Dopamine-induced α-synuclein oligomers show self- and cross-propagation properties

Protein Science

Volumn 23, Issue 10, 2014, Pages 1369-1379

  Planchard, Matthew S ^a   Exley, Sarah E ^b   Morgan, Sarah E ^b   Rangachari, Vijayaraghavan ^a  

^a University of Southern Mississippi   (United States)

^b University of Southern Mississippi   (United States)

Author keywords

amyloid; oligomers; Parkinson's; prion; propagation; synuclein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; DOPAMINE; DOPAMINE DERIVED ALPHA SYNYCLEIN OLIGOMER; MONOMER; OLIGOMER; UNCLASSIFIED DRUG; PRION;

ARTICLE; ATOMIC FORCE MICROSCOPY; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; ELECTROPHORETIC MOBILITY; FRACTIONATION; HYDRODYNAMICS; IMMUNOBLOTTING; MOLECULAR WEIGHT; OXIDATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; WESTERN BLOTTING; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PRION;

ALPHA-SYNUCLEIN; AMYLOID BETA-PEPTIDES; CIRCULAR DICHROISM; DOPAMINE; HUMANS; MODELS, MOLECULAR; PRIONS; PROTEIN STRUCTURE, SECONDARY;

EID: 84922208083     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2521     Document Type: Article

References (31)

1. Kalia LV, Kalia SK, McLean PJ, Lozano AM, Lang AE, (2013) α-Synuclein oligomers and clinical implications for Parkinson disease. Ann Neurol 73: 155-169.
2. Kayed R, Lasagna-Reeves CA, (2013) Molecular mechanisms of amyloid oligomers toxicity. J Alzheimers Dis 33 (Suppl 1): S67-78.
3. Jucker M, Walker LC, (2011) Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 70: 532-540.
4. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, Neuenschwander A, Abramowski D, Frey P, Jaton AL, Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, Neuenschwander A, Abramowski D, Frey P, Jaton AL, Vigouret JM, Paganetti P, Walsh DM, Mathews PM, Ghiso J, Staufenbiel M, Walker LC, Jucker M, (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313: 1781-1784.
5. Prusiner SB, (2012) Cell biology. A unifying role for prions in neurodegenerative diseases. Science 336: 1511-1513.
6. Stohr J, Watts JC, Mensinger ZL, Oehler A, Grillo SK, Dearmond SJ, Prusiner SB, Giles K, (2012) Purified and synthetic Alzheimer's amyloid beta (Abeta) prions. Proc Natl Acad Sci U S A 109: 11025-11030.
7. Ryou C, (2007) Prions and prion diseases: fundamentals and mechanistic details. J Microbiol Biotechnol 17: 1059-1070.
8. Clinton LK, Blurton-Jones M, Myczek K, Trojanowski JQ, LaFerla FM, (2010) Synergistic Interactions between Abeta, tau, and alpha-synuclein: acceleration of neuropathology and cognitive decline. J Neurosci 30: 7281-7289.
9. Kotzbauer PT, CN, Campbell MC, Willis AW, Racette BA, Tabbal SD, Perlmutter JS, (2012) Pathologic accumulation of α-synuclein and Aβ in Parkinson disease patients with dementia. Arch Neurol 69: 1326-1331.
10. Olichney JM, GD, Salmon DP, Hofstetter CR, Hansen LA, Katzman R, Thal LJ, (1998) Cognitive decline is faster in Lewy body variant than in Alzheimer's disease. Neurology 51: 351-357.
11. Ono K, Takahashi R, Ikeda T, Yamada M, (2012) Cross-seeding effects of amyloid beta-protein and alpha-synuclein. J Neurochem 122: 883-890.
12. Tsigelny IF, Crews L, Desplats P, Shaked GM, Sharikov Y, Mizuno H, Spencer B, Rockenstein E, Trejo M, Platoshyn O, Yuan JX, Masliah E, (2008) Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS One 3: e3135.
13. Larson ME, SM, Greimel S, Kuskowski M, Schneider JA, Bennett DA, Lesné SE, (2012) Soluble α-synuclein is a novel modulator of Alzheimer's disease pathophysiology. J Neuro 32: 10253-10266.
14. Kumar A, Paslay LC, Lyons D, Morgan SE, Correia JJ, Rangachari V, (2012) Specific soluble oligomers of amyloid-β peptide undergo replication and form non-fibrillar aggregates in interfacial environments. J Biol Chem 287: 21253-21264.
15. Rekas A, Knott RB, Sokolova A, Barnham KJ, Perez KA, Masters CL, Drew SC, Cappai R, Curtain CC, Pham CLL, (2010) The structure of dopamine induced α-synuclein oligomers. Eur Biophys J 39: 1407-1419.
16. Conway KA, Rochet JC, Bieganski RM, Lansbury PT, (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294: 1346-1349.
17. Cappai R, Leck S-L, Tew DJ, Williamson NA, Smith DP, Galatis D, Sharples RA, Curtain CC, Ali FE, Cherny RA, Culvenor JG, Bottomley SP, Masters CL, Barnham KJ, Hill AF, (2005) Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. FASEB J 19: 1377-1379.
18. Choi B-K, Choi M-G, Kim J-Y, Yang Y, Lai Y, Kweon D-H, Lee NK, Shin Y-K, (2013) Large α-synuclein oligomers inhibit neuronal SNARE-mediated vesicle docking. Proc Natl Acad Sci Early Edition: 201218424.
19. Moussa CE1, WC, Rusnak M, Tomita Y, Sidhu A, (2004) Abnormal migration of human wild-type alpha-synuclein upon gel electrophoresis. Neuro Lett 371: 239-243.
20. Vlad C, Lindner K, Karreman C, Schildknecht S, Leist M, Tomczyk N, Rontree J, Langridge J, Danzer K, Ciossek T, Petre A, Gross ML, Hengerer B, Przybylski M, (2011) Autoproteolytic fragments are intermediates in the oligomerization/aggregation of the Parkinson's disease protein alpha-synuclein as revealed by ion mobility mass spectrometry. Chembiochem 12: 2740-2744.
21. Yagi H, Kusaka E, Hongo K, Mizobata T, Kawata Y, (2005) Amyloid fibril formation of α-synuclein is accelerated by preformed amyloid seeds of other proteins. J Biol Chem 280: 38609-38616.
22. Ono K, Takahashi R, Ikeda T, Yamada M, (2012) Cross-seeding effects of amyloid β-protein and α-synuclein. J Neurochem 122: 883-890.
23. Leong SL, Pham CLL, Galatis D, Fodero-Tavoletti MT, Perez K, Hill AF, Masters CL, Ali FE, Barnham KJ, Cappai R, (2009) Formation of dopamine-mediated alpha-synuclein-soluble oligomers requires methionine oxidation. Free Radic Biol Med 46: 1328-1337.
24. Pham CL, Leong SL, Ali FE, Kenche VB, Hill AF, Gras SL, Barnham KJ, Cappai R, (2009) Dopamine and the dopamine oxidation product 5,6-dihydroxylindole promote distinct on-pathway and off-pathway aggregation of alpha-synuclein in a pH-dependent manner. J Mol Biol 387: 771-785.
25. Illes-Toth E, Dalton CF, Smith DP, (2013) Binding of dopamine to alpha-synuclein is mediated by specific conformational states. J Am Soc Mass Spectrom 24: 1346-1354.
26. Bisaglia M, Tosatto L, Munari F, Tessari I, de Laureto PP, Mammi S, Bubacco L, (2010) Dopamine quinones interact with alpha-synuclein to form unstructured adducts. Biochem Biophys Res Commun 394: 424-428.
27. Vitalis A, Wang X, Pappu RV, (2008) Atomistic simulations of the effects of polyglutamine chain length and solvent quality on conformational equilibria and spontaneous homodimerization. J Mol Biol 384: 279-297.
28. Vitalis A, Pappu RV, (2011) Assessing the contribution of heterogeneous distributions of oligomers to aggregation mechanisms of polyglutamine peptides. Biophys Chem 159: 14-23.
29. Wild-Bode C, Yamazaki T, Capell A, Leimer U, Steiner H, Ihara Y, Haass C, (1997) Intracellular generation and accumulation of amyloid beta-peptide terminating at amino acid 42. J Biol Chem 272: 16085-16088.
30. Masuda-Suzukake M, Nonaka T, Hosokawa M, Oikawa T, Arai T, Akiyama H, Mann DMA, Hasegawa M, (2013) Prion-like spreading of pathological α-synuclein in brain. Brain 136: 1128-1138.
31. Kumar A, Bullard RL, Patel P, Paslay LC, Singh D, Bienkiewicz EA, Morgan SE, Rangachari V, (2011) Non-esterified fatty acids generate distinct low-molecular weight amyloid-β (Aβ42) oligomers along pathway different from fibril formation. PLoS One 6: e18759.