Cu(II) and dopamine bind to α-synuclein and cause large conformational changes

FEBS Journal

Volumn 281, Issue 12, 2014, Pages 2738-2753

  Tavassoly, Omid ^a   Nokhrin, Sergiy ^a   Dmitriev, Oleg Y ^a   Lee, Jeremy S ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

dopamine; intrinsically disordered protein; nanopore analysis; Parkinson's disease; synuclein

Indexed keywords

ALPHA SYNUCLEIN; CUPRIC ION; DOPAMINE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; METAL BINDING; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN UNFOLDING;

DOPAMINE; INTRINSICALLY DISORDERED PROTEIN; NANOPORE ANALYSIS; PARKINSON'S DISEASE; Α-SYNUCLEIN;

ALPHA-SYNUCLEIN; BINDING SITES; CALORIMETRY; COPPER; DOPAMINE; PROTEIN CONFORMATION; PROTEIN TRANSPORT;

EID: 84902664447     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12817     Document Type: Article

References (74)

1. Lotharius J, &, Brundin P, (2002) Pathogenesis of Parkinson's disease: dopamine, vesicles and [alpha]-synuclein. Nat Rev Neurosci 3, 932-942.
2. Watanabe M, Dykes-Hoberg M, Cizewski Culotta V, Price DL, Wong PC, &, Rothstein JD, (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol Dis 8, 933-941.
3. Jaikaran ETAS, &, Clark A, (2001) Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim Biophys Acta Mol Basis Dis 1537, 179-203.
4. Dawson TM, &, Dawson VL, (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302, 819-822.
5. Selkoe DJ, (2004) Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat Cell Biol 6, 1054-1061.
6. Prusiner SB, (2001) Neurodegenerative diseases and prions. N Engl J Med 344, 1516-1526.
7. Chiti F, &, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75, 333-366.
8. Janson J, Laedtke T, Parisi JE, O'Brien P, Petersen RC, &, Butler PC, (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474-481.
9. Jackson K, Barisone GA, Diaz E, Jin L-w, DeCarli C, &, Despa F, (2013) Amylin deposition in the brain: a second amyloid in Alzheimer disease? Ann Neurol 4, 517-526.
10. Wild S, Roglic G, Green A, Sicree R, &, King H, (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27, 1047-1053.
11. Hampel H, Prvulovic D, Teipel S, Jessen F, Luckhaus C, Frölich L, Riepe MW, Dodel R, Leyhe T, Bertram L, et al,. (2011) The future of Alzheimer's disease: the next 10 years. Prog Neurobiol 95, 718-728.
12. Valentine JS, Doucette PA, &, Zittin Potter S, (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu Rev Biochem 74, 563-593.
13. Uversky VN, (2007) Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation. J Neurochem 103, 17-37.
14. Capellari S, Strammiello R, Saverioni D, Kretzschmar H, &, Parchi P, (2011) Genetic Creutzfeldt-Jakob disease and fatal familial insomnia: insights into phenotypic variability and disease pathogenesis. Acta Neuropathol 121, 21-37.
15. Shaw BF, &, Valentine JS, (2007) How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem Sci 32, 78-85.
16. Millhauser GL, (2004) Copper binding in the prion protein. Acc Chem Res 37, 79-85.
17. Binolfi A, Quintanar L, Bertoncini CW, Griesinger C, &, Fernández CO, (2012) Bioinorganic chemistry of copper coordination to alpha-synuclein: relevance to Parkinson's disease. Coord Chem Rev 256, 2188-2201.
18. Furukawa Y, Kaneko K, Watanabe S, Yamanaka K, &, Nukina N, (2013) Intracellular seeded aggregation of mutant Cu, Zn-superoxide dismutase associated with amyotrophic lateral sclerosis. FEBS Lett 587, 2500-2505.
19. Walker LC, &, LeVine H, (2012) Corruption and spread of pathogenic proteins in neurodegenerative diseases. J Biol Chem 287, 33109-33115.
20. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, &, Lee VM-Y, (2012) Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338, 949-953.
21. Chandra S, Gallardo G, Fernandez-Chacon R, Schluter OM, &, Sudhof TC, (2005) Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123, 383-396.
22. Trojanowski JQ, &, Lee VM, (2002) Parkinson's disease and related synucleinopathies are a new class of nervous system amyloidoses. Neurotoxicology 23, 457-460.
23. Vamvaca K, Volles MJ, &, Lansbury PT Jr, (2009) The first N-terminal amino acids of α-synuclein are essential for α-helical structure formation in vitro and membrane binding in yeast. J Mol Biol 389, 413-424.
24. Tavassoly O, &, Lee JS, (2012) Methamphetamine binds to alpha-synuclein and causes a conformational change which can be detected by nanopore analysis. FEBS Lett 586, 3222-3228.
25. Hong D-P, Fink AL, &, Uversky VN, (2009) Smoking and Parkinson's disease: does nicotine affect α-synuclein fibrillation? Biochim Biophys Acta Proteins Proteomics 1794, 282-290.
26. Ono K, Hirohata M, &, Yamada M, (2007) Anti-fibrillogenic and fibril-destabilizing activities of anti-Parkinsonian agents for alpha-synuclein fibrils in vitro. J Neurosci Res 85, 1547-1557.
27. Latawiec D, Herrera F, Bek A, Losasso V, Candotti M, Benetti F, Carlino E, Kranjc A, Lazzarino M, Gustincich S, et al,. (2010) Modulation of alpha-synuclein aggregation by dopamine analogs. PLoS ONE 5, e9234.
28. Conway KA, Rochet JC, Bieganski RM, &, Lansbury PT Jr, (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294, 1346-1349.
29. Jethva PN, Kardani JR, &, Roy I, (2011) Modulation of alpha-synuclein aggregation by dopamine in the presence of MPTP and its metabolite. FEBS J 278, 1688-1698.
30. Di Giovanni S, Eleuteri S, Paleologou KE, Yin G, Zweckstetter M, Carrupt PA, &, Lashuel HA, (2010) Entacapone and tolcapone, two catechol O-methyltransferase inhibitors, block fibril formation of alpha-synuclein and beta-amyloid and protect against amyloid-induced toxicity. J Biol Chem 285, 14941-14954.
31. Braga CA, Follmer C, Palhano FL, Khattar E, Freitas MS, Romao L, Di Giovanni S, Lashuel HA, Silva JL, &, Foguel D, (2011) The anti-Parkinsonian drug selegiline delays the nucleation phase of alpha-synuclein aggregation leading to the formation of nontoxic species. J Mol Biol 405, 254-273.
32. Roostaee A, Beaudoin S, Staskevicius A, &, Roucou X, (2013) Aggregation and neurotoxicity of recombinant alpha-synuclein aggregates initiated by dimerization. Mol Neurodegeneration 8, 1-12.
33. Boassa D, Berlanga ML, Yang MA, Terada M, Hu J, Bushong EA, Hwang M, Masliah E, George JM, &, Ellisman MH, (2013) Mapping the subcellular distribution of α-synuclein in neurons using genetically encoded probes for correlated light and electron microscopy: implications for Parkinson's disease pathogenesis. J Neurosci 33, 2605-2615.
34. Dobson CM, (2003) Protein folding and misfolding. Nature 426, 884-890.
35. Goedert M, (2001) Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2, 492-501.
36. Walsh DM, &, Selkoe DJ, (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11, 213-228.
37. Davies P, Moualla D, &, Brown DR, (2011) Alpha-synuclein is a cellular ferrireductase. PLoS ONE 6, e15814.
38. Davies P, Wang X, Sarell CJ, Drewett A, Marken F, Viles JH, &, Brown DR, (2010) The synucleins are a family of redox-active copper binding proteins. Biochemistry 50, 37-47.
39. Wright JA, Wang X, &, Brown DR, (2009) Unique copper-induced oligomers mediate alpha-synuclein toxicity. FASEB J 23, 2384-2393.
40. Bartels T, Choi JG, &, Selkoe DJ, (2011) alpha-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477, 107-110.
41. Pedersen JT, &, Heegaard NHH, (2013) Analysis of protein aggregation in neurodegenerative disease. Anal Chem 85, 4215-4227.
42. Madampage C, Tavassoly O, Christensen C, Kumari M, &, Lee JS, (2012) Nanopore analysis: an emerging technique for studying the folding and misfolding of proteins. Prion 6, 116-123.
43. Maltsev AS, Ying J, &, Bax A, (2012) Impact of N-terminal acetylation of α-synuclein on its random coil and lipid binding properties. Biochemistry 51, 5004-5013.
44. Stefureac R, Long YT, Kraatz HB, Howard P, &, Lee JS, (2006) Transport of alpha-helical peptides through alpha-hemolysin and aerolysin pores. Biochemistry 45, 9172-9179.
45. Meng H, Detillieux D, Baran C, Krasniqi B, Christensen C, Madampage C, Stefureac RI, &, Lee JS, (2010) Nanopore analysis of tethered peptides. J Pept Sci 16, 701-708.
46. Stefureac R, Waldner L, Howard P, &, Lee JS, (2008) Nanopore analysis of a small 86-residue protein. Small 4, 59-63.
47. Stefureac RI, Madampage CA, Andrievskaia O, &, Lee JS, (2010) Nanopore analysis of the interaction of metal ions with prion proteins and peptides. Biochem Cell Biol 88, 347-358.
48. Christensen C, Baran C, Krasniqi B, Stefureac RI, Nokhrin S, &, Lee JS, (2011) Effect of charge, topology and orientation of the electric field on the interaction of peptides with the alpha-hemolysin pore. J Pept Sci 17, 726-734.
49. Zhu M, &, Fink AL, (2003) Lipid binding inhibits α-synuclein fibril formation. J Biol Chem 278, 16873-16877.
50. 2+ binding modes of recombinant alpha-synuclein-insights from EPR spectroscopy. J Am Chem Soc 130, 7766-7773.
51. Binolfi A, Rasia RM, Bertoncini CW, Ceolin M, Zweckstetter M, Griesinger C, Jovin TM, &, Fernández CO, (2006) Interaction of α-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity and fibrillation enhancement. J Am Chem Soc 128, 9893-9901.
52. Rasia RM, Bertoncini CW, Marsh D, Hoyer W, Cherny D, Zweckstetter M, Griesinger C, Jovin TM, &, Fernandez CO, (2005) Structural characterization of copper(II) binding to alpha-synuclein: insights into the bioinorganic chemistry of Parkinson's disease. Proc Natl Acad Sci USA 102, 4294-4299.
53. Sung Y-H, Rospigliosi C, &, Eliezer D, (2006) NMR mapping of copper binding sites in alpha-synuclein. Biochim Biophys Acta Proteins Proteomics 1764, 5-12.
54. Binolfi A, Lamberto GR, Duran R, Quintanar L, Bertoncini CW, Souza JM, Cervenansky C, Zweckstetter M, Griesinger C, &, Fernandez CO, (2008) Site-specific interactions of Cu(II) with alpha and beta-synuclein: bridging the molecular gap between metal binding and aggregation. J Am Chem Soc 130, 11801-11812.
55. Binolfi AS, Rodriguez EE, Valensin D, D'Amelio N, Ippoliti E, Obal G, Duran R, Magistrato A, Pritsch O, Zweckstetter M, et al,. (2010) Bioinorganic chemistry of Parkinson's disease: structural determinants for the copper-mediated amyloid formation of alpha-synuclein. Inorg Chem 49, 10668-10679.
56. Brown DR, (2007) Interactions between metals and α-synuclein- function or artefact? FEBS J 274, 3766-3774.
57. Stefureac RI, Kachayev A, &, Lee JS, (2012) Modulation of the translocation of peptides through nanopores by the application of an AC electric field. Chem Commun (Camb) 48, 1928-1930.
58. Maltsev A, Ying J, &, Bax A, (2012) Deuterium isotope shifts for backbone 1H, 15N and 13C nuclei in intrinsically disordered protein α-synuclein. J Biomol NMR 54, 181-191.
59. Maltsev AS, Chen J, Levine RL, &, Bax A, (2013) Site-specific interaction between α-synuclein and membranes probed by NMR-observed methionine oxidation rates. J Am Chem Soc 135, 2943-2946.
60. Maltsev AS, Grishaev A, &, Bax A, (2011) Monomeric α-synuclein binds Congo Red micelles in a disordered manner. Biochemistry 51, 631-642.
61. Georgieva ER, Ramlall TF, Borbat PP, Freed JH, &, Eliezer D, (2010) The lipid-binding domain of wild type and mutant α-synuclein: compactness and interconversion between the broken and extended helix forms. J Biol Chem 285, 28261-28274.
62. Bisaglia M, Tessari I, Pinato L, Bellanda M, Giraudo S, Fasano M, Bergantino E, Bubacco L, &, Mammi S, (2004) A topological model of the interaction between α-synuclein and sodium dodecyl sulfate micelles. Biochemistry 44, 329-339.
63. Krasniqi B, Scruten E, Piller J, Lee J, &, Napper S, (2012) Stability, toxicity and biological activity of retro, inversed and retro-inversed glucagon isomers. J Peptide Sci 18, 519-526.
64. Cappai R, Leck SL, Tew DJ, Williamson NA, Smith DP, Galatis D, Sharples RA, Curtain CC, Ali FE, Cherny RA, et al,. (2005) Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. FASEB J 19, 1377-1379.
65. Andén N-E, Fuxe K, Hamberoer B, &, Hökfelt T, (1966) A quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta Physiol Scand 67, 306-312.
66. Spencer JPE, Jenner A, Butler J, Aruoma OI, Dexter DT, Jenner P, &, Halliwell B, (1996) Evaluation of the pro-oxidant and antioxidant actions of L-DOPA and dopamine in vitro: implications for Parkinson's disease. Free Rad Res 24, 95-105.
67. Lendel C, Bertoncini CW, Cremades N, Waudby CA, Vendruscolo M, Dobson CM, Schenk D, Christodoulou J, &, Toth G, (2009) On the mechanism of nonspecific inhibitors of protein aggregation: dissecting the interactions of alpha-synuclein with Congo red and Lacmoid. Biochemistry 48, 8322-8334.
68. Herrera FE, Chesi A, Paleologou KE, Schmid A, Munoz A, Vendruscolo M, Gustincich S, Lashuel HA, &, Carloni P, (2008) Inhibition of alpha-synuclein fibrillization by dopamine is mediated by interactions with five C-terminal residues and with E83 in the NAC region. PLoS ONE 3, e3394.
69. Lee H-J, Baek SM, Ho D-H, Suk J-E, Cho E-D, &, Lee S-J, (2011) Dopamine promotes formation and secretion of non-fibrillar alpha-synuclein oligomers. Exp Mol Med 43, 216-222.
70. Leong SL, Cappai R, Barnham KJ, &, Pham CL, (2009) Modulation of alpha-synuclein aggregation by dopamine: a review. Neurochem Res 34, 1838-1846.
71. Li H-T, Lin D-H, Luo X-Y, Zhang F, Ji L-N, Du H-N, Song G-Q, Hu J, Zhou J-W, &, Hu H-Y, (2005) Inhibition of α-synuclein fibrillization by dopamine analogs via reaction with the amino groups of α-synuclein. FEBS J 272, 3661-3672.
72. Delaglio F, Grzesiek S, Vuister G, Zhu G, Pfeifer J, &, Bax A, (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293.
73. Johnson B, &, Blevins R, (1994) NMR View: a computer program for the visualization and analysis of NMR data. J Biomol NMR 4, 603-614.
74. Stefureac RI, &, Lee JS, (2008) Nanopore analysis of the folding of zinc fingers. Small 4, 1646-1650.