Covalent α-Synuclein Dimers: Chemico-Physical and Aggregation Properties

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Pivato, Micaela ^a   De Franceschi, Giorgia ^a   Tosatto, Laura ^a,c   Frare, Erica ^a   Kumar, Dhruv ^b   Aioanei, Daniel ^b   Brucale, Marco ^c   Tessari, Isabella ^a   Bisaglia, Marco ^a   Samori, Bruno ^b   de Laureto, Patrizia Polverino ^a   Bubacco, Luigi ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COVALENT BOND; DIMERIZATION; FLUORESCENCE POLARIZATION; INFRARED SPECTROSCOPY; MOLECULAR CLONING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TRANSMISSION ELECTRON MICROSCOPY;

ALPHA-SYNUCLEIN; AMYLOID; ANIMALS; CHEMISTRY, PHYSICAL; CHROMATOGRAPHY; CIRCULAR DICHROISM; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASE K; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; PARKINSON DISEASE; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SODIUM DODECYL SULFATE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SWINE;

EID: 84871332049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050027     Document Type: Article

References (58)

1. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
2. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M, (1998) alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci U S A 95: 6469-6473.
3. Geddes AJ, Parker KD, Atkins EDT, Beighton E, (1968) Cross-β conformation in proteins. J Mol Biol 32: 343-344.
4. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
5. Krueger R, Kuhn W, Mueller T, Woitalla D, Graeber M, et al. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18: 106-108.
6. Zarranz JJ, Alegre J, Comez-Esteban JC, Lezcano E, Ros R, et al. (2003) The new mutation, E46K, of α-synuclein causes Parkinson and Lewy Body Dementia. Ann Neurobiol 55: 164-173.
7. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, et al. (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
8. Chartier-Harlin MC, Kachergus BS, Roumier C, Mouroux V, Lincoln S, et al. (2004) α-Synuclein locus duplication as a cause of familiar Parkinson's disease. The Lancet 364: 1167-1169.
9. Cookson MR, (2009) α-Synuclein and neuronal cell death. Mol Neurodegen 4: 114.
10. Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, et al. (1993) Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 23: 282-286.
11. Han H, Weinreb PH, Lansbury PTJ, (1995) The core Alzheimer's peptide NAC forms amyloid fibrils which seed and ae seeded by beta-amyloid: is NAC a common trigger or target in neurodegenerative disease? Chem Biol 2: 163-169.
12. Li J, Uversky VN, Fink A, (2001) Effect of Familial Parkinson's Disease Point Mutations A30P and A53T on the Structural Properties, Aggregation, and Fibrillation of Human alpha-Synuclein. Biochemistry 40: 11604-11613.
13. Wright PE, Dyson HJ, (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293: 321-331.
14. Uversky VN, (2003) A protein-chameleon: conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 21: 211-234.
15. Uversky VN, Lee HJ, Li J, Fink AL, Lee SJ, (2001) Stabilization of partially folded conformation during alpha-synuclein oligomerization in both purified and cytosolic preparations. J Biol Chem 276: 43495-43498.
16. Uversky VN, Li J, Fink AL, (2001) Evidence for a Partially Folded Intermediate in α-Synuclein Fibril Formation. J Biol Chem 276: 10737-10744.
17. Dedmon MM, Lindorff-Larsen K, Christodoulou J, Vendruscolo M, Dobson CM, (2005) Mapping long-range interactions in alpha-synuclein using spin-label NMR and ensemble molecular dynamics simulations. J Am Chem Soc 127: 476-477.
18. Bertoncini CW, Jung YS, Fernandez CO, Hoyer W, Griesinger C, et al. (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein. Proc Natl Acad Sci U S A 102: 1430-1435.
19. Bartels T, Choi JG, Selkoe DJ, (2011) α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477: 107-110.
20. Wang W, Perovic I, Chittuluru J, Kaganovich A, Nguyen LTT, et al. (2011) A soluble α synuclein construct forms a dynamic tetramer. Proc Natl Acad Sci U S A 109: 2336-2341.
21. Fauvet B, Kamdem MM, Fares MB, Desobry C, Michaela S, et al. (2012) Alpha-synuclein in the central nervous system and from erythrocytes, mammalian cells and E. coli exists predominantly as a disordered monomer. J Biol Chem 287: 15345-15364.
22. Jarret JT, Lansbury PTJ, (1992) Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31: 12345-12352.
23. Wood SJ, Wypych J, Steavenson S, Louis JC, Citron M, et al. (1999) α-Synuclein fibrillogenesis is nucleation dependent. J Biol Chem 278: 19509-19512.
24. Cremandes N, Cohen SI, Deas E, Abramov AY, Chen AY, et al. (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell 25: 1048-1059.
25. Souza JM, Giasson BI, Chen Q, Lee VM, Ischiropoulos H, (2000) Dityrosine cross-linking promotes formation of stable alpha-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J Biol Chem 275: 18344-18348.
26. Takahashi T, Yamashita H, Nakamura T, Nagano Y, Nakamura S, (2002) Tyrosine 125 of α-synuclein plays a critical role for dimerization following nitrative stress. Brain Res 938: 73-80.
27. Krishnan S, Chi EY, Wood SJ, Kendrick BS, Li C, et al. (2003) Oxidative dimer formation is the critical rate-limiting step for Parkinson's disease α-synuclein fibrillogenesis. Biochemistry 42: 829-837.
28. De Franceschi G, Frare E, Bubacco L, Mammi S, Fontana A, et al. (2009) Molecular insights into the interaction between α-synuclein and docosahexaenoic acid. J Mol Biol 394: 94-107.
29. Gill SC, Hippel PH, (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326.
30. Byler DM, Susi H, (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25: 469-487.
31. Arrondo JLR, Muga A, Castresana J, Goni FM, (1993) Quantitative studies ofthe structure ofproteins in solution by Fourier-transform infrared-spectroscopy. Prog Biophys Mol Biol 59: 23-56.
32. LeVine H, (1993) Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci 2: 404-410.
33. Aioanei D (2012) Lazy Shortest Path Computation in Dynamic Graphs. Computer Science, AGH University of Science and Technology Press, ISSN 1508-2806.
34. Weinreb PH, Zhen W, Poon AW, Conway KA, Lansbury PT, (1996) NACP, a protein implicated in Alzheimer disease comprehension and learning, is natively unfolded. Biochemistry 35: 13709-13705.
35. Surewicz WK, Mantsch HH, Chapman D, (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry 32: 389-394.
36. Wellner N, Belton PS, Tatham AS, (1996) Fourier transform IR spectroscopic study of hydration-induced structure changes in the solid state of x-gliadins. Biochemistry J 319: 741-747.
37. Barth A, (2000) The infrared absorption of amino acid side chains. Prog Biophys & Mol Biol 74: 141-173.
38. Venyaminov SY, Kalnin NN, (1990) Biopolymers 30: 1243-1257.
39. Oberg KA, Ruysschaert JM, Goormaghtigh E, (2004) The optimization of protein secondary structure determination with infrared and circular dichroism spectra. Eur J Biochem 271: 2937-2948.
40. Adochitei A, Drochioiu G, (2011) Rapid characterization of peptide secondary structure by FT-IR spectroscopy. Rev Roum Chim 56: 783-791.
41. Fabian H, Choo LP, Szendrei GI, Jackson M, Halliday WC, et al. (1993) Infrared spectroscopic characterization of Alzheimer plaques. Applied Spectroscopy 47: 1513-1518.
42. Ferreon AC, Deniz AA, (2007) α-Synuclein multistate folding thermodynamics: implications for the protein misfolding and aggregation. Biochemistry 46: 4409-4509.
43. Luk CK, Hyde EG, Trojanowski JQ, Lee VMY, (2007) Sensitive fluorescence polarization technique for rapid screening of α-synuclein oligomerization/fibrillization inhibitors. Biochemistry 46: 12522-12529.
44. Frare E, Mossuto MF, Polverino de Laureto P, Dumoulin M, Dobson CM, et al. (2006) Identification of the core structure of lysozyme amyloid fibrils by proteolysis. J Mol Biol 361: 551-561.
45. van Raaij ME, van Gestel J, Segers-Nolten IMJ, de Leeuw SW, Subramaniam V, (2008) Concentration dependence of α-synuclein fibril length assessed by quantitative atomic force microscopy and statistical-mechanical theory. Biophys J 95: 4871-4878.
46. Fink AL, (2006) The aggregation and fibrillation of α-synuclein. Acc Chem Res 39: 628-634.
47. Fontana A, Polverino de Laureto P, Spolaore B, Frare E, Picotti P, et al. (2004) Probing protein structure by limited proteolysis. Acta Biochim Pol 51: 299-321.
48. Polverino de Laureto P, Taddei N, Frare E, Capanni C, Costantini S, et al. (2003) Protein Aggregation and Amyloid Fibril Formation by an SH3 Domain Probed by Limited Proteolysis. J Mol Biol 334: 129-141.
49. Ebeling W, Hennrich N, Klockow M, Metz H, Orth HD, et al. (1974) Proteinase K from Tritirachium album Limber. Eur J Biochem 47: 91-97.
50. Miake H, Mizusawa H, Iwatsubo T, Hasegawa M, (2002) Biochemical characterization of the core structure of alpha-synuclein filaments. J Biol Chem 277: 19213-19219.
51. Qin Z, Hu D, Han S, Reaney SH, Di Monte DA, et al. (2007) Role of different regions of α-synuclein in the assembly of fibrils. Biochemistry 46: 13322-13330.
52. Zhou W, Freed CR, (2004) Tyrosine-to-cysteine modification of human alpha-synuclein enhances protein aggregation and cellular toxicity. J Biol Chem 279: 10128-10135.
53. Zhou W, Milder JB, Freed CR, (2008) Transgenic mice overexpressing tyrosine-to-cysteine mutant human alpha-synuclein: a progressive neurodegenerative model of diffuse Lewy body disease. J Biol Chem 283: 9863-9870.
54. Kloepper KD, Hartman KL, Ladror DT, Rienstra CM, (2007) Solid-state NMR spectroscopy reveals that water is nonessential to the core structure of α-synuclein fibrils. J Physical Chem 111: 13353-13356.
55. Vilar M, Chou HT, Luehrs T, Maji SK, Riek-Loher D, et al. (2008) The fold of α-synuclein fibrils. Proc Natl Acad Sci U S A 105: 8637-8642.
56. Karyagina I, Becker S, Giller K, Riedel D, Jovin TM, et al. (2011) Electron paramagnetic resonance spectroscopy measures the distance between the external β-strands of folded α-synuclein in amyloid fibrils. Biophy J pp. L01-L03.
57. Serpell LC, Berriman J, Jakes R, Goedert M, Crowther RA, (2000) Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 25: 4897-4902.
58. Zhang F, Lin XJ, Ji LN, Du HN, Tang L, et al. (2008) Assembly of alpha-synuclein fibrils in nanoscale studied by peptide truncation and AFM. Biochem Biophys Res Commun 368: 388-394.