Identification of fibril-like tertiary contacts in soluble monomeric α-synuclein

Biophysical Journal

Volumn 105, Issue 5, 2013, Pages 1192-1198

  Esteban Martín, Santiago ^a   Silvestre Ryan, Jordi ^b   Bertoncini, Carlos W ^b   Salvatella, Xavier ^b,c  

^a BARCELONA SUPERCOMPUTING CENTER   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SOLUBILITY;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SOLUBILITY;

EID: 84883629745     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.07.044     Document Type: Article

References (64)

1. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
2. S. Campioni, and B. Mannini F. Chiti A causative link between the structure of aberrant protein oligomers and their toxicity Nat. Chem. Biol. 6 2010 140 147
3. N. Cremades, and S.I. Cohen D. Klenerman Direct observation of the interconversion of normal and toxic forms of α-synuclein Cell 149 2012 1048 1059
4. Y. Miller, B. Ma, and R. Nussinov Polymorphism in Alzheimer Abeta amyloid organization reflects conformational selection in a rugged energy landscape Chem. Rev. 110 2010 4820 4838
5. T.M. Dawson, and V.L. Dawson Molecular pathways of neurodegeneration in Parkinson's disease Science 302 2003 819 822
6. H.A. Lashuel, and C.R. Overk E. Masliah The many faces of α-synuclein: from structure and toxicity to therapeutic target Nat. Rev. Neurosci. 14 2013 38 48
7. T. Bartels, J.G. Choi, and D.J. Selkoe α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation Nature 477 2011 107 110
8. B. Fauvet, and M.K. Mbefo H.A. Lashuel α-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer J. Biol. Chem. 287 2012 15345 15364
9. D.P. Karpinar, and M.B. Balija M. Zweckstetter Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models EMBO J. 28 2009 3256 3268
10. H. Heise, and W. Hoyer M. Baldus Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR Proc. Natl. Acad. Sci. USA 102 2005 15871 15876
11. M. Vilar, and H.T. Chou R. Riek The fold of alpha-synuclein fibrils Proc. Natl. Acad. Sci. USA 105 2008 8637 8642
12. V.N. Uversky, J. Li, and A.L. Fink Evidence for a partially folded intermediate in alpha-synuclein fibril formation J. Biol. Chem. 276 2001 10737 10744
13. A.S. Morar, and A. Olteanu G.J. Pielak Solvent-induced collapse of alpha-synuclein and acid-denatured cytochrome c Protein Sci. 10 2001 2195 2199
14. J.C. Lee, and R. Langen J.R. Winkler Alpha-synuclein structures from fluorescence energy-transfer kinetics: implications for the role of the protein in Parkinson's disease Proc. Natl. Acad. Sci. USA 101 2004 16466 16471
15. C.W. Bertoncini, and Y.S. Jung M. Zweckstetter Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein Proc. Natl. Acad. Sci. USA 102 2005 1430 1435
16. M.M. Dedmon, and K. Lindorff-Larsen 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
17. Y.H. Sung, and D. Eliezer Residual structure, backbone dynamics, and interactions within the synuclein family J. Mol. Biol. 372 2007 689 707
18. A.C. Ferreon, and Y. Gambin A.A. Deniz Interplay of alpha-synuclein binding and conformational switching probed by single-molecule fluorescence Proc. Natl. Acad. Sci. USA 106 2009 5645 5650
19. E. Sevcsik, and A.J. Trexler E. Rhoades Allostery in a disordered protein: oxidative modifications to α-synuclein act distally to regulate membrane binding J. Am. Chem. Soc. 133 2011 7152 7158
20. J.C. Lee, H.B. Gray, and J.R. Winkler Tertiary contact formation in alpha-synuclein probed by electron transfer J. Am. Chem. Soc. 127 2005 16388 16389
21. J.C. Lee, and B.T. Lai J.R. Winkler Alpha-synuclein tertiary contact dynamics J. Phys. Chem. B 111 2007 2107 2112
22. H.Y. Kim, and H. Heise M. Zweckstetter Correlation of amyloid fibril beta-structure with the unfolded state of alpha-synuclein ChemBioChem 8 2007 1671 1674
23. L. Salmon, and G. Nodet M. Blackledge NMR characterization of long-range order in intrinsically disordered proteins J. Am. Chem. Soc. 132 2010 8407 8418
24. J.R. Allison, and P. Varnai M. Vendruscolo Determination of the free energy landscape of alpha-synuclein using spin label nuclear magnetic resonance measurements J. Am. Chem. Soc. 131 2009 18314 18326
25. G.M. Clore, and J. Iwahara Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes Chem. Rev. 109 2009 4108 4139
26. K.P. Wu, and J. Baum Detection of transient interchain interactions in the intrinsically disordered protein alpha-synuclein by NMR paramagnetic relaxation enhancement J. Am. Chem. Soc. 132 2010 5546 5547
27. J. Silvestre-Ryan, and C.W. Bertoncini X. Salvatella Average conformations determined from PRE data provide high-resolution maps of transient tertiary interactions in disordered proteins Biophys. J. 104 2013 1740 1751
28. D. Ganguly, and J. Chen Structural interpretation of paramagnetic relaxation enhancement-derived distances for disordered protein states J. Mol. Biol. 390 2009 467 477
29. D. Van Der Spoel, and E. Lindahl H.J. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
30. R. Cowan, and R.G. Whittaker Hydrophobicity indices for amino acid residues as determined by high-performance liquid chromatography Pept. Res. 3 1990 75 80
31. S. Maurer-Stroh, and M. Debulpaep F. Rousseau Exploring the sequence determinants of amyloid structure using position-specific scoring matrices Nat. Methods 7 2010 237 242
32. G.G. Tartaglia, and M. Vendruscolo The Zyggregator method for predicting protein aggregation propensities Chem. Soc. Rev. 37 2008 1395 1401
33. R. Bussell Jr., and D. Eliezer A structural and functional role for 11-mer repeats in alpha-synuclein and other exchangeable lipid binding proteins J. Mol. Biol. 329 2003 763 778
34. D. Eliezer, and E. Kutluay G. Browne Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073
35. R. Bussell Jr., and D. Eliezer Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein J. Biol. Chem. 276 2001 45996 46003
36. A. Binolfi, and R.M. Rasia C.O. Fernández Interaction of alpha-synuclein with divalent metal ions reveals key differences: a link between structure, binding specificity and fibrillation enhancement J. Am. Chem. Soc. 128 2006 9893 9901
37. M. Chen, and M. Margittai R. Langen Investigation of alpha-synuclein fibril structure by site-directed spin labeling J. Biol. Chem. 282 2007 24970 24979
38. C. Del Mar, and E.A. Greenbaum V.L. Woods Jr. Structure and properties of alpha-synuclein and other amyloids determined at the amino acid level Proc. Natl. Acad. Sci. USA 102 2005 15477 15482
39. G.R. Lamberto, and A. Binolfi 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
40. B.I. Giasson, and I.V. Murray V.M. Lee A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly J. Biol. Chem. 276 2001 2380 2386
41. A.P. Capaldi, C. Kleanthous, and S.E. Radford Im7 folding mechanism: misfolding on a path to the native state Nat. Struct. Biol. 9 2002 209 216
42. D.M. Korzhnev, and X. Salvatella L.E. Kay Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR Nature 430 2004 586 590
43. A.A. Di Nardo, and D.M. Korzhnev A.R. Davidson Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation Proc. Natl. Acad. Sci. USA 101 2004 7954 7959
44. X. Salvatella, and C.M. Dobson M. Vendruscolo Determination of the folding transition states of barnase by using PhiI-value-restrained simulations validated by double mutant PhiIJ-values Proc. Natl. Acad. Sci. USA 102 2005 12389 12394
45. P. Neudecker, and P. Robustelli L.E. Kay Structure of an intermediate state in protein folding and aggregation Science 336 2012 362 366
46. L.M. Espinoza-Fonseca Aromatic residues link binding and function of intrinsically disordered proteins Mol. Biosyst. 8 2012 237 246
47. M. Vendruscolo Determination of conformationally heterogeneous states of proteins Curr. Opin. Struct. Biol. 17 2007 15 20
48. T. Mittag, and J.D. Forman-Kay Atomic-level characterization of disordered protein ensembles Curr. Opin. Struct. Biol. 17 2007 3 14
49. H.Y. Kim, and M.K. Cho M. Zweckstetter Structural properties of pore-forming oligomers of alpha-synuclein J. Am. Chem. Soc. 131 2009 17482 17489
50. M.S. Celej, and R. Sarroukh V. Raussens Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure Biochem. J. 443 2012 719 726
51. T.R. Jahn, and S.E. Radford The Yin and Yang of protein folding FEBS J. 272 2005 5962 5970
52. A. Sandberg, and L.M. Luheshi T. Härd Stabilization of neurotoxic Alzheimer amyloid-beta oligomers by protein engineering Proc. Natl. Acad. Sci. USA 107 2010 15595 15600
53. D.E. Ehrnhoefer, and J. Bieschke E.E. Wanker EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15 2008 558 566
54. C. Roodveldt, and C.W. Bertoncini C.M. Dobson Chaperone proteostasis in Parkinson's disease: stabilization of the Hsp70/alpha-synuclein complex by Hip EMBO J. 28 2009 3758 3770
55. C. Lendel, and C.W. Bertoncini G. Toth On the mechanism of nonspecific inhibitors of protein aggregation: dissecting the interactions of alpha-synuclein with Congo red and lacmoid Biochemistry 48 2009 8322 8334
56. T.L. Yap, C.M. Pfefferkorn, and J.C. Lee Residue-specific fluorescent probes of α-synuclein: detection of early events at the N- and C-termini during fibril assembly Biochemistry 50 2011 1963 1965
57. B. Ahmad, Y. Chen, and L.J. Lapidus Aggregation of α-synuclein is kinetically controlled by intramolecular diffusion Proc. Natl. Acad. Sci. USA 109 2012 2336 2341
58. R. Schneider, and J.R. Huang M. Blackledge Towards a robust description of intrinsic protein disorder using nuclear magnetic resonance spectroscopy Mol. Biosyst. 8 2012 58 68
59. S. Esteban-Martín, R.B. Fenwick, and X. Salvatella Refinement of ensembles describing unstructured proteins using NMR residual dipolar couplings J. Am. Chem. Soc. 132 2010 4626 4632
60. J. Iwahara, C.D. Schwieters, and G.M. Clore Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule J. Am. Chem. Soc. 126 2004 5879 5896
61. Y. Xue, and I.S. Podkorytov N.R. Skrynnikov Paramagnetic relaxation enhancements in unfolded proteins: theory and application to drkN SH3 domain Protein Sci. 18 2009 1401 1424
62. M.D. Mukrasch, and S. Bibow M. Zweckstetter Structural polymorphism of 441-residue tau at single residue resolution PLoS Biol. 7 2009 e34
63. J.R. Gillespie, and D. Shortle Characterization of long-range structure in the denatured state of staphylococcal nuclease. II. Distance restraints from paramagnetic relaxation and calculation of an ensemble of structures J. Mol. Biol. 268 1997 170 184
64. J. Song, and L.W. Guo J.L. Markley Intrinsically disordered gamma-subunit of cGMP phosphodiesterase encodes functionally relevant transient secondary and tertiary structure Proc. Natl. Acad. Sci. USA 105 2008 1505 1510