Small-angle neutron scattering reveals the assembly of alpha-synuclein in lipid membranes

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 12, 2015, Pages 1881-1889

  Anunciado, Divina ^a   Rai, Durgesh K ^a   Qian, Shuo ^a   Urban, Volker ^a   O'Neill, Hugh ^a  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Aggregation; Alpha synuclein; Hierarchical structure; Lipid membrane; Parkinson's disease; Small angle scattering

Indexed keywords

ALPHA SYNUCLEIN; MONOMER; MEMBRANE LIPID;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DATA ANALYSIS; DISPERSION; NEUTRON SCATTERING; PHOSPHOLIPID MEMBRANE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; WESTERN BLOTTING; METABOLISM; NEUTRON; RADIATION SCATTERING;

ALPHA-SYNUCLEIN; MEMBRANE LIPIDS; NEUTRONS; SCATTERING, RADIATION;

EID: 84944081296     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.08.009     Document Type: Article

References (88)

1. V.N.U.a.A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 6 2010 1231 1264
2. P.E.a.D. Wright, and H.J. Linking folding and binding Curr. Opin. Struct. Biol. 19 2009
3. V.N. Uversky Intrinsically disordered proteins from A to Z Int. J. Biochem. Cell Biol. 43 2011 1090 1103
4. S. Ltic, and et al. Alpha-synuclein is expressed in different tissues during human fetal development J. Mol. Neurosci. 22 3 2004 199 204
5. R. Jakes, M.G. Spillantini, and M. Goedert Identification of two distinct synucleins from human brain FEBS Lett. 345 1 1994 27 32
6. H. Han, P.H. Weinreb, and P.T. Lansbury Jr. The core Alzheimer's peptide NAC forms amyloid fibrils which seed and are seeded by beta-amyloid: is NAC a common trigger or target in neurodegenerative disease? Chem. Biol. 2 3 1995 163 169
7. W.S. Davidson, and et al. Stabilization of α-synuclein secondary structure upon binding to synthetic membranes J. Biol. Chem. 273 16 1998 9443 9449
8. O.M.a.T. Outeiro Alpha-synuclein: from secretion to dysfunction Cell Death Dis. 2012 3(350)
9. J. Neurosci. Res. 58 1998 120 129
10. J.A. Obeso, and et al. Missing pieces in the Parkinson's disease puzzle Nat. Med. 16 6 2010 653 661
11. S. Appel-Cresswell, and et al. Alpha-synuclein p.H50Q, a novel pathogenic mutation for Parkinson's disease Mov. Disord. 28 6 2013 811 813
12. A.P. Kiely, and et al. α-Synucleinopathy associated with G51D SNCA mutation: a link between Parkinson's disease and multiple system atrophy? Acta Neuropathol. 125 5 2013 753 769
13. P. Pasanen, and et al. Novel alpha-synuclein mutation A53E associated with atypical multiple system atrophy and Parkinson's disease-type pathology Neurobiol. Aging 35 9 2014 2180 (e1-5)
14. M.H. Polymeropoulos, and et al. Mutation in the α-synuclein gene identified in families with Parkinson's disease Science 276 5321 1997 2045 2047
15. A. Recchia, and et al. α-Synuclein and Parkinson's disease FASEB J. 18 6 2004 617 626
16. J.J. Zarranz, and et al. The new mutation, E46K, of α-synuclein causes Parkinson and Lewy body dementia Ann. Neurol. 55 2 2004 164 173
17. O. Marques, and T.F. Outeiro Alpha-synuclein: from secretion to dysfunction and death Cell Death Dis. 3 2012 e350
18. E. Hellstrand, and et al. Membrane lipid co-aggregation with alpha-synuclein fibrils PLoS One 8 10 2013 e77235
19. L. Bousset, and et al. Structural and functional characterization of two alpha-synuclein strains Nat. Commun. 4 2013 2575
20. B. Winner, and et al. In vivo demonstration that {alpha}-synuclein oligomers are toxic Proc. Natl. Acad. Sci. U. S. A. 2011
21. V.N. Uversky, and D. Eliezer Biophysics of Parkinson's disease: structure and aggregation of alpha-synuclein Curr. Protein Pept. Sci. 10 5 2009 483 499
22. P.J. McLean, and et al. Membrane association and protein conformation of α-synuclein in intact neurons: effect of Parkinson′s disease-linked mutations J. Biol. Chem. 275 12 2000 8812 8816
23. P.K. Auluck G. Caraveo, and S. Lindquist, alpha-Synuclein: membrane interactions and toxicity in Parkinson's disease Annu. Rev. Cell Dev. Biol. 26 2010 211 233
24. E. Jo, and et al. Alpha-synuclein membrane interactions and lipid specificity J. Biol. Chem. 275 44 2000 34328 34334
25. T. Bartels, and et al. The N-terminus of the intrinsically disordered protein alpha-synuclein triggers membrane binding and helix folding Biophys. J. 99 7 2010 2116 2124
26. I. Dikiy, and D. Eliezer Folding and misfolding of alpha-synuclein on membranes Biochim. Biophys. Acta Biomembr. 1818 4 2012 1013 1018
27. A.C. Ferreon, and et al. Interplay of alpha-synuclein binding and conformational switching probed by single-molecule fluorescence Proc. Natl. Acad. Sci. U. S. A. 106 14 2009 5645 5650
28. M. Sandal, and et al. Conformational equilibria in monomeric alpha-synuclein at the single-molecule level PLoS Biol. 6 1 2008 e6
29. T.S. Ulmer, and et al. Structure and dynamics of micelle-bound human alpha-synuclein J. Biol. Chem. 280 10 2005 9595 9603
30. A.J. Trexler, and E. Rhoades Single molecule characterization of alpha-synuclein in aggregation-prone states Biophys. J. 99 9 2010 3048 3055
31. C.M. Pfefferkorn Heinrich, Frank., Sodt, Alexander., Maltsev, Alexander., Pastor, Richard., and Jennifer C. Lee Biophys. J. 102 2012 613 621
32. E. Hellstrand, M. Grey, M.L. Ainalem, J. Ankner, and et al. Adsorption of alpha-synuclein to supported lipid bilayers: positioning and role of electrostatics ACS Chem. Neurosci. 4 10 2013 1339 1351
33. J. Varkey, and et al. Alpha-synuclein oligomers with broken helical conformation form lipoprotein nanoparticles J. Biol. Chem. 288 24 2013 17620 17630
34. C. Huang, and et al. A new method for purification of recombinant human alpha-synuclein in Escherichia coli Protein Expr. Purif. 42 1 2005 173 177
35. F.E. Herrera, and et al. 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 10 2008 e3394
36. N.a.R.W. Sreerama Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with expanded reference set Anal. Biochem. 15 287 (2) 2000 252 260
37. R.W. Woody Circular dichroism Methods Enzymol. 246 1995 34 71
38. W.T. Heller, and et al. The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory J. Appl. Crystallogr. 47 4 2014
39. K. Rubinson, C. Pokalsky, S. Krueger, and L. Prochaska Structure determination of functional membrane proteins using Small-Angle Neutron Scattering (SANS) with small, mixed-lipid liposomes: native beef heart mitochondrial cytochrome c oxidase forms dimers Protein J. 32 2013 27 38
40. W. Lee, P. Kfinas, and R.M. Briber Small angle neutron scattering study of deuterated sodium dodecyl sulfate micellation in dilute poly((2-dimethylamino)ethyl methacrylate) solutions Polymer 51 2010 2872 2878
41. P. Bernado, E. Mylonas, M.V. Petoukhov, M. Blackledge, and D.I. Svergun Structural characterization of flexible proteins using small-angle-X-ray scattering J. Am. Chem. Soc. 129 17 2007 5656 5664
42. P. Calmettes, and et al. How random is a highly denatured protein? Biophys. Chem. 53 1-2 1994 105 113
43. P. Debye Molecular-weight determination by light scattering J. Phys. Colloid Chem. 51 1 1947 18 32
44. G. Beaucage, and et al. Persistence length of isotactic poly(hydroxy butyrate) Macromolecules 30 14 1997 4158 4162
45. T.E. Creighton Proteins: Structures and Molecular Properties 1993 W.H. Freeman and Co New York
46. V. Receveur-Bréchot, and D. Durand How random are intrinsically disordered proteins? A small angle scattering perspective Curr. Protein Pept. Sci. 13 1 2012 55 75
47. G. Beaucage Approximations leading to a unified exponential power-law approach to small-angle scattering J. Appl. Crystallogr. 28 1995 717 728
48. G. Beaucage Small-angle scattering from polymeric mass fractals of arbitrary mass-fractal dimension J. Appl. Crystallogr. 29 1996 134 146
49. G. Beaucage Determination of branch fraction and minimum dimension of mass-fractal aggregates Phys. Rev. E 70 3 2004 031401
50. G. Beaucage, H.K. Kammler, and S.E. Pratsinis Particle size distributions from small-angle scattering using global scattering functions J. Appl. Crystallogr. 37 2004 523 535
51. D.K. Rai, and et al. Quantitative investigations of aggregate systems J. Chem. Phys. 137 4 2012 044311 044316
52. J. Ilavsky, and P.R. Jemian Irena: tool suite for modeling and analysis of small-angle scattering J. Appl. Crystallogr. 42 2 2009 347 353
53. P.H. Weinreb, and et al. NACP, a protein implicated in Alzheimer's disease and Learning, is natively unfolded† Biochemistry 35 43 1996 13709 13715
54. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
55. R. Khurana, and et al. Mechanism of thioflavin T binding to amyloid fibrils J. Struct. Biol. 151 3 2005 229 238
56. N.C. Fitzkee, and G.D. Rose Reassessing random-coil statistics in unfolded proteins Proc. Natl. Acad. Sci. U. S. A. 101 34 2004 12497 12502
57. V.N. Uversky, J. Li, and A.L. Fink Evidence for a partially folded intermediate in α-synuclein fibril formation J. Biol. Chem. 276 14 2001 10737 10744
58. V.N. Uversky, and et al. Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of α-synuclein assembly by β- and γ-synucleins J. Biol. Chem. 277 14 2002 11970 11978
59. M. Sugiyama, and et al. Conformational characterization of a protein complex involving intrinsically disordered protein by small-angle neutron scattering using the inverse contrast matching method: a case study of interaction between [alpha]-synuclein and PbaB tetramer as a model chaperone J. Appl. Crystallogr. 47 1 2014 430 435
60. K. Moncoq, and et al. SAXS study of the PIR domain from the Grb14 molecular adaptor: a natively unfolded protein with a transient structure primer? Biophys. J. 87 6 2004 4056 4064
61. C. Putnam, M. Hammel, G.L. Hura, and J.A. Tainer Q. Rev. Biophys. 40 3 2007 191 285
62. P. Bernardo, E.M., M.V. Petoukhov, G. Tria, and D.I. Svergun Structural characterization of flexible proteins using small-angle X-ray scattering J. Am. Chem. Soc. 129 17 2007 5656 5664
63. O. Ullman, C.K. Fisher, and C.M. Stultz Explaining the structural plasticity of α-synuclein J. Am. Chem. Soc. 133 48 2011 19536 19546
64. H.B. Stuhrmann, and A. Miller Small-angle scattering of biological structures J. Appl. Crystallogr. 11 5 1978 325 345
65. S. Chandra, and et al. A broken alpha-helix in folded alpha-synuclein J. Biol. Chem. 278 17 2003 15313 15318
66. W.B. O'Dell, K.J. Beatty, J.K.-H. Tang, R.E. Blankenship, V. Urban, and H. O'Neill Sol-gel entrapped light harvesting antennas: immobilization and stabilization of chlorosomes for energy harvesting J. Mater. Chem. 22 2012 22582 22591
67. M.B. Cardoso, H.R. Luckarift, V.S. Urban, H. O'Neill, and G.R. Johnson Protein localization in silica nanospheres derived via biomimetic mineralization Mater. Views 20 2010 3031 3038
68. M. Enright, and D. Leitner Mass fractal dimension and the compactness of proteins Phys. Rev. E 71 1 2005 011912
69. K. Beyer Mechanistic aspects of Parkinson's disease: alpha-synuclein and the biomembrane Cell Biochem. Biophys. 47 2007 285 299
70. M. Bisaglia, S. Mammi, and L. Bubacco Structural insights on physiological functions and pathological effects of alpha-synuclein FASEB J. 23 2 2009 329 340
71. N.P. Reynolds, A. Soragni, M. Rabe, D. Verdes, E. Liverani, S. Handschin, R. Riek, and S. Seeger Mechanism of membrane interaction and disruption by α-synuclein J. Am. Chem. Soc. 133 2011 19366 19375
72. E. Jo, and et al. α-Synuclein-synaptosomal membrane interactions Eur. J. Biochem. 271 15 2004 3180 3189
73. Vekrellis, K., H. Rideout, and L. Stefanis, Neurobiology of α-synuclein. Mol. Neurobiol., 2004. 30(1): p. 1-21.
74. A. Sethi, D. Anunciado, J. Tian, D. Vu, and S. Gnanakaran Deducing conformational variability of intrinsically disordered proteins from infrared spectroscopy with Bayesian statistics Chem. Phys. 422 2013 143 155
75. A.L. Fink The aggregation and fibrillation of alpha-synuclein Acc. Chem. Res. 39 9 2006 628 634
76. G.P. Gorbenko, and P.K. Kinnunen The role of lipid-protein interactions in amyloid-type protein fibril formation Chem. Phys. Lipids 141 1-2 2006 72 82
77. M.O. Jensen, and O.G. Mouritsen Lipids do influence protein function - the hydrophobic matching hypothesis revisited Biochim. Biophys. Acta 1666 1-2 2004 205 226
78. L. Kjaer, L. Giehm, and D. Otzen The influence of vesicle size and composition on α-synuclein structure and stability Biophys. J. 96 2009 2857 2870
79. W.C. Breckenridge, and et al. Adult rat brain synaptic vesicles. II. Lipid composition Biochim. Biophys. Acta 320 3 1973 681 686
80. J.W. Deutsch, and R.B. Kelly Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion Biochemistry 20 2 1981 378 385
81. W. Ariesandi, C.F. Chang, T.E. Chen, and Y.R. Chen Temperature-dependent structural changes of Parkinson's alpha-synuclein reveal the role of pre-existing oligomers in alpha-synuclein fibrillarion PLoS One 8 1 2013 e53487
82. Y. Mao, and et al. Surface-induced phase separation of a sphingomyelin/cholesterol/ganglioside GM1-planar bilayer on mica surfaces and microdomain molecular conformation that accelerates Abeta oligomerization Biochim. Biophys. Acta 1798 6 2010 1090 1099
83. Fusco, G., De Simone, A., Gopinath, T., Vostrikov, V., Vendruscolo, M., Dobson, C. and G. Veglia, Direct observation of the three regions in alpha-synuclein that determine its membrane-bound behaviour. Nat. Commun., 2014. article number 3857(May 2014): p. http://dx.doi.org/10.1038/ncomms4827.
84. C. Bodner, C. Dobson, and A. Bax Multiple tight phospholipid-binding modes of α-synuclein revealed by solution NMR spectroscopy J. Mol. Biol. 390 4 2009 775 790
85. Drescher, M., Van rooijen, BD., Veldhuis, G., Subramaniam, V., and M. Huber, A Stable Lipid-induced aggregate of α-synuclein. JACS Commun., 2010. 132: p. 4080-4082.
86. A. Iyer, N.O. Petersen, M.M.A.E. Claessens, and V. Subramaniam Amyloids of alpha-synuclein affect the structure and dynamics of supported lipid bilayers Biophys. J. 106 2014 2585 2594
87. Relini, A., N. Marano, and A. Gliozzi, Probing the interplay between amyloidogenic proteins and membranes using lipid monolayers and bilayers. Adv. Colloid Interf. Sci., 2014. 207(0): p. 81-92.
88. F.T. Arce, and et al. Polymorphism of amyloid beta peptide in different environments: implications for membrane insertion and pore formation Soft Matter 7 11 2011 5267 5273