A53T-alpha-synuclein-overexpression in the mouse nigrostriatal pathway leads to early increase of 14-3-3 epsilon and late increase of GFAP

Journal of Neural Transmission

Volumn 119, Issue 3, 2012, Pages 297-312

  Kurz, Alexander ^a   May, Caroline ^b   Schmidt, Oliver ^b   Müller, Thorsten ^b   Stephan, Christian ^b   Meyer, Helmut E ^b   Gispert, Suzana ^a   Auburger, Georg ^a,b,c   Marcus, Katrin ^b  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

14 3 3 protein; A53T alpha synuclein overexpression; Striatal proteome; Transgenic mice

Indexed keywords

ALPHA SYNUCLEIN; CHAPERONE; CYTOSKELETON PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; PROTEIN 14 3 3; PROTEIN 14 3 3 EPSILON; PROTEOME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BIOENERGY; CORPUS STRIATUM; DOPAMINE METABOLISM; DOPAMINERGIC NERVE CELL; DOWN REGULATION; IMMUNOBLOTTING; LEWY BODY; MASS SPECTROMETRY; MESENCEPHALON; MOUSE; NERVE DEGENERATION; NERVE ENDING; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; STRESS; SYNAPSE VESICLE; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION;

14-3-3 PROTEINS; ALPHA-SYNUCLEIN; ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MICE, TRANSGENIC; PARKINSON DISEASE; SUBSTANTIA NIGRA;

EID: 84857637973     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-011-0717-3     Document Type: Article

References (69)

1. N Ahmed S Battah N Karachalias R Babaei-Jadidi M Horanyi K Baroti S Hollan PJ Thornalley 2003 Increased formation of methylglyoxal and protein glycation, oxidation and nitrosation in triosephosphate isomerase deficiency Biochim Biophys Acta 1639 121 132 14559119 1:CAS:528:DC%2BD3sXotVyltb8%3D (Pubitemid 38366216)
2. S Baumann U Ceglarek GM Fiedler J Lembcke A Leichtle J Thiery 2005 Standardized approach to proteome profiling of human serum based on magnetic bead separation and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry Clin Chem 51 973 980 15845803 10.1373/clinchem.2004.047308 1:CAS:528:DC%2BD2MXkvF2nsrs%3D (Pubitemid 40740877)
3. D Berg C Holzmann O Riess 2003 14-3-3 proteins in the nervous system Nat Rev Neurosci 4 752 762 12951567 10.1038/nrn1197 1:CAS:528:DC%2BD3sXmvVWksbw%3D (Pubitemid 37280154)
4. H Braak K Del Tredici U Rub RA de Vos EN Jansen Steur E Braak 2003 Staging of brain pathology related to sporadic Parkinson's disease Neurobiol Aging 24 197 211 12498954 10.1016/S0197-4580(02)00065-9 (Pubitemid 36007810)
5. R Bussell Jr D Eliezer 2003 A structural and functional role for 11-mer repeats in alpha-synuclein and other exchangeable lipid binding proteins J Mol Biol 329 763 778 12787676 10.1016/S0022-2836(03)00520-5 1:CAS:528: DC%2BD3sXkt1Gktr4%3D (Pubitemid 36629369)
6. C Butor S Diaz A Varki 1993 High level O-acetylation of sialic acids on N-linked oligosaccharides of rat liver membranes. Differential subcellular distribution of 7- and 9-O-acetyl groups and of enzymes involved in their regulation J Biol Chem 268 10197 10206 8486687 1:CAS:528:DyaK3sXkt1eit78%3D (Pubitemid 23150200)
7. DE Cabin S Gispert-Sanchez D Murphy G Auburger RR Myers RL Nussbaum 2005 Exacerbated synucleinopathy in mice expressing A53T SNCA on a Snca null background Neurobiol Aging 26 25 35 15585343 10.1016/j.neurobiolaging.2004.02. 026 1:CAS:528:DC%2BD2cXhtVCltbzP (Pubitemid 39600588)
8. DC Chamrad G Koerting J Gobom H Thiele J Klose HE Meyer M Blueggel 2003 Interpretation of mass spectrometry data for high-throughput proteomics Anal Bioanal Chem 376 1014 1022 12845399 10.1007/s00216-003-1995-x 1:CAS:528:DC%2BD3sXmtVGrsrs%3D (Pubitemid 40877918)
9. S Chandra F Fornai HB Kwon U Yazdani D Atasoy X Liu RE Hammer G Battaglia DC German PE Castillo TC Sudhof 2004 Double-knockout mice for alpha- and beta-synucleins: effect on synaptic functions Proc Natl Acad Sci USA 101 14966 14971 15465911 10.1073/pnas.0406283101 1:CAS:528:DC%2BD2cXovVyisLw%3D (Pubitemid 39410782)
10. S Chandra G Gallardo R Fernandez-Chacon OM Schluter TC Sudhof 2005 Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration Cell 123 383 396 16269331 10.1016/j.cell.2005.09.028 1:CAS:528:DC%2BD2MXht1altLnN (Pubitemid 41546670)
11. DF Clayton JM George 1998 The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease Trends Neurosci 21 249 254 9641537 10.1016/S0166-2236(97)01213-7 1:CAS:528:DyaK1cXjs1Kms78%3D (Pubitemid 28239982)
12. KA Conway JD Harper PT Lansbury 1998 Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease Nat Med 4 1318 1320 9809558 10.1038/3311 1:CAS:528:DyaK1cXntlakur0%3D (Pubitemid 28512115)
13. DC Crowther 2002 Familial conformational diseases and dementias Hum Mutat 20 1 14 12112652 10.1002/humu.10100 1:CAS:528:DC%2BD38XlslKrtrw%3D (Pubitemid 34747711)
14. N Dzamko M Deak F Hentati AD Reith AR Prescott DR Alessi RJ Nichols 2010 Inhibition of LRRK2 kinase activity leads to dephosphorylation of Ser(910)/Ser(935), disruption of 14-3-3 binding and altered cytoplasmic localization Biochem J 430 405 413 20659021 10.1042/BJ20100784 1:CAS:528:DC%2BC3cXhtVyrtbzL
15. JM Eng AL McCornack JR Yates 3rd 1994 An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database J Am Soc Mass Spectrom 5 976 989 10.1016/1044-0305(94)80016-2 1:CAS:528:DyaK2MXhvF2htLw%3D
16. S Fahn 2003 Description of Parkinson's disease as a clinical syndrome Ann N Y Acad Sci 991 1 14 12846969 10.1111/j.1749-6632.2003.tb07458.x 1:CAS:528:DC%2BD3sXmtVCkur4%3D (Pubitemid 36793796)
17. SM Ferguson G Brasnjo M Hayashi M Wolfel C Collesi S Giovedi A Raimondi LW Gong P Ariel S Paradise E O'Toole R Flavell O Cremona G Miesenbock TA Ryan P De Camilli 2007 A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis Science 316 570 574 17463283 10.1126/science. 1140621 1:CAS:528:DC%2BD2sXksFeksbc%3D (Pubitemid 46683137)
18. P Garcia-Reitbock O Anichtchik A Bellucci M Iovino C Ballini E Fineberg B Ghetti L Della Corte P Spano GK Tofaris M Goedert MG Spillantini 2010 SNARE protein redistribution and synaptic failure in a transgenic mouse model of Parkinson's disease Brain 133 2032 2044 20534649 10.1093/brain/awq132
19. T Gasser 2001 Genetics of Parkinson's disease J Neurol 248 833 840 11697518 10.1007/s004150170066 1:CAS:528:DC%2BD3MXosFSis78%3D (Pubitemid 32955666)
20. F Gillardon M Mack W Rist C Schnack M Lenter T Hildebrandt B Hengerer 2008 MicroRNA and proteome expression profiling in early-symptomatic alpha-synuclein (A30P)-transgenic mice Proteomics 2 697 705 21136867 10.1002/prca.200780025 1:CAS:528:DC%2BD1cXms1emtbw%3D (Pubitemid 351772025)
21. S Gispert D Del Turco L Garrett A Chen DJ Bernard J Hamm-Clement HW Korf T Deller H Braak G Auburger RL Nussbaum 2003 Transgenic mice expressing mutant A53T human alpha-synuclein show neuronal dysfunction in the absence of aggregate formation Mol Cell Neurosci 24 419 429 14572463 10.1016/S1044-7431(03)00198-2 1:CAS:528:DC%2BD3sXot1Grs7s%3D (Pubitemid 37311305)
22. Y Huang L Cheung D Rowe G Halliday 2004 Genetic contributions to Parkinson's disease Brain Res Brain Res Rev 46 44 70 15297154 10.1016/j.brainresrev.2004.04.007 1:CAS:528:DC%2BD2cXmsVGit7k%3D (Pubitemid 39030771)
23. T Ichibangase H Saimaru N Takamura T Kuwahara A Koyama T Iwatsubo K Imai 2008 Proteomics of Caenorhabditis elegans over-expressing human alpha-synuclein analyzed by fluorogenic derivatization-liquid chromatography/tandem mass spectrometry: identification of actin and several ribosomal proteins as negative markers at early Parkinson's disease stages Biomed Chromatogr 22 232 234 17939164 10.1002/bmc.931 1:CAS:528:DC%2BD1cXktVertrg%3D (Pubitemid 351459935)
24. 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 2001 Selective insolubility of alpha-synuclein in human Lewy body diseases is recapitulated in a transgenic mouse model Am J Pathol 159 2215 2225 11733371 10.1016/S0002-9440(10)63072-6 1:CAS:528:DC%2BD38Xhslejsw%3D%3D (Pubitemid 33104275)
25. NA Karp PS McCormick MR Russell KS Lilley 2007 Experimental and statistical considerations to avoid false conclusions in proteomics studies using differential in-gel electrophoresis Mol Cell Proteom 6 1354 1364 10.1074/mcp.M600274-MCP200 1:CAS:528:DC%2BD2sXps1aktr0%3D (Pubitemid 47365434)
26. JC Kessler JC Rochet PT Lansbury Jr 2003 The N-terminal repeat domain of alpha-synuclein inhibits beta-sheet and amyloid fibril formation Biochemistry 42 672 678 12534279 10.1021/bi020429y 1:CAS:528:DC%2BD38XpslOns7g%3D (Pubitemid 36133291)
27. J Klose U Kobalz 1995 Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome Electrophoresis 16 1034 1059 7498127 10.1002/elps.11501601175 1:CAS:528:DyaK2MXmslKmurg%3D
28. A Kurz KL Double I Lastres-Becker A Tozzi M Tantucci V Bockhart M Bonin M García-Arencibia S Nuber F Schlaudraff B Liss J Fernández-Ruiz M Gerlach U Wüllner H Lüddens P Calabresi G Auburger S Gispert 2010 A53T-alpha-synuclein overexpression impairs dopamine signaling and striatal synaptic plasticity in old mice PLoS ONE 5 e11464 20628651 10.1371/journal.pone. 0011464
29. E Leroy R Boyer G Auburger B Leube G Ulm E Mezey G Harta MJ Brownstein S Jonnalagada T Chernova A Dehejia C Lavedan T Gasser PJ Steinbach KD Wilkinson MH Polymeropoulos 1998 The ubiquitin pathway in Parkinson's disease Nature 395 451 452 9774100 10.1038/26652 1:CAS:528:DyaK1cXms1antLo%3D (Pubitemid 28462431)
30. V Licker E Kovari DF Hochstrasser PR Burkhard 2009 Proteomics in human Parkinson's disease research J Proteom 73 10 29 10.1016/j.jprot.2009.07.007 1:CAS:528:DC%2BD1MXhtlWitrjP
31. KJ Livak TD Schmittgen 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 402 408 11846609 10.1006/meth.2001.1262 1:CAS:528:DC%2BD38XhtFelt7s%3D (Pubitemid 34164012)
32. E Maries B Dass TJ Collier JH Kordower K Steece-Collier 2003 The role of alpha-synuclein in Parkinson's disease: insights from animal models Nat Rev Neurosci 4 727 738 12951565 10.1038/nrn1199 1:CAS:528:DC%2BD3sXmvVWksbg%3D (Pubitemid 37280152)
33. H Martin J Rostas Y Patel A Aitken 1994 Subcellular localisation of 14-3-3 isoforms in rat brain using specific antibodies J Neurochem 63 2259 2265 7964746 10.1046/j.1471-4159.1994.63062259.x 1:CAS:528:DyaK2MXit12ku7Y%3D (Pubitemid 24370003)
34. L Narhi SJ Wood S Steavenson Y Jiang GM Wu D Anafi SA Kaufman F Martin K Sitney P Denis JC Louis J Wypych AL Biere M Citron 1999 Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation J Biol Chem 274 9843 9846 10092675 10.1074/jbc.274.14.9843 1:CAS:528:DyaK1MXisVWks7o%3D (Pubitemid 29180308)
35. RJ Nichols N Dzamko NA Morrice DG Campbell M Deak A Ordureau T Macartney Y Tong J Shen AR Prescott DR Alessi 2010 14-3-3 binding to LRRK2 is disrupted by multiple Parkinson's disease-associated mutations and regulates cytoplasmic localization Biochem J 430 393 404 20642453 10.1042/BJ20100483 1:CAS:528:DC%2BC3cXhtVyrtbzK
36. CW Olanow KS McNaught 2006 Ubiquitin-proteasome system and Parkinson's disease Mov Disord 21 1806 1823 16972273 10.1002/mds.21013 (Pubitemid 44856478)
37. N Ostrerova L Petrucelli M Farrer N Mehta P Choi J Hardy B Wolozin 1999 alpha-Synuclein shares physical and functional homology with 14-3-3 proteins J Neurosci 19 5782 5791 10407019 1:CAS:528:DyaK1MXksVyktL4%3D (Pubitemid 29327915)
38. JJ Palacino D Sagi MS Goldberg S Krauss C Motz M Wacker J Klose J Shen 2004 Mitochondrial dysfunction and oxidative damage in parkin-deficient mice J Biol Chem 279 18614 18622 14985362 10.1074/jbc.M401135200 1:CAS:528: DC%2BD2cXjsVKmsrc%3D (Pubitemid 38623283)
39. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates., Second edn. Academic Press, San Diego
40. K Pennington J Peng CC Hung RE Banks PA Robinson 2010 Differential effects of wild-type and A53T mutant isoform of alpha-synuclein on the mitochondrial proteome of differentiated SH-SY5Y cells J Proteom Res 9 2390 2401 10.1021/pr901102d 1:CAS:528:DC%2BC3cXkvVKqs7g%3D
41. RG Perez JC Waymire E Lin JJ Liu F Guo MJ Zigmond 2002 A role for alpha-synuclein in the regulation of dopamine biosynthesis J Neurosci 22 3090 3099 11943812 1:CAS:528:DC%2BD38XjtF2htrg%3D (Pubitemid 35379198)
42. DN Perkins DJ Pappin DM Creasy JS Cottrell 1999 Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 20 3551 3567 10612281 10.1002/(SICI)1522-2683(19991201)20: 18<3551::AID-ELPS3551>3.0.CO;2-2 1:CAS:528:DC%2BD3cXhtF2ntw%3D%3D (Pubitemid 30007252)
43. BT Poll-The J Aicardi R Girot R Rosa 1985 Neurological findings in triosephosphate isomerase deficiency Ann Neurol 17 439 443 4004168 10.1002/ana.410170504 1:STN:280:DyaL2M3itl2gug%3D%3D (Pubitemid 15019981)
44. 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 1997 Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 2045 2047 9197268 10.1126/science.276.5321.2045 1:CAS:528:DyaK2sXkt1altr4%3D (Pubitemid 27443610)
45. HF Poon M Frasier N Shreve V Calabrese B Wolozin DA Butterfield 2005 Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice-a model of familial Parkinson's disease Neurobiol Dis 18 492 498 15755676 10.1016/j.nbd.2004.12.009 1:CAS:528: DC%2BD2MXhvFynsrg%3D (Pubitemid 40332708)
46. AD Reynolds DK Stone RL Mosley HE Gendelman 2009 Proteomic studies of nitrated alpha-synuclein microglia regulation by CD4+ CD25+ T cells J Proteome Res 8 3497 3511 19432400 10.1021/pr9001614 1:CAS:528:DC%2BD1MXms1egu7Y%3D
47. IN Rudenko MR Cookson 2010 14-3-3 proteins are promising LRRK2 interactors Biochem J 430 e5 e6 20795948 10.1042/BJ20101200 1:CAS:528: DC%2BC3cXhtVyrtbrN
48. H Schaefer K Marcus A Sickmann M Herrmann J Klose HE Meyer 2003 Identification of phosphorylation and acetylation sites in alphaA-crystallin of the eye lens (mus musculus) after two-dimensional gel electrophoresis Anal Bioanal Chem 376 966 972 12856102 10.1007/s00216-003-1983-1 1:CAS:528: DC%2BD3sXmtVGrs74%3D (Pubitemid 40877914)
49. H Schaefer JP Chervet C Bunse C Joppich HE Meyer K Marcus 2004 A peptide preconcentration approach for nano-high-performance liquid chromatography to diminish memory effects Proteomics 4 2541 2544 15352228 10.1002/pmic.200300801 1:CAS:528:DC%2BD2cXns1Ors7s%3D (Pubitemid 39202155)
50. H Schaefer DC Chamrad M Herrmann J Stuwe G Becker J Klose M Blueggel HE Meyer K Marcus 2006 Study of posttranslational modifications in lenticular alphaA-Crystallin of mice using proteomic analysis techniques Biochim Biophys Acta 1764 1948 1962 17157567 1:CAS:528:DC%2BD28XhtlaltL3O (Pubitemid 44895030)
51. AH Schapira E Tolosa 2010 Molecular and clinical prodrome of Parkinson disease: implications for treatment Nat Rev Neurol 6 309 317 20479780 10.1038/nrneurol.2010.52 1:CAS:528:DC%2BC3cXntFSntbg%3D
52. R Setsuie K Wada 2007 The functions of UCH-L1 and its relation to neurodegenerative diseases Neurochem Int 51 105 111 17586089 10.1016/j.neuint.2007.05.007 1:CAS:528:DC%2BD2sXosFOhur8%3D (Pubitemid 47179898)
53. Y Shirakashi Y Kawamoto H Tomimoto R Takahashi M Ihara 2006 alpha-Synuclein is colocalized with 14-3-3 and synphilin-1 in A53T transgenic mice Acta Neuropathol 112 681 689 16957925 10.1007/s00401-006-0132-2 1:CAS:528:DC%2BD28XhtFWlur%2FN (Pubitemid 44615029)
54. 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 2003 Alpha-synuclein locus triplication causes Parkinson's disease Science 302 841 14593171 10.1126/science.1090278 1:CAS:528:DC%2BD3sXoslehsbc%3D (Pubitemid 37339619)
55. B Sitek O Apostolov K Stuhler K Pfeiffer HE Meyer A Eggert A Schramm 2005 Identification of dynamic proteome changes upon ligand activation of Trk-receptors using two-dimensional fluorescence difference gel electrophoresis and mass spectrometry Mol Cell Proteom 4 291 299 10.1074/mcp.M400188-MCP200 1:CAS:528:DC%2BD2MXisFSmsrc%3D (Pubitemid 40439772)
56. MG Spillantini ML Schmidt VM Lee JQ Trojanowski R Jakes M Goedert 1997 Alpha-synuclein in Lewy bodies Nature 388 839 840 9278044 10.1038/42166 1:CAS:528:DyaK2sXlslWru7o%3D (Pubitemid 27377048)
57. C Stephan KA Reidegeld M Hamacher A van Hall K Marcus C Taylor P Jones M Muller R Apweiler L Martens G Korting DC Chamrad H Thiele M Bluggel D Parkinson PA Binz A Lyall HE Meyer 2006 Automated reprocessing pipeline for searching heterogeneous mass spectrometric data of the HUPO Brain Proteome Project pilot phase Proteomics 6 5015 5029 16927432 10.1002/pmic.200600294 1:CAS:528:DC%2BD28XhtVClurbI (Pubitemid 44483896)
58. K Stuhler K Pfeiffer C Joppich C Stephan K Jung M Muller O Schmidt A van Hall M Hamacher W Urfer HE Meyer K Marcus 2006 Pilot study of the Human Proteome Organisation Brain Proteome Project: applying different 2-DE techniques to monitor proteomic changes during murine brain development Proteomics 6 4899 4913 16927428 10.1002/pmic.200600089 (Pubitemid 44483887)
59. B Titz T Low E Komisopoulou SS Chen L Rubbi TG Graeber 2010 The proximal signaling network of the BCR-ABL1 oncogene shows a modular organization Oncogene 29 5895 5910 20697350 10.1038/onc.2010.331 1:CAS:528:DC%2BC3cXpvFelsr8%3D
60. MJ Volles PT Lansbury Jr 2003 Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's disease Biochemistry 42 7871 7878 12834338 10.1021/bi030086j 1:CAS:528: DC%2BD3sXktlWrtrg%3D (Pubitemid 36807703)
61. H Wiesinger B Hamprecht R Dringen 1997 Metabolic pathways for glucose in astrocytes Glia 21 22 34 9298844 10.1002/(SICI)1098-1136(199709)21:1<22::AID- GLIA3>3.0.CO;2-3 1:STN:280:DyaK2svkt1aqtw%3D%3D (Pubitemid 27389637)
62. J Xu SY Kao FJ Lee W Song LW Jin BA Yankner 2002 Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease Nat Med 8 600 606 12042811 10.1038/nm0602-600 1:CAS:528:DC%2BD38XktVyit7w%3D (Pubitemid 34633438)
63. Z Xun RA Sowell TC Kaufman DE Clemmer 2007 Lifetime proteomic profiling of an A30P alpha-synuclein Drosophila model of Parkinson's disease J Proteome Res 6 3729 3738 17683129 10.1021/pr0700504 1:CAS:528:DC%2BD2sXos1Klurk%3D (Pubitemid 47522761)
64. Z Xun RA Sowell TC Kaufman DE Clemmer 2007 Protein expression in a Drosophila model of Parkinson's disease J Proteome Res 6 348 357 17203978 10.1021/pr060488o 1:CAS:528:DC%2BD28XhtlCitbzO (Pubitemid 46173686)
65. Z Xun RA Sowell TC Kaufman DE Clemmer 2008 Quantitative proteomics of a presymptomatic A53T alpha-synuclein Drosophila model of Parkinson disease Mol Cell Proteom 7 1191 1203 10.1074/mcp.M700467-MCP200 1:CAS:528: DC%2BD1cXotlygtbY%3D (Pubitemid 352038266)
66. Yacoubian TA, Slone SR, Harrington AJ, Hamamichi S, Schieltz JM, Caldwell KA, Caldwell GA, Standaert DG (2011) Differential neuroprotective effects of 14-3-3 proteins in models of Parkinson's disease. Cell Death Dis 1
67. JR Yates 3rd JK Eng AL McCormack D Schieltz 1995 Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database Anal Chem 67 1426 1436 7741214 10.1021/ac00104a020 1:CAS:528: DyaK2MXksVymt7g%3D
68. W Zhang BT Chait 2000 ProFound: an expert system for protein identification using mass spectrometric peptide mapping information Anal Chem 72 2482 2489 10857624 10.1021/ac991363o 1:CAS:528:DC%2BD3cXivVGkurg%3D (Pubitemid 30395651)
69. Y Zhou G Gu DR Goodlett T Zhang C Pan TJ Montine KS Montine RH Aebersold J Zhang 2004 Analysis of alpha-synuclein-associated proteins by quantitative proteomics J Biol Chem 279 39155 39164 15234983 10.1074/jbc.M405456200 1:CAS:528:DC%2BD2cXnt1yjtrY%3D (Pubitemid 39296079)