The neurotransmitter serotonin interrupts α-synuclein amyloid maturation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 5, 2011, Pages 553-561

  Falsone, S Fabio ^a   Leitinger, Gerd ^b   Karner, Anita ^c   Kungl, Andreas J ^c   Kosol, Simone ^a   Cappai, Roberto ^d   Zangger, Klaus ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF GRAZ   (Austria)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aggregation; Amyloid; Indoleamine; Neurodegeneration; Parkinson disease; Protein misfolding

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; SEROTONIN;

ARTICLE; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STATIC ELECTRICITY; ULTRAFILTRATION;

ALPHA-SYNUCLEIN; AMYLOID; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROTRANSMITTER AGENTS; PROTEIN BINDING; SEROTONIN;

EID: 79953206595     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.02.008     Document Type: Article

References (57)

1. A.J. Lees, J. Hardy, and T. Revesz Parkinson's disease Lancet 373 2009 2055 2066
2. M.G. Spillantini, M.L. Schmidt, V.M. Lee, J.Q. Trojanowski, R. Jakes, and M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
3. M.G. Spillantini, R.A. Crowther, R. Jakes, M. Hasegawa, and M. Goedert alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies Proc. Natl Acad. Sci. USA 95 1998 6469 6473 (Pubitemid 28249037)
4. M. Windisch, H. Wolf, B. Hutter-Paier, and R. Wronski The role of alpha-synuclein in neurodegenerative diseases: a potential target for new treatment strategies? Neurodegener. Dis. 5 2008 218 221 (Pubitemid 351347855)
5. P.H. Weinreb, W. Zhen, A.W. Poon, K.A. Conway, and P.T. Lansbury NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded Biochemistry 35 1996 13709 13715 (Pubitemid 26363912)
6. V.N. Uversky Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation J. Neurochem. 103 2007 17 37 (Pubitemid 47407730)
7. M. Vilar, H.T. Chou, T. Lührs, S.K. Maji, D. Riek-Loher, R. Verel, G. Manning, H. Stahlberg, and R. Riek The fold of alpha-synuclein fibrils Proc. Natl Acad. Sci. USA 105 2008 8637 8642
8. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489 (Pubitemid 36444329)
9. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, and P.T. Lansbury Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291 (Pubitemid 34790672)
10. T.F. Outeiro, P. Putcha, J.E. Tetzlaff, R. Spoelgen, M. Koker, F. Carvalho, B.T. Hyman, and P.J. McLean Formation of toxic oligomeric alpha-synuclein species in living cells PLoS ONE 4 2008 e1867
11. E. Tsika, M. Moysidou, J. Guo, M. Cushman, P. Gannon, R. Sandaltzopoulos, B.I. Giasson, D. Krainc, H. Ischiropoulos, and J.R. Mazzulli Distinct region-specific alpha-synuclein oligomers in A53T transgenic mice: implications for neurodegeneration J. Neurosci. 30 2010 3409-3344
12. K.M. Danzer, D. Haasen, A.R. Karow, S. Moussaud, M. Habeck, A. Giese, H. Kretzschmar, B. Hengerer, and M. Kostka Different species of alpha-synuclein oligomers induce calcium influx and seeding J. Neurosci. 27 2007 9220 9232 (Pubitemid 47312071)
13. J.A. Wright, X. Wang, and D.R. Brown Unique copper-induced oligomers mediate alpha-synuclein toxicity FASEB J. 23 2009 2384 2393
14. H.Y. Kim, M.K. Cho, A. Kumar, E. Maier, C. Siebenhaar, S. Becker, C.O. Fernandez, H.A. Lashuel, R. Benz, A. Lange, and M. Zweckstetter Structural properties of pore-forming oligomers of alpha-synuclein J. Am. Chem. Soc. 131 2009 17482 17489
15. D.P. Karpinar, M.B. Balija, S. Kügler, F. Opazo, N. Rezaei-Ghaleh, N. Wender, H.Y. Kim, G. Taschenberger, B.H. Falkenburger, H. Heise, A. Kumar, D. Riedel, L. Fichtner, A. Voigt, G.H. Braus, K. Giller, S. Becker, A. Herzig, M. Baldus, H. Jäckle, S. Eimer, J.B. Schulz, C. Griesinger, and M. Zweckstetter Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models EMBO J. 28 2009 3256 3268
16. G.R. Lamberto, A. Binolfi, M.L. Orcellet, C.W. Bertoncini, M. Zweckstetter, C. Griesinger, and C.O. Fernández Structural and mechanistic basis behind the inhibitory interaction of PcTS on alpha-synuclein amyloid fibril formation Proc Natl Acad Sci USA 106 2009 21057 21062
17. D.E. Ehrnhoefer, J. Bieschke, A. Boeddrich, M. Herbst, L. Masino, R. Lurz, S. Engemann, A. Pastore, and E.E. Wanker EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15 2008 558 566 (Pubitemid 351799141)
18. S.L. Leong, R. Cappai, K.J. Barnham, and C.L. Pham Modulation of alpha-synuclein aggregation by dopamine: a review Neurochem. Res. 34 2009 1838 1846
19. R. Cappai, S.L. Leck, D.J. Tew, N.A. Williamson, D.P. Smith, D. Galatis, R.A. Sharples, C.C. Curtain, F.E. Ali, R.A. Cherny, J.G. Culvenor, S.P. Bottomley, C.L. Masters, K.J. Barnham, and A.F. Hill Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway FASEB J. 19 2005 1377 1379 (Pubitemid 41113755)
20. K.A. Conway, J.C. Rochet, R.M. Bieganski, and P.T. Lansbury Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct Science 294 2001 1346 1349 (Pubitemid 33063102)
21. M. Periquet, T. Fulga, L. Myllykangas, M.G. Schlossmacher, and M.B. Feany Aggregated alpha-synuclein mediates dopaminergic neurotoxicity in vivo J. Neurosci. 27 2007 3338 3346 (Pubitemid 46474139)
22. T.F. Outeiro, J. Klucken, K. Bercury, J. Tetzlaff, P. Putcha, L.M. Oliveira, A. Quintas, P.J. McLean, and B.T. Hyman Dopamine-induced conformational changes in alpha-synuclein PLoS ONE 4 2009 e6906
23. E.H. Norris, B.I. Giasson, R. Hodara, S. Xu, J.Q. Trojanowski, H. Ischiropoulos, and V.M. Lee Reversible inhibition of alpha-synuclein fibrillization by dopaminochrome-mediated conformational alterations J. Biol. Chem. 280 2005 21212 21219 (Pubitemid 40805683)
24. J.R. Mazzulli, A.J. Mishizen, B.I. Giasson, D.R. Lynch, S.A. Thomas, A. Nakashima, T. Nagatsu, A. Ota, and H. Ischiropoulos Cytosolic catechols inhibit alpha-synuclein aggregation and facilitate the formation of intracellular soluble oligomeric intermediates J. Neurosci. 26 2006 10068 10078 (Pubitemid 44477168)
25. C. Alves da Costa, J. Dunys, F. Brau, S. Wilk, R. Cappai, and F. Checler 6-Hydroxydopamine but not 1-methyl-4-phenylpyridinium abolishes alpha-synuclein antiapoptotic phenotype by inhibiting its proteasomal degradation and by promoting its aggregation J. Biol. Chem. 281 2006 9824 9831 (Pubitemid 43864701)
26. C.L. Pham, S.L. Leong, F.E. Ali, V.B. Kenche, A.F. Hill, S.L. Gras, K.J. Barnham, and R. Cappai 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 2009 771 785
27. M. Bisaglia, S. Mammi, and L. Bubacco Kinetic and structural analysis of the early oxidation products of dopamine: analysis of the interactions with alpha-synuclein J. Biol. Chem. 282 2007 15597 15605 (Pubitemid 47093273)
28. D. Latawiec, F. Herrera, A. Bek, V. Losasso, M. Candotti, F. Benetti, E. Carlino, A. Kranjc, M. Lazzarino, S. Gustincich, P. Carloni, and G. Legname Modulation of alpha-synuclein aggregation by dopamine analogs PLoS ONE 5 2010 e9234
29. P. Inbar, M.R. Bautista, S.A. Takayama, and J. Yang Assay to screen for molecules that associate with Alzheimer's related beta-amyloid fibrils Anal. Chem. 80 2008 3502 3506 (Pubitemid 351620741)
30. D. Morshedi, N. Rezaei-Ghaleh, A. Ebrahim-Habibi, S. Ahmadian, and M. Nemat-Gorgani Inhibition of amyloid fibrillation of lysozyme by indole derivatives-possible mechanism of action FEBS J. 274 2007 6415 6425 (Pubitemid 350215930)
31. T. Cohen, A. Frydman-Marom, M. Rechter, and E. Gazit Inhibition of amyloid fibril formation and cytotoxicity by hydroxyindole derivatives Biochemistry 45 2006 4727 4735
32. A.A. Reinke, H.Y. She, and J.E. Gestwicki A chemical screening approach reveals that indole fluorescence is quenched by pre-fibrillar but not fibrillar amyloid-beta Bioorg. Med. Chem. Lett. 19 2009 4952 4957
33. S.H. Fox, R. Chuang, and J.M. Brotchie Serotonin and Parkinson's disease: on movement, mood, and madness Mov. Disord. 24 2009 1255 1266
34. K.R. Chaudhuri, and A.H. Schapira Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment Lancet Neurol. 8 2009 464 474
35. T.N. Taylor, W.M. Caudle, K.R. Shepherd, A. Noorian, C.R. Jackson, P.M. Iuvone, D. Weinshenker, J.G. Greene, and G.W. Miller Nonmotor symptoms of Parkinson's disease revealed in an animal model with reduced monoamine storage capacity J. Neurosci. 29 2009 8103 8113
36. M. Kasten, L. Kertelge, N. Brüggemann, J. van der Vegt, A. Schmidt, V. Tadic, C. Buhmann, S. Steinlechner, M.I. Behrens, A. Ramirez, F. Binkofski, H. Siebner, H. Raspe, J. Hagenah, R. Lencer, and C. Klein Nonmotor symptoms in genetic Parkinson disease Arch. Neurol. 67 2010 670 676
37. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
38. N. Sreerama, S.Y. Venyaminov, and R.W. Woody Estimation of the number of helical and strand segments in proteins using CD spectroscopy Protein Sci. 8 1999 370 380 (Pubitemid 29072437)
39. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
40. H. LeVine III Quantification of beta-sheet amyloid fibril structures with thioflavin T Meth. Enzymol. 309 1999 274 284
41. G. Yamin, V.N. Uversky, and A.L. Fink Nitration inhibits fibrillation of human alpha-synuclein in vitro by formation of soluble oligomers FEBS Lett. 542 2003 147 152 (Pubitemid 36555731)
42. J. Li, V.N. Uversky, and A.L. Fink Conformational behavior of human alpha-synuclein is modulated by familial Parkinson's disease point mutations A30P and A53T Neurotoxicology 23 2002 553 567 (Pubitemid 36527676)
43. S.F. Falsone, A.J. Kungl, A. Rek, R. Cappai, and K. Zangger The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein alpha-synuclein J. Biol. Chem. 284 2009 31190 31199
44. X. Meng, L.A. Munishkina, A.L. Fink, and V.N. Uversky Molecular mechanisms underlying the flavonoid-induced inhibition of alpha-synuclein fibrillation Biochemistry 48 2009 8206 8212
45. W. Zhou, A. Gallagher, D.P. Hong, C. Long, A.L. Fink, and V.N. Uversky At low concentrations, 3,4-dihydroxyphenylacetic acid (DOPAC) binds non-covalently to alpha-synuclein and prevents its fibrillation J. Mol. Biol. 388 2009 597 610
46. V.N. Uversky, and A.L. Fink Conformational constraints for amyloid fibrillation: the importance of being unfolded Biochim. Biophys. Acta 1698 2004 131 153 (Pubitemid 38591469)
47. C.R. Bodner, A.S. Maltsev, C.M. Dobson, and A. Bax Differential phospholipid binding of alpha-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy Biochemistry 49 2010 862 871
48. C.O. Fernández, W. Hoyer, M. Zweckstetter, E.A. Jares-Erijman, V. Subramaniam, C. Griesinger, and T.M. Jovin NMR of alpha-synuclein-polyamine complexes elucidates the mechanism and kinetics of induced aggregation EMBO J. 23 2004 2039 2046 (Pubitemid 38737731)
49. M.M. Dedmon, K. Lindorff-Larsen, J. Christodoulou, M. Vendruscolo, and C.M. Dobson Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations J. Am. Chem. Soc. 127 2005 476 477 (Pubitemid 40174345)
50. C.W. Bertoncini, Y.S. Jung, C.O. Fernandez, W. Hoyer, C. Griesinger, T.M. Jovin, and M. Zweckstetter Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein Proc. Natl Acad. Sci. USA 102 2005 1430 1435 (Pubitemid 40209187)
51. E.N. Lee, H.J. Cho, C.H. Lee, D. Lee, K.C. Chung, and S.R. Paik Dequalinium-induced protofibril formation of alpha-synuclein J. Biol. Chem. 281 2006 3463 3472
52. R. Lowe, D.L. Pountney, P.H. Jensen, W.P. Gai, and N.H. Voelcker Calcium(II) selectively induces alpha-synuclein annular oligomers via interaction with the C-terminal domain Protein Sci. 13 2004 3245 3252 (Pubitemid 39557794)
53. J.R. Mazzulli, M. Armakola, M. Dumoulin, I. Parastatidis, and H. Ischiropoulos Cellular oligomerization of alpha-synuclein is determined by the interaction of oxidized catechols with a C-terminal sequence J. Biol. Chem. 282 2007 31621 31630 (Pubitemid 350044848)
54. J. Pratuangdejkul, W. Nosoongnoen, G.A. Guerin, S. Loric, M. Conti, J.M. Launay, and P. Manivet Conformational dependence of serotonin theoretical pK(a) prediction Chem. Phys. Lett. 420 2006 538 544 (Pubitemid 43332884)
55. Z. Qin, D. Hu, S. Han, D.P. Hong, and A.L. Fink Role of different regions of alpha-synuclein in the assembly of fibrils Biochemistry 46 2007 13322 13330 (Pubitemid 350136372)
56. M. Chen, M. Margittai, J. Chen, and R. Langen Investigation of alpha-synuclein fibril structure by site-directed spin labeling J. Biol. Chem. 282 2007 24970 24979 (Pubitemid 47347515)
57. H. Braak, E. Ghebremedhin, U. Rüb, H. Bratzke, and K. Del Tredici Stages in the development of Parkinson's disease-related pathology Cell Tissue Res. 318 2004 121 134 (Pubitemid 39362633)