Characterization of Conformational and Dynamic Properties of Natively Unfolded Human and Mouse α-Synuclein Ensembles by NMR: Implication for Aggregation

Journal of Molecular Biology

Volumn 378, Issue 5, 2008, Pages 1104-1115

  Wu, Kuen Phon ^a   Kim, Seho ^a   Fela, David A ^a   Baum, Jean ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

dynamics; mouse; NMR; Parkinson's disease; synuclein

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID A PROTEIN; AMYLOID BETA PROTEIN;

ARTICLE; GENE CLUSTER; HUMAN; HYDROPHOBICITY; LOW TEMPERATURE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 42649142233     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.017     Document Type: Article

References (55)

1. T. Mittag J.D. Forman-Kay Atomic-level characterization of disordered protein ensembles Curr. Opin. Struct. Biol. 17 2007 3 14
2. H.J. Dyson P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
3. M.G. Spillantini M.L. Schmidt V.M. Lee J.Q. Trojanowski R. Jakes M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
4. M.G. Spillantini R.A. Crowther R. Jakes M. Hasegawa 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
5. B. Caughey P.T. Lansbury Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26 2003 267 298
6. M.J. Volles P.T. Lansbury Jr Zeroing in on the pathogenic form of alpha-synuclein and its mechanism of neurotoxicity in Parkinson's disease Biochemistry 42 2003 7871 7878
7. D. Eliezer E. Kutluay R. Bussell Jr G. Browne Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073
8. C.W. Bertoncini Y.S. Jung C.O. Fernandez W. Hoyer C. Griesinger T.M. Jovin M. Zweckstetter Release of long-range tertiary interactions potentiates aggregation of natively unstructured alpha-synuclein Proc. Natl Acad. Sci. USA 102 2005 1430 1435
9. M.M. Dedmon K. Lindorff-Larsen J. Christodoulou M. Vendruscolo 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
10. Y.H. Sung D. Eliezer Residual structure, backbone dynamics, and interactions within the synuclein family J. Mol. Biol. 372 2007 689 707
11. R. Bussell Jr D. Eliezer Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein J. Biol. Chem. 276 2001 45996 46003
12. M.H. Polymeropoulos C. Lavedan E. Leroy S.E. Ide A. Dehejia A. Dutra Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047
13. R. Kruger W. Kuhn T. Muller D. Woitalla M. Graeber S. Kosel Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nature Genet. 18 1998 106 108
14. J.J. Zarranz J. Alegre J.C. Gomez-Esteban E. Lezcano R. Ros I. Ampuero The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia Ann. Neurol. 55 2004 164 173
15. K.A. Conway S.J. Lee J.C. Rochet T.T. Ding R.E. Williamson P.T. Lansbury Jr Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy Proc. Natl Acad. Sci. USA 97 2000 571 576
16. J.C. Rochet K.A. Conway P.T. Lansbury Jr Inhibition of fibrillization and accumulation of prefibrillar oligomers in mixtures of human and mouse alpha-synuclein Biochemistry 39 2000 10619 10626
17. L. Narhi S.J. Wood S. Steavenson Y. Jiang G.M. Wu D. Anafi Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation J. Biol. Chem. 274 1999 9843 9846
18. S.J. Wood J. Wypych S. Steavenson J.C. Louis M. Citron A.L. Biere alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease J. Biol. Chem. 274 1999 19509 19512
19. L.C. Serpell J. Berriman R. Jakes M. Goedert R.A. Crowther Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation Proc. Natl Acad. Sci. USA 97 2000 4897 4902
20. K.A. Conway J.D. Harper P.T. Lansbury Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease Nature Med. 4 1998 1318 1320
21. R.M. Rasia C.W. Bertoncini D. Marsh W. Hoyer D. Cherny M. Zweckstetter Structural characterization of copper(II) binding to alpha-synuclein: Insights into the bioinorganic chemistry of Parkinson's disease Proc. Natl Acad. Sci. USA 102 2005 4294 4299
22. A.E. Ferentz G. Wagner NMR spectroscopy: a multifaceted approach to macromolecular structure Quart. Rev. Biophys. 33 2000 29 65
23. S. Kim T. Szyperski GFT NMR, a new approach to rapidly obtain precise high-dimensional NMR spectral information J. Am. Chem. Soc. 125 2003 1385 1393
24. S. Kim T. Szyperski GFT NMR experiments for polypeptide backbone and 13Cbeta chemical shift assignment J. Biomol. NMR 28 2004 117 130
25. C.W. Bertoncini R.M. Rasia G.R. Lamberto A. Binolfi M. Zweckstetter C. Griesinger C.O. Fernandez Structural characterization of the intrinsically unfolded protein beta-synuclein, a natural negative regulator of alpha-synuclein aggregation J. Mol. Biol. 372 2007 708 722
26. J.A. Marsh V.K. Singh Z. Jia J.D. Forman-Kay Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein: implications for fibrillation Protein Sci. 15 2006 2795 2804
27. D. Eliezer P. Barre M. Kobaslija D. Chan X. Li L. Heend Residual structure in the repeat domain of tau: echoes of microtubule binding and paired helical filament formation Biochemistry 44 2005 1026 1036
28. J. Yao H.J. Dyson P.E. Wright Chemical shift dispersion and secondary structure prediction in unfolded and partly folded proteins FEBS Lett. 419 1997 285 289
29. H.Y. Kim H. Heise C.O. Fernandez M. Baldus M. Zweckstetter Correlation of amyloid fibril beta-structure with the unfolded state of alpha-synuclein ChemBiochem 8 2007 1671 1674
30. H. Schwalbe K.M. Fiebig M. Buck J.A. Jones S.B. Grimshaw A. Spencer Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea Biochemistry 36 1997 8977 8991
31. W.S. Cleveland S.J. Devlin Locally weighted regression: an approach to regression analysis by local fitting J. Am. Stat. Assoc. 83 1988 596 610
32. J. Klein-Seetharaman M. Oikawa S.B. Grimshaw J. Wirmer E. Duchardt T. Ueda Long-range interactions within a nonnative protein Science 295 2002 1719 1722
33. J. Wirmer H. Berk R. Ugolini C. Redfield H. Schwalbe Characterization of the unfolded state of bovine alpha-lactalbumin and comparison with unfolded states of homologous proteins Protein Sci. 15 2006 1397 1407
34. C.D. Kroenke J.P. Loria L.K. Lee M. Rance A.G. Palmer Longitudinal and transverse 1H-15N dipolar/15N chemical shift anisotropy relaxation interference: unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules J. Am. Chem. Soc. 120 1998 7905 7915
35. N. Tjandra A. Szabo A. Bax Protein backbone dynamics and 15N chemical shift anisotropy from quantitative measurement of relaxation interference effects J. Am. Chem. Soc. 118 1996 6986 6991
36. C. Wang A.G. Palmer III Solution NMR methods for quantitative identification of chemical exchange in 15N-labeled proteins Magn. Reson. Chem. 41 2003 866 876
37. C. Wang M.J. Grey A.G. Palmer III CPMG sequences with enhanced sensitivity to chemical exchange J. Biomol. NMR 21 2001 361 366
38. D.H. Wu A.D. Chen C.S. Johnson An improved diffusion-ordered spectroscopy experiment incorporating bipolar-gradient pulses J. Magn. Reson. A 115 1995 260 264
39. L.A. Munishkina J. Henriques V.N. Uversky A.L. Fink Role of protein-water interactions and electrostatics in alpha-synuclein fibril formation Biochemistry 43 2004 3289 3300
40. W. Hoyer D. Cherny V. Subramaniam T.M. Jovin Impact of the acidic C-terminal region comprising amino acids 109-140 on alpha-synuclein aggregation in vitro Biochemistry 43 2004 16233 16242
41. W. Li N. West E. Colla O. Pletnikova J.C. Troncoso L. Marsh Aggregation promoting C-terminal truncation of alpha-synuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations Proc. Natl Acad. Sci. USA 102 2005 2162 2167
42. C.W. Bertoncini C.O. Fernandez C. Griesinger T.M. Jovin M. Zweckstetter Familial mutants of alpha-synuclein with increased neurotoxicity have a destabilized conformation J. Biol. Chem. 280 2005 30649 30652
43. J.C. Kessler J.C. Rochet P.T. Lansbury Jr The N-terminal repeat domain of alpha-synuclein inhibits beta-sheet and amyloid fibril formation Biochemistry 42 2003 672 678
44. P.H. Weinreb W. Zhen A.W. Poon K.A. Conway P.T. Lansbury Jr NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded Biochemistry 35 1996 13709 13715
45. J.L. Mills T. Szyperski Protein dynamics in supercooled water: the search for slow motional modes J. Biomol. NMR 23 2002 63 67
46. J.J. Skalicky J.L. Mills S. Sharma T. Szyperski Aromatic ring-flipping in supercooled water: implications for NMR-based structural biology of proteins J. Am. Chem. Soc. 123 2001 388 397
47. F. Delaglio S. Grzesiek G.W. Vuister G. Zhu J. Pfeifer A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
48. B.A. Johnson R.A. Blevins NMR View: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
49. T.D. Goddard, D.G. Kneller, Sparky 3. University of California, San Francisco.
50. D.S. Wishart D.A. Case L. Thomas V.D.U.S. James Use of chemical shifts in macromolecular structure determination Methods in Enzymology vol. 338 2002 Academic Press 3 34
51. N.A. Farrow R. Muhandiram A.U. Singer S.M. Pascal C.M. Kay G. Gish Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation Biochemistry 33 1994 5984 6003
52. A. Jerschow N. Muller Suppression of convection artifacts in stimulated-echo diffusion experiments. double-stimulated-echo experiments J. Magn. Reson. B 125 1997 372 375
53. D.K. Wilkins S.B. Grimshaw V. Receveur C.M. Dobson J.A. Jones L.J. Smith Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38 1999 16424 16431
54. C.D. Schwieters J.J. Kuszewski N. Tjandra G.M. Clore The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 65 73
55. W. Fieber S. Kristjansdottir F.M. Poulsen Short-range, long-range and transition state interactions in the denatured state of ACBP from residual dipolar couplings J. Mol. Biol. 339 2004 1191 1199