Amyloids of alpha-synuclein affect the structure and dynamics of supported lipid bilayers

Biophysical Journal

Volumn 106, Issue 12, 2014, Pages 2585-2594

  Iyer, Aditya ^a,b   Petersen, Nils O ^b,c   Claessens, Mireille M A E ^b   Subramaniam, Vinod ^a,b  

^a FOM INSTITUTE AMOLF   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; ALPHA SYNUCLEIN; AMYLOID; LIPID BILAYER; LIPOSOME; MUTANT PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; PROTEIN AGGREGATE; PROTEIN BINDING; THIAZOLE DERIVATIVE; THIOFLAVINE;

ADSORPTION; CHEMISTRY; LIPID BILAYER; METABOLISM; STAINING;

ADSORPTION; ALPHA-SYNUCLEIN; AMYLOID; LIPID BILAYERS; LIPOSOMES; MUTANT PROTEINS; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PROTEIN AGGREGATES; PROTEIN BINDING; STAINING AND LABELING; THIAZOLES;

EID: 84902995340     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.05.001     Document Type: Article

References (49)

1. M.G. Spillantini, and M.L. Schmidt M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
2. G. Fiskum, and A. Starkov C. Chinopoulos Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease Ann. N. Y. Acad. Sci. 991 2003 111 119 (Pubitemid 36793807)
3. M.H. Polymeropoulos, and C. Lavedan R.L. Nussbaum Mutation in the α-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047 (Pubitemid 27443610)
4. V.M. Nemani, and W. Lu R.H. Edwards Increased expression of α-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis Neuron 65 2010 66 79
5. M.J. Farrer Genetics of Parkinson disease: paradigm shifts and future prospects Nat. Rev. Genet. 7 2006 306 318
6. W.P. Gai, and H.X. Yuan P.H. Jensen In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin, and lipids in Lewy bodies Exp. Neurol. 166 2000 324 333
7. M.E. van Raaij, and J. van Gestel V. Subramaniam Concentration dependence of α-synuclein fibril length assessed by quantitative atomic force microscopy and statistical-mechanical theory Biophys. J. 95 2008 4871 4878
8. W. Hoyer, and T. Antony V. Subramaniam Dependence of α-synuclein aggregate morphology on solution conditions J. Mol. Biol. 322 2002 383 393
9. L.A. Munishkina, and J. Henriques A.L. Fink Role of protein-water interactions and electrostatics in α-synuclein fibril formation Biochemistry 43 2004 3289 3300 (Pubitemid 38352279)
10. K.A. Burke, E.A. Yates, and J. Legleiter Biophysical insights into how surfaces, including lipid membranes, modulate protein aggregation related to neurodegeneration Frontiers Neurol 4 2013 17
11. E. Hellstrand, and M. Grey E. Sparr Adsorption of α-synuclein to supported lipid bilayers: positioning and role of electrostatics ACS Chem. Neurosci 4 2013 1339 1351
12. M. Zhu, J. Li, and A.L. Fink The association of α-synuclein with membranes affects bilayer structure, stability, and fibril formation J. Biol. Chem. 278 2003 40186 40197 (Pubitemid 37248587)
13. M. Necula, C.N. Chirita, and J. Kuret Rapid anionic micelle-mediated α-synuclein fibrillization in vitro J. Biol. Chem. 278 2003 46674 46680 (Pubitemid 37452245)
14. J. Goers, V.N. Uversky, and A.L. Fink Polycation-induced oligomerization and accelerated fibrillation of human α-synuclein in vitro Protein Sci. 12 2003 702 707 (Pubitemid 36348457)
15. N. Lorenzen, and L. Lemminger D.E. Otzen The N-terminus of α-synuclein is essential for both monomeric and oligomeric interactions with membranes FEBS Lett. 588 2014 497 502
16. W.S. Davidson, and A. Jonas J.M. George Stabilization of α-synuclein secondary structure upon binding to synthetic membranes J. Biol. Chem. 273 1998 9443 9449 (Pubitemid 28183026)
17. E. Jo, and J. McLaurin P.E. Fraser α-Synuclein membrane interactions and lipid specificity J. Biol. Chem. 275 2000 34328 34334
18. Y.A. Domanov, and P.K. Kinnunen Islet amyloid polypeptide forms rigid lipid-protein amyloid fibrils on supported phospholipid bilayers J. Mol. Biol. 376 2008 42 54
19. K. Sasahara, and K. Morigaki D. Hamada Binding of islet amyloid polypeptide to supported lipid bilayers and amyloid aggregation at the membranes Biochemistry 51 2012 6908 6919
20. P.M. Pifer, E.A. Yates, and J. Legleiter Point mutations in Aβ result in the formation of distinct polymorphic aggregates in the presence of lipid bilayers PLoS ONE 6 2011 e16248
21. F. Hane, and E. Drolle Z. Leonenko Amyloid-β aggregation on model lipid membranes: an atomic force microscopy study J. Alzheimers Dis. 26 2011 485 494
22. N.B. Last, E. Rhoades, and A.D. Miranker Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity Proc. Natl. Acad. Sci. USA 108 2011 9460 9465
23. L. Khemtémourian, and E. Doménech J.A. Killian Low pH acts as inhibitor of membrane damage induced by human islet amyloid polypeptide J. Am. Chem. Soc. 133 2011 15598 15604
24. N.P. Reynolds, and A. Soragni S. Seeger Mechanism of membrane interaction and disruption by α-synuclein J. Am. Chem. Soc. 133 2011 19366 19375
25. M.M. Ouberai, and J. Wang M.E. Welland α-Synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling J. Biol. Chem. 288 2013 20883 20895
26. M. Rabe, and A. Soragni S. Seeger On-surface aggregation of α-synuclein at nanomolar concentrations results in two distinct growth mechanisms ACS Chem. Neurosci. 4 2013 408 417
27. E. Hellstrand, and A. Nowacka E. Sparr Membrane lipid co-aggregation with α-synuclein fibrils PLoS ONE 8 2013 e77235
28. H.A. Lashuel, and D. Hartley P.T. Lansbury Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291 (Pubitemid 34790672)
29. M. Hashimoto, and E. Rockenstein E. Masliah Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases Neuromolecular Med. 4 2003 21 36
30. C. Pacheco, L.G. Aguayo, and C. Opazo An extracellular mechanism that can explain the neurotoxic effects of α-synuclein aggregates in the brain Frontiers Physiol. 3 2012 297
31. N. Lorenzen, and S.B. Nielsen D.E. Otzen The role of stable α-synuclein oligomers in the molecular events underlying amyloid formation J. Am. Chem. Soc. 136 2014 3859 3868
32. M.T. Stöckl, M.M.A.E. Claessens, and V. Subramaniam Kinetic measurements give new insights into lipid membrane permeabilization by α-synuclein oligomers Mol. Biosyst. 8 2012 338 345
33. B.D. van Rooijen, M.M.A.E. Claessens, and V. Subramaniam Membrane permeabilization by oligomeric α-synuclein: in search of the mechanism PLoS ONE 5 2010 e14292
34. B.D. van Rooijen, M.M.A.E. Claessens, and V. Subramaniam Lipid bilayer disruption by oligomeric α-synuclein depends on bilayer charge and accessibility of the hydrophobic core Biochim. Biophys. Acta 1788 2009 1271 1278
35. A. Quist, and I. Doudevski R. Lal Amyloid ion channels: a common structural link for protein-misfolding disease Proc. Natl. Acad. Sci. USA 102 2005 10427 10432 (Pubitemid 41061570)
36. B.I. Giasson, and I.V. Murray V.M. Lee A hydrophobic stretch of 12 amino acid residues in the middle of α-synuclein is essential for filament assembly J. Biol. Chem. 276 2001 2380 2386
37. A.P. Pandey, and F. Haque J.S. Hovis Clustering of α-synuclein on supported lipid bilayers: role of anionic lipid, protein, and divalent ion concentration Biophys. J. 96 2009 540 551
38. M.E. van Raaij, I.M. Segers-Nolten, and V. Subramaniam Quantitative morphological analysis reveals ultrastructural diversity of amyloid fibrils from α-synuclein mutants Biophys. J. 91 2006 L96 L98
39. R.A. Armstrong Size frequency distributions of abnormal protein deposits in Alzheimer's disease and variant Creutzfeldt-Jakob disease Folia Neuropathol. 45 2007 108 114 (Pubitemid 47520858)
40. D.M. Soumpasis Theoretical analysis of fluorescence photobleaching recovery experiments Biophys. J. 41 1983 95 97 (Pubitemid 13114325)
41. K.J. Seu, and L.R. Cambrea J.S. Hovis Influence of lipid chemistry on membrane fluidity: tail and headgroup interactions Biophys. J. 91 2006 3727 3735 (Pubitemid 44788315)
42. V.V. Shvadchak, and L.J. Falomir-Lockhart T.M. Jovin Specificity and kinetics of α-synuclein binding to model membranes determined with fluorescent excited state intramolecular proton transfer (ESIPT) probe J. Biol. Chem. 286 2011 13023 13032
43. E.A. Waxman, J.R. Mazzulli, and B.I. Giasson Characterization of hydrophobic residue requirements for α-synuclein fibrillization Biochemistry 48 2009 9427 9436
44. J.S. Hovis, and S.G. Boxer Patterning and composition arrays of supported lipid bilayers by microcontact printing Langmuir 17 2001 3400 3405 (Pubitemid 35330451)
45. D.H. Murray, L.K. Tamm, and V. Kiessling Supported double membranes J. Struct. Biol. 168 2009 183 189
46. B. Winner, and R. Jappelli R. Riek In vivo demonstration that alpha-synuclein oligomers are toxic Proc. Natl. Acad. Sci. USA 108 2011 4194 4199
47. A.R. Braun, and E. Sevcsik J.N. Sachs α-Synuclein induces both positive mean curvature and negative Gaussian curvature in membranes J. Am. Chem. Soc. 134 2012 2613 2620
48. A.P. Pandey, and F. Haque J.S. Hovis α-Synuclein-induced tubule formation in lipid bilayers J. Phys. Chem. B 115 2011 5886 5893
49. H. Ding, and J.A. Schauerte A. Gafni β-Amyloid (1-40) peptide interactions with supported phospholipid membranes: a single-molecule study Biophys. J. 103 2012 1500 1509