss in multiple system atrophy-a one-year follow-up study. Mov. Disord. 2010, 25:2613-2620.
66. Mirza B., Hadberg H., Thomsen P., Moos T. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 2000, 95:425-432.
67. Morais V.A., Verstreken P., Roethig A., Smet J., Snellinx A., Vanbrabant M., Haddad D., Frezza C., Mandemakers W., Vogt-Weisenhorn D., Van Coster R., Wurst W., Scorrano L., De Strooper B. Parkinson's disease mutations in PINK1 result in decreased complex I activity and deficient synaptic function. EMBO Mol. Med. 2009, 1:99-111.
68. Mutations in COQ2 in familial and sporadic multiple-system atrophy. N.Engl. J. Med. 2013, 369:233-244. Multiple-System Atrophy Research Collaboration.
69. Murray I.V., Giasson B.I., Quinn S.M., Koppaka V., Axelsen P.H., Ischiropoulos H., Trojanowski J.Q., Lee V.M. Role of alpha-synuclein carboxy-terminus on fibril formation invitro. Biochemistry 2003, 42:8530-8540.
70. Nakayama K., Suzuki Y., Yazawa I. Microtubule depolymerization suppresses alpha-synuclein accumulation in a mouse model of multiple system atrophy. Am. J. Pathol. 2009, 174:1471-1480.
71. Nakayama K., Suzuki Y., Yazawa I. Binding of neuronal alpha-synuclein to beta-III tubulin and accumulation in a model of multiple system atrophy. Biochem. Biophys. Res. Commun. 2012, 417:1170-1175.
72. Nee L.E., Gomez M.R., Dambrosia J., Bale S., Eldridge R., Polinsky R.J. Environmental-occupational risk factors and familial associations in multiple system atrophy: a preliminary investigation. Clin. Auton. Res. 1991, 1:9-13.
73. Nicoletti G., Lodi R., Condino F., Tonon C., Fera F., Malucelli E., Manners D., Zappia M., Morgante L., Barone P., Barbiroli B., Quattrone A. Apparent diffusion coefficient measurements of the middle cerebellar peduncle differentiate the Parkinson variant of MSA from Parkinson's disease and progressive supranuclear palsy. Brain 2006, 129(Pt 10):2679-2687.
74. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma invivo. Science 2005, 308:1314-1318.
75. O'Sullivan S.S., Massey L.A., Williams D.R., Silveira-Moriyama L., Kempster P.A., Holton J.L., Revesz T., Lees A.J. Clinical outcomes of progressive supranuclear palsy and multiple system atrophy. Brain 2008, 131(Pt 5):1362-1372.
76. Ozawa T., Okuizumi K., Ikeuchi T., Wakabayashi K., Takahashi H., Tsuji S. Analysis of the expression level of alpha-synuclein mRNA using postmortem brain samples from pathologically confirmed cases of multiple system atrophy. Acta Neuropathol. 2001, 102:188-190.
77. Paik S.R., Lee J.H., Kim D.H., Chang C.S., Kim J. Aluminum-induced structural alterations of the precursor of the non-A beta component of Alzheimer's disease amyloid. Arch. Biochem. Biophys. 1997, 344:325-334.
78. Paik S.R., Shin H.J., Lee J.H., Chang C.S., Kim J. Copper(II)-induced self-oligomerization of alpha-synuclein. Biochem. J. 1999, 340(Pt 3):821-828.
79. Probst-Cousin S., Rickert C.H., Schmid K.W., Gullotta F. Cell death mechanisms in multiple system atrophy. J.Neuropathol. Exp. Neurol. 1998, 57(9):814-821.
80. Qureshi I.A., Mattick J.S., Mehler M.F. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010, 1338:20-35.
81. Sai Y., Zou Z., Peng K., Dong Z. The Parkinson's disease-related genes act in mitochondrial homeostasis. Neurosci. Biobehav. Rev. 2012, 36:2034-2043.
82. Sato K., Kaji R., Matsumoto S., Nagahiro S., Goto S. Compartmental loss of striatal medium spiny neurons in multiple system atrophy of parkinsonian type. Mov. Disord. 2007, 22:2365-2370.
83. Scheele C., Petrovic N., Faghihi M.A., Lassmann T., Fredriksson K., Rooyackers O., Wahlestedt C., Good L., Timmons J.A. The human PINK1 locus is regulated invivo by a non-coding natural antisense RNA during modulation of mitochondrial function. BMC Genomics 2007, 8:74.
84. Scherzer C.R., Jensen R.V., Gullans S.R., Feany M.B. Gene expression changes presage neurodegeneration in a drosophila model of Parkinson's disease. Hum. Mol. Genet. 2003, 12:2457-2466.
85. Serpell L.C., Berriman J., Jakes R., Goedert M., Crowther R.A. Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc. Natl. Acad. Sci. U.S.A 2000, 97:4897-4902.
86. Sharon R., Bar-Joseph I., Frosch M.P., Walsh D.M., Hamilton J.A., Selkoe D.J. The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron 2003, 37:583-595.
87. Shiga K., Yamada K., Yoshikawa K., Mizuno T., Nishimura T., Nakagawa M. Local tissue anisotropy decreases in cerebellopetal fibers and pyramidal tract in multiple system atrophy. J.Neurol. 2005, 252:589-596.
88. Souza J.M., Giasson B.I., Lee V.M., Ischiropoulos H. Chaperone-like activity of synucleins. FEBS Lett. 2000, 474:116-119.
89. Stefanis L. alpha-Synuclein in Parkinson's disease. Cold Spring Harb. Perspect. Med. 2012, 2:a009399.
90. Stefanova N., Reindl M., Neumann M., Haass C., Poewe W., Kahle P.J., Wenning G.K. Oxidative stress in transgenic mice with oligodendroglial alpha-synuclein overexpression replicates the characteristic neuropathology of multiple system atrophy. Am. J. Pathol. 2005, 166:869-876.
91. Tong J., Wong H., Guttman M., Ang L.C., Forno L.S., Shimadzu M., Rajput A.H., Muenter M.D., Kish S.J., Hornykiewicz O., Furukawa Y. Brain alpha-synuclein accumulation in multiple system atrophy, Parkinson's disease and progressive supranuclear palsy: a comparative investigation. Brain 2010, 133(Pt 1):172-188.
92. Ubhi K., Rockenstein E., Kragh C., Inglis C., Spencer B., Michael S., Mante M., Adame A., Galasko D., Masliah E. Widespread microRNA dysregulation in multiple system atrophy - disease-related alteration in miR-96. Eur. J. Neurosci. 2014, 39:1026-1041.
93. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., Otero D.A., Kondo J., Ihara Y., Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A 1993, 90:11282-11286.
94. Umoto M., Miwa H., Ando R., Kajimoto Y., Kondo T. White matter hyperintensities in patients with multiple system atrophy. Parkinsonism Relat. Disord. 2012, 18:17-20.
95. Uversky V.N. Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. J.Neurochem. 2007, 103:17-37.
96. Vanacore N., Bonifati V., Fabbrini G., Colosimo C., De Michele G., Marconi R., Nicholl D., Locuratolo N., Talarico G., Romano S., Stocchi F., Bonuccelli U., De Mari M., Vieregge P., Meco G. Epidemiology of multiple system atrophy. ESGAP consortium. European study group on atypical parkinsonisms. Neurol. Sci. 2001, 22:97-99. European Study Group on Atypical, P.
97. Vidal J.S., Vidailhet M., Derkinderen P., Tzourio C., Alperovitch A. Familial aggregation in atypical Parkinson's disease: a case control study in multiple system atrophy and progressive supranuclear palsy. J.Neurol. 2010, 257:1388-1393.
98. Vila M., Jackson-Lewis V., Guegan C., Wu D.C., Teismann P., Choi D.K., Tieu K., Przedborski S. The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 2001, 14:483-489.
99. Wakabayashi K., Hayashi S., Yoshimoto M., Kudo H., Takahashi H. NACP/alpha-synuclein-positive filamentous inclusions in astrocytes and oligodendrocytes of Parkinson's disease brains. Acta Neuropathol. 2000, 99:14-20.
100. Wakabayashi K., Takahashi H. Cellular pathology in multiple system atrophy. Neuropathology 2006, 26:338-345.
101. Watanabe H., Saito Y., Terao S., Ando T., Kachi T., Mukai E., Aiba I., Abe Y., Tamakoshi A., Doyu M., Hirayama M., Sobue G. Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain 2002, 125(Pt 5):1070-1083.
102. Wenning G.K., Colosimo C., Geser F., Poewe W. Multiple system atrophy. Lancet Neurol. 2004, 3:93-103.
103. Wenning G.K., Wagner S., Daniel S., Quinn N.P. Multiple system atrophy: sporadic or familial?. Lancet 1993, 342:681.
104. Wilhelmsson U., Bushong E.A., Price D.L., Smarr B.L., Phung V., Terada M., Ellisman M.H., Pekny M. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc. Natl. Acad. Sci. U.S.A 2006, 103:17513-17518.
105. Zarranz J.J., Alegre J., Gomez-Esteban J.C., Lezcano E., Ros R., Ampuero I., Vidal L., Hoenicka J., Rodriguez O., Atares B., Llorens V., Gomez Tortosa E., del Ser T., Munoz D.G., de Yebenes J.G. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 2004, 55:164-173.
106. Zhang W., Wang T., Pei Z., Miller D.S., Wu X., Block M.L., Wilson B., Zhang W., Zhou Y., Hong J.S., Zhang J. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 2005, 19:533-542.