Interaction of α-synuclein with biomembranes in Parkinson's disease - Role of cardiolipin

Progress in Lipid Research

Volumn 61, Issue , 2016, Pages 73-82

  Ghio, Stephanie ^a   Kamp, Frits ^b   Cauchi, Ruben ^a   Giese, Armin ^b   Vassallo, Neville ^a  

^a UNIVERSITY OF MALTA   (Malta)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Alpha synuclein; Cardiolipin; Membrane permeabilization; Mitochondria; Oligomers; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; CARDIOLIPIN; OLIGOMER; PHOSPHOLIPID;

CHANNEL GATING; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXTRACTION; HUMAN; LIPID BILAYER; LYSIS; MEMBRANE BINDING; MITOCHONDRIAL MEMBRANE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN INTERACTION; REVIEW; ANIMAL; CELL MEMBRANE; METABOLISM; MITOCHONDRIAL DYNAMICS; PATHOLOGY; PHYSIOLOGY;

ALPHA-SYNUCLEIN; ANIMALS; CARDIOLIPINS; CELL MEMBRANE; HUMANS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANES; PARKINSON DISEASE;

EID: 84952333007     PISSN: 01637827     EISSN: 18732194     Source Type: Journal    
DOI: 10.1016/j.plipres.2015.10.005     Document Type: Review

References (173)

1. A. Elbaz, J.M. Manubens-Bertran, M. Baldereschi, M.M. Breteler, F. Grigoletto, S. Lopez-Pousa, and et al. Parkinson's disease, smoking, and family history. EUROPARKINSON Study Group J. Neurol. 247 2000 793 798
2. M. Goedert Alpha-synuclein and neurodegenerative diseases Nat. Rev. Neurosci. 2 2001 492 501
3. J. Eschbach, and K.M. Danzer Alpha-synuclein in Parkinson's disease: pathogenic function and translation into animal models Neurodegener Dis 14 2014 1 17
4. M.H. Polymeropoulos, C. Lavedan, E. Leroy, S.E. Ide, A. Dehejia, A. Dutra, and et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 276 1997 2045 2047
5. M.C. Chartier-Harlin, J. Kachergus, C. Roumier, V. Mouroux, X. Douay, S. Lincoln, and et al. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease Lancet 364 2004 1167 1169
6. R. Kruger, W. Kuhn, T. Muller, D. Woitalla, M. Graeber, S. Kosel, and et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18 1998 106 108
7. J.J. Zarranz, J. Alegre, J.C. Gomez-Esteban, E. Lezcano, R. Ros, I. Ampuero, and et al. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia Ann. Neurol. 55 2004 164 173
8. V.K. Mishra, and M.N. Palgunachari Interaction of model class A1, class A2, and class Y amphipathic helical peptides with membranes Biochemistry 35 1996 11210 11220
9. B.I. Giasson, I.V. Murray, J.Q. Trojanowski, and 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
10. D. Eliezer, E. Kutluay, R. Bussell Jr., and G. Browne Conformational properties of alpha-synuclein in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073
11. M. Chen, M. Margittai, J. Chen, and R. Langen Investigation of alpha-synuclein fibril structure by site-directed spin labeling J. Biol. Chem. 282 2007 24970 24979
12. A. Iwai, E. Masliah, M. Yoshimoto, N. Ge, L. Flanagan, H.A. de Silva, and et al. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system Neuron 14 1995 467 475
13. J. Burre, M. Sharma, T. Tsetsenis, V. Buchman, M.R. Etherton, and T.C. Sudhof Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro Science 329 2010 1663 1667
14. J. Burre, M. Sharma, and T.C. Sudhof Alpha-synuclein assembles into higher-order multimers upon membrane binding to promote SNARE complex formation Proceedings of the National Academy of Sciences of the United States of America 111 2014 E4274 E4283
15. B. Fauvet, M.K. Mbefo, M.B. Fares, C. Desobry, S. Michael, M.T. Ardah, and et al. Alpha-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
16. K.E. Paleologou, and O.M. El-Agnaf Alpha-synuclein aggregation and modulating factors Subcell. Biochem. 65 2012 109 164
17. M.G. Spillantini, M.L. Schmidt, V.M. Lee, J.Q. Trojanowski, R. Jakes, and M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
18. B. Cheng, H. Gong, H. Xiao, R.B. Petersen, L. Zheng, and K. Huang Inhibiting toxic aggregation of amyloidogenic proteins: a therapeutic strategy for protein misfolding diseases Biochim. Biophys. Acta 2013 1830 4860 4871
19. A.L. Fink The aggregation and fibrillation of alpha-synuclein Acc. Chem. Res. 39 2006 628 634
20. S.W. Chen, S. Drakulic, E. Deas, M. Ouberai, F.A. Aprile, R. Arranz, and et al. Structural characterization of toxic oligomers that are kinetically trapped during alpha-synuclein fibril formation. Proceedings of the National Academy of Sciences of the United States of America 112 2015 E1994 E2003
21. E. Kara, P.A. Lewis, H. Ling, C. Proukakis, H. Houlden, and J. Hardy Alpha-synuclein mutations cluster around a putative protein loop Neurosci. Lett. 546 2013 67 70
22. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, and et al. Alpha-synuclein locus triplication causes Parkinson's disease Science 302 2003 841
23. A. Binolfi, R.M. Rasia, C.W. Bertoncini, M. Ceolin, M. Zweckstetter, C. Griesinger, and et al. 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
24. S. Huls, T. Hogen, N. Vassallo, K.M. Danzer, B. Hengerer, A. Giese, and et al. AMPA-receptor-mediated excitatory synaptic transmission is enhanced by iron-induced alpha-synuclein oligomers J. Neurochem. 117 2011 868 878
25. A. Santner, and V.N. Uversky Metalloproteomics and metal toxicology of alpha-synuclein Metallomics: Integrated Biometal Science 2 2010 378 392
26. J. Levin, T. Hogen, A.S. Hillmer, B. Bader, F. Schmidt, F. Kamp, and et al. Generation of ferric iron links oxidative stress to alpha-synuclein oligomer formation J. Park. Dis. 1 2011 205 216
27. G.S. Nubling, J. Levin, B. Bader, S. Lorenzl, A. Hillmer, T. Hogen, and et al. Modelling Ser129 phosphorylation inhibits membrane binding of pore-forming alpha-synuclein oligomers PLoS ONE 9 2014 e98906
28. D. Lundvig, E. Lindersson, and P.H. Jensen Pathogenic effects of alpha-synuclein aggregation Brain Res. Mol. Brain Res. 134 2005 3 17
29. N. Plotegher, E. Gratton, and L. Bubacco Number and brightness analysis of alpha-synuclein oligomerization and the associated mitochondrial morphology alterations in live cells Biochim. Biophys. Acta 2014 1840 2014 2024
30. B.D. van Rooijen, M.M. Claessens, and V. Subramaniam Membrane interactions of oligomeric alpha-synuclein: potential role in Parkinson's disease Curr. Protein Pept. Sci. 11 2010 334 342
31. D. Snead, and D. Eliezer Alpha-synuclein function and dysfunction on cellular membranes Exp. Neurol. 23 2014 292 313
32. K. Beyer Mechanistic aspects of Parkinson's disease: alpha-synuclein and the biomembrane Cell Biochem. Biophys. 47 2007 285 299
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. G. Fusco, A. De Simone, T. Gopinath, V. Vostrikov, M. Vendruscolo, C.M. Dobson, and et al. Direct observation of the three regions in alpha-synuclein that determine its membrane-bound behaviour Nat. Commun. 5 2014 3827
35. C.R. Bodner, A.S. Maltsev, C.M. Dobson, and A. Bax Differential phospholipid binding of alpha-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy Biochemistry 49 2010 862 871
36. T. Bartels, L.S. Ahlstrom, A. Leftin, F. Kamp, C. Haass, M.F. Brown, and et al. The N-terminus of the intrinsically disordered protein alpha-synuclein triggers membrane binding and helix folding Biophys. J. 99 2010 2116 2124
37. T.S. Ulmer, A. Bax, N.B. Cole, and R.L. Nussbaum Structure and dynamics of micelle-bound human alpha-synuclein J. Biol. Chem. 280 2005 9595 9603
38. M. Stockl, P. Fischer, E. Wanker, and A. Herrmann Alpha-synuclein selectively binds to anionic phospholipids embedded in liquid-disordered domains J. Mol. Biol. 375 2008 1394 1404
39. W.S. Davidson, A. Jonas, D.F. Clayton, and J.M. George Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes J. Biol. Chem. 273 1998 9443 9449
40. E. Rhoades, T.F. Ramlall, W.W. Webb, and D. Eliezer Quantification of alpha-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy Biophys. J. 90 2006 4692 4700
41. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
42. C. Osman, D.R. Voelker, and T. Langer Making heads or tails of phospholipids in mitochondria J. Biol. Chem. 192 2011 7 16
43. S. Kubo, V.M. Nemani, R.J. Chalkley, M.D. Anthony, N. Hattori, Y. Mizuno, and et al. A combinatorial code for the interaction of alpha-synuclein with membranes J. Biol. Chem. 280 2005 31664 31672
44. R.J. Perrin, W.S. Woods, D.F. Clayton, and J.M. George Exposure to long chain polyunsaturated fatty acids triggers rapid multimerization of synucleins J. Biol. Chem. 276 2001 41958 41962
45. M.M. Ouberai, J. Wang, M.J. Swann, C. Galvagnion, T. Guilliams, C.M. Dobson, and et al. Alpha-synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling J. Biol. Chem. 288 2013 20883 20895
46. H. Hahl, I. Moller, I. Kiesel, S. Campioni, R. Riek, D. Verdes, and et al. Alpha-synuclein insertion into supported lipid bilayers as seen by in situ X-ray reflectivity ACS Chem. Neurosci. 6 2015 374 379
47. Z. Shi, J.N. Sachs, E. Rhoades, and T. Baumgart Biophysics of alpha-synuclein induced membrane remodelling Phys. Chem. Chem. Phys. 17 2015 15561 15568
48. V.V. Shvadchak, L.J. Falomir-Lockhart, D.A. Yushchenko, and T.M. Jovin Specificity and kinetics of alpha-synuclein binding to model membranes determined with fluorescent excited state intramolecular proton transfer (ESIPT) probe J. Biol. Chem. 286 2011 13023 13032
49. L. Kjaer, L. Giehm, T. Heimburg, and D. Otzen The influence of vesicle size and composition on alpha-synuclein structure and stability Biophys. J. 96 2009 2857 2870
50. F. Kamp, and K. Beyer Binding of alpha-synuclein affects the lipid packing in bilayers of small vesicles J. Biol. Chem. 281 2006 9251 9259
51. A.J. Trexler, and E. Rhoades Alpha-synuclein binds large unilamellar vesicles as an extended helix Biochemistry 48 2009 2304 2306
52. F. Haque, A.P. Pandey, L.R. Cambrea, J.C. Rochet, and J.S. Hovis Adsorption of alpha-synuclein on lipid bilayers: modulating the structure and stability of protein assemblies J. Phys. Chem. B 114 2010 4070 4081
53. E.R. Middleton, and E. Rhoades Effects of curvature and composition on alpha-synuclein binding to lipid vesicles Biophys. J. 99 2010 2279 2288
54. C.M. Pfefferkorn, Z. Jiang, and J.C. Lee Biophysics of alpha-synuclein membrane interactions Biochim. Biophys. Acta 2012 1818 162 171
55. K. Pirc, and N.P. Ulrih Alpha-synuclein interactions with phospholipid model membranes: key roles for electrostatic interactions and lipid-bilayer structure Biochim. Biophys. Acta 2015
56. F. Kamp, N. Exner, A.K. Lutz, N. Wender, J. Hegermann, B. Brunner, and et al. Inhibition of mitochondrial fusion by alpha-synuclein is rescued by PINK1, Parkin and DJ-1 EMBO J. 29 2010 3571 3589
57. R.C. Rivers, J.R. Kumita, G.G. Tartaglia, M.M. Dedmon, A. Pawar, M. Vendruscolo, and et al. Molecular determinants of the aggregation behavior of alpha- and beta-synuclein Protein Sci. Publ.Proten Soc. 17 2008 887 898
58. H.J. Lee, C. Choi, and S.J. Lee Membrane-bound alpha-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form J. Biol. Chem. 277 2002 671 678
59. M. Necula, C.N. Chirita, and J. Kuret Rapid anionic micelle-mediated alpha-synuclein fibrillization in vitro J. Biol. Chem. 278 2003 46674 46680
60. M. Zhu, J. Li, and A.L. Fink The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation J. Biol. Chem. 278 2003 40186 40197
61. R. Sharon, I. Bar-Joseph, M.P. Frosch, D.M. Walsh, J.A. Hamilton, and D.J. Selkoe The formation of highly soluble oligomers of alpha-synuclein is regulated by fatty acids and enhanced in Parkinson's disease Neuron 37 2003 583 595
62. N.B. Cole, D.D. Murphy, T. Grider, S. Rueter, D. Brasaemle, and R.L. Nussbaum Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein J. Biol. Chem. 277 2002 6344 6352
63. G. De Franceschi, E. Frare, M. Pivato, A. Relini, A. Penco, E. Greggio, and et al. Structural and morphological characterization of aggregated species of alpha-synuclein induced by docosahexaenoic acid J. Biol. Chem. 286 2011 22262 22274
64. M. Zhu, and A.L. Fink Lipid binding inhibits alpha-synuclein fibril formation J. Biol. Chem. 278 2003 16873 16877
65. C. Aisenbrey, T. Borowik, R. Bystrom, M. Bokvist, F. Lindstrom, H. Misiak, and et al. How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur. Biophys. J. 37 2008 247 255
66. S.L. Hardt Rates of diffusion controlled reactions in one, two and three dimensions Biophys. Chem. 10 1979 239 243
67. I.F. Tsigelny, Y. Sharikov, M.A. Miller, and E. Masliah Mechanism of alpha-synuclein oligomerization and membrane interaction: theoretical approach to unstructured proteins studies Nanomed.: Nanotechnol., Biol. Med. 4 2008 350 357
68. M. Rabe, A. Soragni, N.P. Reynolds, D. Verdes, E. Liverani, R. Riek, and et al. On-surface aggregation of alpha-synuclein at nanomolar concentrations results in two distinct growth mechanisms ACS Chem. Neurosci. 4 2013 408 417
69. C. Galvagnion, A.K. Buell, G. Meisl, T.C. Michaels, M. Vendruscolo, T.P. Knowles, and et al. Lipid vesicles trigger alpha-synuclein aggregation by stimulating primary nucleation Nat. Chem. Biol. 11 2015 229 234
70. D.P. Smith, D.J. Tew, A.F. Hill, S.P. Bottomley, C.L. Masters, K.J. Barnham, and et al. Formation of a high affinity lipid-binding intermediate during the early aggregation phase of alpha-synuclein Biochemistry 47 2008 1425 1434
71. N. Sood, and G. Jayaram Cytology of papillary adenoma of the nipple: a case diagnosed on fine-needle aspiration Diagn. Cytopathol. 6 1990 345 348
72. G. Comellas, L.R. Lemkau, D.H. Zhou, J.M. George, and C.M. Rienstra Structural intermediates during alpha-synuclein fibrillogenesis on phospholipid vesicles J. Am. Chem. Soc. 134 2012 5090 5099
73. N. Lorenzen, S.B. Nielsen, A.K. Buell, J.D. Kaspersen, P. Arosio, B.S. Vad, and et al. The role of stable alpha-synuclein oligomers in the molecular events underlying amyloid formation J. Am. Chem. Soc. 136 2014 3859 3868
74. M.S. Celej, R. Sarroukh, E. Goormaghtigh, G.D. Fidelio, J.M. Ruysschaert, and V. Raussens Toxic prefibrillar alpha-synuclein amyloid oligomers adopt a distinctive antiparallel beta-sheet structure Biochem. J. 443 2012 719 726
75. P.H. Jensen, M.S. Nielsen, R. Jakes, C.G. Dotti, and M. Goedert Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation J. Biol. Chem. 273 1998 26292 26294
76. E. Jo, N. Fuller, R.P. Rand, P. St George-Hyslop, and P.E. Fraser Defective membrane interactions of familial Parkinson's disease mutant A30P alpha-synuclein J. Mol. Biol. 315 2002 799 807
77. R. Bussell Jr., and D. Eliezer Effects of Parkinson's disease-linked mutations on the structure of lipid-associated alpha-synuclein Biochemistry 43 2004 4810 4818
78. I.F. Tsigelny, Y. Sharikov, V.L. Kouznetsova, J.P. Greenberg, W. Wrasidlo, C. Overk, and et al. Molecular determinants of alpha-synuclein mutants' oligomerization and membrane interactions ACS Chem. Neurosci. 6 2015 403 416
79. D. Ysselstein, M. Joshi, V. Mishra, A.M. Griggs, J.M. Asiago, G.P. McCabe, and et al. Effects of impaired membrane interactions on alpha-synuclein aggregation and neurotoxicity Neurobiol. Dis. 79 2015 150 163
80. B.D. van Rooijen, M.M. Claessens, and V. Subramaniam Membrane binding of oligomeric alpha-synuclein depends on bilayer charge and packing FEBS Lett. 582 2008 3788 3792
81. N. Lorenzen, L. Lemminger, J.N. Pedersen, S.B. Nielsen, and D.E. Otzen The N-terminus of alpha-synuclein is essential for both monomeric and oligomeric interactions with membranes FEBS Lett. 588 2014 497 502
82. K. Vamvaca, M.J. Volles, and P.T. Lansbury Jr. The first N-terminal amino acids of alpha-synuclein are essential for alpha-helical structure formation in vitro and membrane binding in yeast J. Mol. Biol. 389 2009 413 424
83. M. Caruana, J. Neuner, T. Hogen, F. Schmidt, F. Kamp, C. Scerri, and et al. Polyphenolic compounds are novel protective agents against lipid membrane damage by alpha-synuclein aggregates in vitro Biochim. Biophys. Acta 2012 1818 2502 2510
84. M. Stockl, M.M. Claessens, and V. Subramaniam Kinetic measurements give new insights into lipid membrane permeabilization by alpha-synuclein oligomers Mol. BioSyst. 8 2012 338 345
85. T. Hogen, J. Levin, F. Schmidt, M. Caruana, N. Vassallo, H. Kretzschmar, and et al. Two different binding modes of alpha-synuclein to lipid vesicles depending on its aggregation state Biophys. J. 102 2012 1646 1655
86. S. Askarova, X. Yang, and J.C. Lee Impacts of membrane biophysics in Alzheimer's disease: from amyloid precursor protein processing to abeta peptide-induced membrane changes Int. J. Alzheimers Dis. 2011 2011 134971
87. K. Flach, I. Hilbrich, A. Schiffmann, U. Gartner, M. Kruger, M. Leonhardt, and et al. Tau oligomers impair artificial membrane integrity and cellular viability J. Biol. Chem. 287 2012 43223 43233
88. M.F. Engel Membrane permeabilization by islet amyloid polypeptide Chem. Phys. Lipids 160 2009 1 10
89. J.F. Chich, C. Chapuis, C. Henry, J. Vidic, H. Rezaei, and S. Noinville Vesicle permeabilization by purified soluble oligomers of prion protein: a comparative study of the interaction of oligomers and monomers with lipid membranes J. Mol. Biol. 397 2010 1017 1030
90. M. Diociaiuti, G. Macchia, S. Paradisi, C. Frank, S. Camerini, P. Chistolini, and et al. Native metastable prefibrillar oligomers are the most neurotoxic species among amyloid aggregates Biochim. Biophys. Acta 2014 1842 1622 1629
91. A. Relini, S. Torrassa, R. Rolandi, A. Gliozzi, C. Rosano, C. Canale, and et al. Monitoring the process of HypF fibrillization and liposome permeabilization by protofibrils J. Mol. Biol. 338 2004 943 957
92. M. Andreasen, N. Lorenzen, and D. Otzen Interactions between misfolded protein oligomers and membranes: a central topic in neurodegenerative diseases? Biochim. Biophys. Acta 2015
93. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250
94. K.A. Maguire-Zeiss, D.W. Short, and H.J. Federoff Synuclein, dopamine and oxidative stress: co-conspirators in Parkinson's disease? Brain Res. Mol. Brain Res. 134 2005 18 23
95. J.C. Rochet, T.F. Outeiro, K.A. Conway, T.T. Ding, M.J. Volles, H.A. Lashuel, and et al. Interactions among alpha-synuclein, dopamine, and biomembranes: some clues for understanding neurodegeneration in Parkinson's disease J. Mol. Neurosci. 23 2004 23 34
96. R. Cappai, S.L. Leck, D.J. Tew, N.A. Williamson, D.P. Smith, D. Galatis, and et al. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway FASEB J. 19 2005 1377 1379
97. S. Turnbull, B.J. Tabner, O.M. El-Agnaf, S. Moore, Y. Davies, and D. Allsop Alpha-synuclein implicated in Parkinson's disease catalyses the formation of hydrogen peroxide in vitro Free Radic. Biol. Med. 30 2001 1163 1170
98. L.R. Feng, and K.A. Maguire-Zeiss Dopamine and paraquat enhance alpha-synuclein-induced alterations in membrane conductance Neurotox. Res. 20 2011 387 401
99. C.L. Pham, and R. Cappai The interplay between lipids and dopamine on alpha-synuclein oligomerization and membrane binding Biosci. Rep. 33 2013
100. C. Follmer, E. Coelho-Cerqueira, D.Y. Yatabe-Franco, G.D. Araujo, A.S. Pinheiro, G.B. Domont, and et al. Oligomerization and membrane-binding properties of covalent adducts formed by the interaction of alpha-synuclein with the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde (DOPAL) J. Biol. Chem. 2015
101. M.J. Volles, and P.T. Lansbury Jr. Vesicle permeabilization by protofibrillar alpha-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism Biochemistry 41 2002 4595 4602
102. H.Y. Kim, M.K. Cho, A. Kumar, E. Maier, C. Siebenhaar, S. Becker, and et al. Structural properties of pore-forming oligomers of alpha-synuclein J. Am. Chem. Soc. 131 2009 17482 17489
103. E. Di Pasquale, J. Fantini, H. Chahinian, M. Maresca, N. Taieb, and N. Yahi Altered ion channel formation by the Parkinson's-disease-linked E46K mutant of alpha-synuclein is corrected by GM3 but not by GM1 gangliosides J. Mol. Biol. 397 2010 202 218
104. M. Kostka, T. Hogen, K.M. Danzer, J. Levin, M. Habeck, A. Wirth, and et al. Single particle characterization of iron-induced pore-forming alpha-synuclein oligomers J. Biol. Chem. 283 2008 10992 11003
105. A.S. Hillmer, P. Putcha, J. Levin, T. Hogen, B.T. Hyman, H. Kretzschmar, and et al. Converse modulation of toxic alpha-synuclein oligomers in living cells by N′-benzylidene-benzohydrazide derivates and ferric iron Biochem. Biophys. Res. Commun. 391 2010 461 466
106. F. Schmidt, J. Levin, F. Kamp, H. Kretzschmar, A. Giese, and K. Botzel Single-channel electrophysiology reveals a distinct and uniform pore complex formed by alpha-synuclein oligomers in lipid membranes PLoS ONE 7 2012 e42545
107. S.D. Zakharov, J.D. Hulleman, E.A. Dutseva, Y.N. Antonenko, J.C. Rochet, and W.A. Cramer Helical alpha-synuclein forms highly conductive ion channels Biochemistry 46 2007 14369 14379
108. L. Tosatto, A.O. Andrighetti, N. Plotegher, V. Antonini, I. Tessari, L. Ricci, and et al. Alpha-synuclein pore forming activity upon membrane association Biochim. Biophys. Acta 2012 1818 2876 2883
109. H.A. Lashuel, B.M. Petre, J. Wall, M. Simon, R.J. Nowak, T. Walz, and et al. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils J. Mol. Biol. 322 2002 1089 1102
110. A. Quist, I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, and et al. Amyloid ion channels: a common structural link for protein-misfolding disease Proceedings of the National Academy of Sciences of the United States of America 102 2005 10427 10432
111. L. Giehm, D.I. Svergun, D.E. Otzen, and B. Vestergaard Low-resolution structure of a vesicle disrupting alpha-synuclein oligomer that accumulates during fibrillation Proceedings of the National Academy of Sciences of the United States of America 108 2011 3246 3251
112. I.F. Tsigelny, Y. Sharikov, W. Wrasidlo, T. Gonzalez, P.A. Desplats, L. Crews, and et al. Role of alpha-synuclein penetration into the membrane in the mechanisms of oligomer pore formation FEBS J. 279 2012 1000 1013
113. A. Demuro, E. Mina, R. Kayed, S.C. Milton, I. Parker, and C.G. Glabe Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J. Biol. Chem. 280 2005 17294 17300
114. K.M. Danzer, D. Haasen, A.R. Karow, S. Moussaud, M. Habeck, A. Giese, and et al. Different species of alpha-synuclein oligomers induce calcium influx and seeding J. Neurosci. 27 2007 9220 9232
115. K. Furukawa, M. Matsuzaki-Kobayashi, T. Hasegawa, A. Kikuchi, N. Sugeno, Y. Itoyama, and et al. Plasma membrane ion permeability induced by mutant alpha-synuclein contributes to the degeneration of neural cells J. Neurochem. 97 2006 1071 1077
116. R. Kayed, Y. Sokolov, B. Edmonds, T.M. McIntire, S.C. Milton, J.E. Hall, and et al. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279 2004 46363 46366
117. M.T. Stockl, N. Zijlstra, and V. Subramaniam Alpha-synuclein oligomers: an amyloid pore? Insights into mechanisms of alpha-synuclein oligomer-lipid interactions Mol. Neurobiol. 47 2013 613 621
118. Y. Sokolov, J.A. Kozak, R. Kayed, A. Chanturiya, C. Glabe, and J.E. Hall Soluble amyloid oligomers increase bilayer conductance by altering dielectric structure J. Gen. Physiol. 128 2006 637 647
119. N.B. Last, and A.D. Miranker Common mechanism unites membrane poration by amyloid and antimicrobial peptides Proceedings of the National Academy of Sciences of the United States of America 110 2013 6382 6387
120. M.T. Lee, F.Y. Chen, and H.W. Huang Energetics of pore formation induced by membrane active peptides Biochemistry 43 2004 3590 3599
121. N.P. Reynolds, A. Soragni, M. Rabe, D. Verdes, E. Liverani, S. Handschin, and et al. Mechanism of membrane interaction and disruption by alpha-synuclein J. Am. Chem. Soc. 133 2011 19366 19375
122. E. Hellstrand, A. Nowacka, D. Topgaard, S. Linse, and E. Sparr Membrane lipid co-aggregation with alpha-synuclein fibrils PLoS ONE 8 2013 e77235
123. H. Chaudhary, A.N. Stefanovic, V. Subramaniam, and M.M. Claessens Membrane interactions and fibrillization of alpha-synuclein play an essential role in membrane disruption FEBS Lett. 588 2014 4457 4463
124. A. van Maarschalkerweerd, V. Vetri, A.E. Langkilde, V. Fodera, and B. Vestergaard Protein/lipid coaggregates are formed during alpha-synuclein-induced disruption of lipid bilayers Biomacromolecules 15 2014 3643 3654
125. B. Winner, R. Jappelli, S.K. Maji, P.A. Desplats, L. Boyer, S. Aigner, and et al. In vivo demonstration that alpha-synuclein oligomers are toxic Proceedings of the National Academy of Sciences of the United States of America 108 2011 4194 4199
126. J.P. Monteiro, P.J. Oliveira, and A.S. Jurado Mitochondrial membrane lipid remodeling in pathophysiology: a new target for diet and therapeutic interventions Prog. Lipid Res. 52 2013 513 528
127. A. Colbeau, J. Nachbaur, and P.M. Vignais Enzymic characterization and lipid composition of rat liver subcellular membranes Biochim. Biophys. Acta 249 1971 462 492
128. M. Klingenberg Cardiolipin and mitochondrial carriers Biochim. Biophys. Acta 2009 1788 2048 2058
129. D. Ardail, J.P. Privat, M. Egret-Charlier, C. Levrat, F. Lerme, and P. Louisot Mitochondrial contact sites. Lipid composition and dynamics J. Biol. Chem. 265 1990 18797 18802
130. E. Mileykovskaya, and W. Dowhan Cardiolipin membrane domains in prokaryotes and eukaryotes Biochim. Biophys. Acta 2009 1788 2084 2091
131. H.H. Szeto First-in-class cardiolipin-protective compound as a therapeutic agent to restore mitochondrial bioenergetics Br. J. Pharmacol. 171 2014 2029 2050
132. J.D. Unsay, K. Cosentino, Y. Subburaj, and A.J. Garcia-Saez Cardiolipin effects on membrane structure and dynamics Langmuir ACS Surf. Colloid 29 2013 15878 15887
133. T.N. Zeczycki, J. Whelan, W.T. Hayden, D.A. Brown, and S.R. Shaikh Increasing levels of cardiolipin differentially influence packing of phospholipids found in the mitochondrial inner membrane Biochem. Biophys. Res. Commun. 450 2014 366 371
134. M.S. Parihar, A. Parihar, M. Fujita, M. Hashimoto, and P. Ghafourifar Mitochondrial association of alpha-synuclein causes oxidative stress Cell. Mol. Life Sci. 65 2008 1272 1284
135. K. Nakamura, V.M. Nemani, E.K. Wallender, K. Kaehlcke, M. Ott, and R.H. Edwards Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria J. Neurosci. Off. J. Soc. Neurosci. 28 2008 12305 12317
136. M. Robotta, H.R. Gerding, A. Vogel, K. Hauser, S. Schildknecht, C. Karreman, and et al. Alpha-synuclein binds to the inner membrane of mitochondria in an alpha-helical conformation Chembiochem Eur. J. Chem. Biol. 15 2014 2499 2502
137. L. Devi, V. Raghavendran, B.M. Prabhu, N.G. Avadhani, and H.K. Anandatheerthavarada Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain J. Biol. Chem. 283 2008 9089 9100
138. M. Robotta, C. Hintze, S. Schildknecht, N. Zijlstra, C. Jungst, C. Karreman, and et al. Locally resolved membrane binding affinity of the N-terminus of alpha-synuclein Biochemistry 51 2012 3960 3962
139. I.G. Zigoneanu, Y.J. Yang, A.S. Krois, E. Haque, and G.J. Pielak Interaction of alpha-synuclein with vesicles that mimic mitochondrial membranes Biochim. Biophys. Acta 2012 1818 512 519
140. W.W. Li, R. Yang, J.C. Guo, H.M. Ren, X.L. Zha, J.S. Cheng, and et al. Localization of alpha-synuclein to mitochondria within midbrain of mice Neuroreport 18 2007 1543 1546
141. L. Lu, C. Zhang, Q. Cai, Q. Lu, C. Duan, Y. Zhu, and et al. Voltage-dependent anion channel involved in the alpha-synuclein-induced dopaminergic neuron toxicity in rats Acta Biochim. Biophys. Sin. 45 2013 170 178
142. T.K. Rostovtseva, P.A. Gurnev, O. Protchenko, D.P. Hoogerheide, T.L. Yap, C.C. Philpott, and et al. Alpha-synuclein shows high-affinity interaction with voltage-dependent anion channel suggesting mechanisms of mitochondrial regulation and toxicity in Parkinson disease J. Biol. Chem. 2015
143. A.N. Stefanovic, M.T. Stockl, M.M. Claessens, and V. Subramaniam Alpha-synuclein oligomers distinctively permeabilize complex model membranes FEBS J. 281 2014 2838 2850
144. A. Camilleri, C. Zarb, M. Caruana, U. Ostermeier, S. Ghio, T. Hogen, and et al. Mitochondrial membrane permeabilisation by amyloid aggregates and protection by polyphenols Biochim. Biophys. Acta 2013 1828 2532 2543
145. 2 +-induced mitochondrial dysfunction J. Biol. Chem. 289 2014 21490 21507
146. K. Banerjee, M. Sinha, L. Pham Cle, S. Jana, D. Chanda, R. Cappai, and et al. Alpha-synuclein induced membrane depolarization and loss of phosphorylation capacity of isolated rat brain mitochondria: implications in Parkinson's disease FEBS Lett. 584 2010 1571 1576
147. J. Shen, T. Du, X. Wang, C. Duan, G. Gao, J. Zhang, and et al. Alpha-synuclein amino terminus regulates mitochondrial membrane permeability Brain Res. 1591 2014 14 26
148. K. Nakamura, V.M. Nemani, F. Azarbal, G. Skibinski, J.M. Levy, K. Egami, and et al. Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein J. Biol. Chem. 286 2011 20710 20726
149. T.R. Flower, L.S. Chesnokova, C.A. Froelich, C. Dixon, and S.N. Witt Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson's disease J. Mol. Biol. 351 2005 1081 1100
150. L.J. Su, P.K. Auluck, T.F. Outeiro, E. Yeger-Lotem, J.A. Kritzer, D.F. Tardiff, and et al. Compounds from an unbiased chemical screen reverse both ER-to-Golgi trafficking defects and mitochondrial dysfunction in Parkinson's disease models Dis. Model. Mech. 3 2010 194 208
151. E. Mileykovskaya, and W. Dowhan Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes Chem. Phys. Lipids 179 2014 42 48
152. M. Fry, and D.E. Green Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain J. Biol. Chem. 256 1981 1874 1880
153. M. Zhang, E. Mileykovskaya, and W. Dowhan Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane J. Biol. Chem. 277 2002 43553 43556
154. H. Bayir, A.A. Kapralov, J. Jiang, Z. Huang, Y.Y. Tyurina, V.A. Tyurin, and et al. Peroxidase mechanism of lipid-dependent cross-linking of synuclein with cytochrome C: protection against apoptosis versus delayed oxidative stress in Parkinson disease J. Biol. Chem. 284 2009 15951 15969
155. S.M. Claypool, Y. Oktay, P. Boontheung, J.A. Loo, and C.M. Koehler Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane J. Cell Biol. 182 2008 937 950
156. K. Beyer, and B. Nuscher Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/adenosine triphosphate carrier protein from beef heart mitochondria Biochemistry 35 1996 15784 15790
157. C.E. Ellis, E.J. Murphy, D.C. Mitchell, M.Y. Golovko, F. Scaglia, G.C. Barcelo-Coblijn, and et al. Mitochondrial lipid abnormality and electron transport chain impairment in mice lacking alpha-synuclein Mol. Cell. Biol. 25 2005 10190 10201
158. S.E. Gasanov, I.H. Shrivastava, F.S. Israilov, A.A. Kim, K.A. Rylova, B. Zhang, and et al. Naja naja oxiana cobra venom cytotoxins CTI and CTII disrupt mitochondrial membrane integrity: implications for basic three-fingered cytotoxins PLoS ONE 10 2015 e0129248
159. J. Xu, T.K. Vanderlick, and P.A. Beales Lytic and non-lytic permeabilization of cardiolipin-containing lipid bilayers induced by cytochrome C PLoS ONE 8 2013 e69492
160. A.M. Firsov, E.A. Kotova, E.A. Korepanova, A.N. Osipov, and Y.N. Antonenko Peroxidative permeabilization of liposomes induced by cytochrome c/cardiolipin complex Biochim. Biophys. Acta 2015 1848 767 774
161. T.A. Sarafian, C.M. Ryan, P. Souda, E. Masliah, U.K. Kar, H.V. Vinters, and et al. Impairment of mitochondria in adult mouse brain overexpressing predominantly full-length, N-terminally acetylated human alpha-synuclein PLoS ONE 8 2013 e63557
162. A. Bender, P. Desplats, B. Spencer, E. Rockenstein, A. Adame, M. Elstner, and et al. TOM40 mediates mitochondrial dysfunction induced by alpha-synuclein accumulation in Parkinson's disease PLoS ONE 8 2013 e62277
163. L.J. Martin, Y. Pan, A.C. Price, W. Sterling, N.G. Copeland, N.A. Jenkins, and et al. Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death J. Neurosci. Off. J. Soc. Neurosci. 26 2006 41 50
164. L. Li, S. Nadanaciva, Z. Berger, W. Shen, K. Paumier, J. Schwartz, and et al. Human A53T alpha-synuclein causes reversible deficits in mitochondrial function and dynamics in primary mouse cortical neurons PLoS ONE 8 2013 e85815
165. Y. Zhu, C. Duan, L. Lu, H. Gao, C. Zhao, S. Yu, and et al. Alpha-synuclein overexpression impairs mitochondrial function by associating with adenylate translocator Int. J. Biochem. Cell Biol. 43 2011 732 741
166. A. Relini, N. Marano, and A. Gliozzi Probing the interplay between amyloidogenic proteins and membranes using lipid monolayers and bilayers Adv. Colloid Interf. Sci. 207 2014 81 92
167. S. Pope, J.M. Land, and S.J. Heales Oxidative stress and mitochondrial dysfunction in neurodegeneration; cardiolipin a critical target? Biochim. Biophys. Acta 2008 1777 794 799
168. M. Lutter, M. Fang, X. Luo, M. Nishijima, X. Xie, and X. Wang Cardiolipin provides specificity for targeting of tBid to mitochondria Nat. Cell Biol. 2 2000 754 761
169. F. Gonzalvez, F. Pariselli, O. Jalmar, P. Dupaigne, F. Sureau, M. Dellinger, and et al. Mechanistic issues of the interaction of the hairpin-forming domain of tBid with mitochondrial cardiolipin PLoS ONE 5 2010 e9342
170. E. Raemy, and J.C. Martinou Involvement of cardiolipin in tBID-induced activation of BAX during apoptosis Chem. Phys. Lipids 179 2014 70 74
171. H. Jin, A. Kanthasamy, A. Ghosh, V. Anantharam, B. Kalyanaraman, and A.G. Kanthasamy Mitochondria-targeted antioxidants for treatment of Parkinson's disease: preclinical and clinical outcomes Biochim. Biophys. Acta 2014 1842 1282 1294
172. J. Wagner, S. Ryazanov, A. Leonov, J. Levin, S. Shi, F. Schmidt, and et al. Anle138b: a novel oligomer modulator for disease-modifying therapy of neurodegenerative diseases such as prion and Parkinson's disease Acta Neuropathol. 125 2013 795 813
173. A.V. Birk, S. Liu, Y. Soong, W. Mills, P. Singh, J.D. Warren, and et al. The mitochondrial-targeted compound SS-31 re-energizes ischemic mitochondria by interacting with cardiolipin J. Am. Soc. Nephrol. 24 2013 1250 1261