Mitochondrial membrane permeabilisation by amyloid aggregates and protection by polyphenols

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 11, 2013, Pages 2532-2543

  Camilleri, Angelique ^a   Zarb, Claire ^a   Caruana, Mario ^a   Ostermeier, Ulrike ^a,b   Ghio, Stephanie ^a   Högen, Tobias ^c   Schmidt, Felix ^d   Giese, Armin ^d   Vassallo, Neville ^a  

^a UNIVERSITY OF MALTA   (Malta)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Alpha synuclein; Amyloid beta; Cardiolipin; Mitochondrial membrane; Polyphenol; Tau

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; BLACK TEA EXTRACT; CARDIOLIPIN; CYTOCHROME C; GRAMICIDIN; ION CHANNEL; MUTANT PROTEIN; POLYPHENOL; ROSMARINIC ACID; TAU 441 PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL VACUOLE; CONTROLLED STUDY; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID VESICLE; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MODEL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STRUCTURE; WILD TYPE;

Α-SYN; Α-SYNUCLEIN; AΒ(42); AD; ALPHA-SYNUCLEIN; ALZHEIMER'S DISEASE; AMYLOID-BETA; AMYLOID-BETA (1-42); CARDIOLIPIN; CCR; CL; CYTO C; CYTOCHROME C; CYTOCHROME C RELEASE; IM AND IMM; INNER MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE; OGB-1; OM AND OMM; OREGON GREEN® 488 BAPTA-1; OUTER MITOCHONDRIAL MEMBRANE; PARKINSON'S DISEASE; PD; POLYPHENOL; TAU; TRITON X-100; TX-100; WILD-TYPE; WT;

ALPHA-SYNUCLEIN; AMYLOID BETA-PEPTIDES; CELL LINE, TUMOR; HUMANS; MITOCHONDRIAL MEMBRANES; PERMEABILITY; POLYPHENOLS; RECOMBINANT PROTEINS; TAU PROTEINS;

EID: 84882665148     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.06.026     Document Type: Article

References (112)

1. C. Soto Unfolding the role of protein misfolding in neurodegenerative diseases Nat. Rev. Neurosci. 4 2003 49 60
2. D.J. Selkoe Alzheimer's disease Cold Spring Harb. Perspect. Biol. 3 2011
3. O. Wirths, and T.A. Bayer Intraneuronal Abeta accumulation and neurodegeneration: lessons from transgenic models Life Sci. 91 2012 1148 1152
4. L.M. Ittner, and J. Gotz Amyloid-beta and tau - a toxic pas de deux in Alzheimer's disease Nat. Rev. Neurosci. 12 2011 65 72
5. M.G. Spillantini, R.A. Crowther, R. Jakes, M. Hasegawa, and M. Goedert Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies Proc. Natl. Acad. Sci. U. S. A. 95 1998 6469 6473
6. M. Goedert Alpha-synuclein and neurodegenerative diseases Nat. Rev. Neurosci. 2 2001 492 501
7. R. Kruger Genes in familial parkinsonism and their role in sporadic Parkinson's disease J. Neurol. 251 Suppl. 6 2004 VI/2 VI/6
8. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
9. F. Rahimi, A. Shanmugam, and G. Bitan Structure-function relationships of pre-fibrillar protein assemblies in Alzheimer's disease and related disorders Curr. Alzheimer Res. 5 2008 319 341
10. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, M.J. Guerrero-Muoz, G.R. Jackson, and R. Kayed Preparation and characterization of neurotoxic tau oligomers Biochemistry 49 2010 10039 10041
11. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, J. Sarmiento, J. Troncoso, G.R. Jackson, and R. Kayed Identification of oligomers at early stages of tau aggregation in Alzheimer's disease FASEB J. 26 2012 1946 1959
12. C.G. Glabe Structural classification of toxic amyloid oligomers J. Biol. Chem. 283 2008 29639 29643
13. D.P. Karpinar, M.B. Balija, S. Kugler, F. Opazo, N. Rezaei-Ghaleh, N. Wender, H.Y. Kim, G. Taschenberger, B.H. Falkenburger, H. Heise, A. Kumar, D. Riedel, L. Fichtner, A. Voigt, G.H. Braus, K. Giller, S. Becker, A. Herzig, M. Baldus, H. Jackle, S. Eimer, J.B. Schulz, C. Griesinger, and M. Zweckstetter Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models EMBO J. 28 2009 3256 3268
14. R.M. Koffie, M. Meyer-Luehmann, T. Hashimoto, K.W. Adams, M.L. Mielke, M. Garcia-Alloza, K.D. Micheva, S.J. Smith, M.L. Kim, V.M. Lee, B.T. Hyman, and T.L. Spires-Jones Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques Proc. Natl. Acad. Sci. U. S. A. 106 2009 4012 4017
15. B. Winner, R. Jappelli, S.K. Maji, P.A. Desplats, L. Boyer, S. Aigner, C. Hetzer, T. Loher, M. Vilar, S. Campioni, C. Tzitzilonis, A. Soragni, S. Jessberger, H. Mira, A. Consiglio, E. Pham, E. Masliah, F.H. Gage, and R. Riek In vivo demonstration that alpha-synuclein oligomers are toxic Proc. Natl. Acad. Sci. U. S. A. 108 2011 4194 4199
16. M. Bucciantini, G. Calloni, F. Chiti, L. Formigli, D. Nosi, C.M. Dobson, and M. Stefani Prefibrillar amyloid protein aggregates share common features of cytotoxicity J. Biol. Chem. 279 2004 31374 31382
17. 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
18. K.M. Danzer, D. Haasen, A.R. Karow, S. Moussaud, M. Habeck, A. Giese, H. Kretzschmar, B. Hengerer, and M. Kostka Different species of alpha-synuclein oligomers induce calcium influx and seeding J. Neurosci. 27 2007 9220 9232
19. M. Kawahara Neurotoxicity of beta-amyloid protein: oligomerization, channel formation, and calcium dyshomeostasis Curr. Pharm. Des. 16 2010 2779 2789
20. M.F. Sciacca, S.A. Kotler, J.R. Brender, J. Chen, D.K. Lee, and A. Ramamoorthy Two-step mechanism of membrane disruption by Abeta through membrane fragmentation and pore formation Biophys. J. 103 2012 702 710
21. P. Prangkio, E.C. Yusko, D. Sept, J. Yang, and M. Mayer Multivariate analyses of amyloid-beta oligomer populations indicate a connection between pore formation and cytotoxicity PLoS One 7 2012 e47261
22. 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
23. B.D. van Rooijen, M.M. Claessens, and V. Subramaniam Membrane permeabilization by oligomeric alpha-synuclein: in search of the mechanism PLoS One 5 2010 e14292
24. 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
25. K. Flach, I. Hilbrich, A. Schiffmann, U. Gartner, M. Kruger, M. Leonhardt, H. Waschipky, L. Wick, T. Arendt, and M. Holzer Tau oligomers impair artificial membrane integrity and cellular viability J. Biol. Chem. 287 2012 43223 43233
26. M.T. Lin, and M.F. Beal Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795
27. M.S. Parihar, and G.J. Brewer Mitoenergetic failure in Alzheimer disease Am. J. Physiol. Cell Physiol. 292 2007 C8 C23
28. A.H. Schapira Complex I: inhibitors, inhibition and neurodegeneration Exp. Neurol. 224 2010 331 335
29. S.C. Correia, R.X. Santos, G. Perry, X. Zhu, P.I. Moreira, and M.A. Smith Mitochondrial importance in Alzheimer's, Huntington's and Parkinson's diseases Adv. Exp. Med. Biol. 724 2012 205 221
30. T.E. Gunter, K.K. Gunter, S.S. Sheu, and C.E. Gavin Mitochondrial calcium transport: physiological and pathological relevance Am. J. Physiol. 267 1994 C313 C339
31. 2 + overload underlies Abeta oligomers neurotoxicity providing an unexpected mechanism of neuroprotection by NSAIDs PLoS One 3 2008 e2718
32. M. Vila, and S. Przedborski Targeting programmed cell death in neurodegenerative diseases Nat. Rev. Neurosci. 4 2003 365 375
33. J.E. Chipuk, L. Bouchier-Hayes, and D.R. Green Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario Cell Death Differ. 13 2006 1396 1402
34. R. Clayton, J.B. Clark, and M. Sharpe Cytochrome c release from rat brain mitochondria is proportional to the mitochondrial functional deficit: implications for apoptosis and neurodegenerative disease J. Neurochem. 92 2005 840 849
35. J.W. Lustbader, M. Cirilli, C. Lin, H.W. Xu, K. Takuma, N. Wang, C. Caspersen, X. Chen, S. Pollak, M. Chaney, F. Trinchese, S. Liu, F. Gunn-Moore, L.F. Lue, D.G. Walker, P. Kuppusamy, Z.L. Zewier, O. Arancio, D. Stern, S.S. Yan, and H. Wu ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease Science 304 2004 448 452
36. C.A. Hansson Petersen, N. Alikhani, H. Behbahani, B. Wiehager, P.F. Pavlov, I. Alafuzoff, V. Leinonen, A. Ito, B. Winblad, E. Glaser, and M. Ankarcrona The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae Proc. Natl. Acad. Sci. U. S. A. 105 2008 13145 13150
37. X. Wang, B. Su, G. Perry, M.A. Smith, and X. Zhu Insights into amyloid-beta-induced mitochondrial dysfunction in Alzheimer disease Free Radic. Biol. Med. 43 2007 1569 1573
38. H. Seelert, D.N. Dani, S. Dante, T. Hauss, F. Krause, E. Schafer, M. Frenzel, A. Poetsch, S. Rexroth, H.J. Schwassmann, T. Suhai, J. Vonck, and N.A. Dencher From protons to OXPHOS supercomplexes and Alzheimer's disease: structure-dynamics-function relationships of energy-transducing membranes Biochim. Biophys. Acta 1787 2009 657 671
39. K.E. Muirhead, E. Borger, L. Aitken, S.J. Conway, and F.J. Gunn-Moore The consequences of mitochondrial amyloid beta-peptide in Alzheimer's disease Biochem. J. 426 2010 255 270
40. L. Pagani, and A. Eckert Amyloid-beta interaction with mitochondria Int. J. Alzheimers Dis. 2011 2011 925050
41. P.H. Reddy Is the mitochondrial outermembrane protein VDAC1 therapeutic target for Alzheimer's disease? Biochim. Biophys. Acta 1832 2013 67 75
42. M.Y. Cha, S.H. Han, S.M. Son, H.S. Hong, Y.J. Choi, J. Byun, and I. Mook-Jung Mitochondria-specific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death PLoS One 7 2012 e34929
43. P.F. Pavlov, B. Wiehager, J. Sakai, S. Frykman, H. Behbahani, B. Winblad, and M. Ankarcrona Mitochondrial gamma-secretase participates in the metabolism of mitochondria-associated amyloid precursor protein FASEB J. 25 2011 78 88
44. P.J. Crouch, R. Blake, J.A. Duce, G.D. Ciccotosto, Q.X. Li, K.J. Barnham, C.C. Curtain, R.A. Cherny, R. Cappai, T. Dyrks, C.L. Masters, and I.A. Trounce Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42 J. Neurosci. 25 2005 672 679
45. M. Manczak, T.S. Anekonda, E. Henson, B.S. Park, J. Quinn, and P.H. Reddy Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression Hum. Mol. Genet. 15 2006 1437 1449
46. C. Caspersen, N. Wang, J. Yao, A. Sosunov, X. Chen, J.W. Lustbader, H.W. Xu, D. Stern, G. McKhann, and S.D. Yan Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease FASEB J. 19 2005 2040 2041
47. H. Du, L. Guo, F. Fang, D. Chen, A.A. Sosunov, G.M. McKhann, Y. Yan, C. Wang, H. Zhang, J.D. Molkentin, F.J. Gunn-Moore, J.P. Vonsattel, O. Arancio, J.X. Chen, and S.D. Yan Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease Nat. Med. 14 2008 1097 1105
48. K. Leuner, T. Schutt, C. Kurz, S.H. Eckert, C. Schiller, A. Occhipinti, S. Mai, M. Jendrach, G.P. Eckert, S.E. Kruse, R.D. Palmiter, U. Brandt, S. Drose, I. Wittig, M. Willem, C. Haass, A.S. Reichert, and W.E. Muller Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation Antioxid. Redox Signal. 16 2012 1421 1433
49. F. Gillardon, W. Rist, L. Kussmaul, J. Vogel, M. Berg, K. Danzer, N. Kraut, and B. Hengerer Proteomic and functional alterations in brain mitochondria from Tg2576 mice occur before amyloid plaque deposition Proteomics 7 2007 605 616
50. H. Du, L. Guo, S. Yan, A.A. Sosunov, G.M. McKhann, and S.S. Yan Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model Proc. Natl. Acad. Sci. U. S. A. 107 2010 18670 18675
51. V. Rhein, X. Song, A. Wiesner, L.M. Ittner, G. Baysang, F. Meier, L. Ozmen, H. Bluethmann, S. Drose, U. Brandt, E. Savaskan, C. Czech, J. Gotz, and A. Eckert Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice Proc. Natl. Acad. Sci. U. S. A. 106 2009 20057 20062
52. R.A. Quintanilla, P.J. Dolan, Y.N. Jin, and G.V. Johnson Truncated tau and Abeta cooperatively impair mitochondria in primary neurons Neurobiol. Aging 33 2012 619e625 619e635
53. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, A.L. Clos, G.R. Jackson, and R. Kayed Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice Mol. Neurodegener. 6 2011 39
54. J. Zhu, and C.T. Chu Mitochondrial dysfunction in Parkinson's disease J. Alzheimers Dis. 20 Suppl. 2 2010 S325 S334
55. N. Exner, A.K. Lutz, C. Haass, and K.F. Winklhofer Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences EMBO J. 31 2012 3038 3062
56. W.W. Li, R. Yang, J.C. Guo, H.M. Ren, X.L. Zha, J.S. Cheng, and D.F. Cai Localization of alpha-synuclein to mitochondria within midbrain of mice NeuroReport 18 2007 1543 1546
57. 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. 28 2008 12305 12317
58. L. Zhang, C. Zhang, Y. Zhu, Q. Cai, P. Chan, K. Ueda, S. Yu, and H. Yang Semi-quantitative analysis of alpha-synuclein in subcellular pools of rat brain neurons: an immunogold electron microscopic study using a C-terminal specific monoclonal antibody Brain Res. 1244 2008 40 52
59. 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
60. 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
61. W. Dauer, N. Kholodilov, M. Vila, A.C. Trillat, R. Goodchild, K.E. Larsen, R. Staal, K. Tieu, Y. Schmitz, C.A. Yuan, M. Rocha, V. Jackson-Lewis, S. Hersch, D. Sulzer, S. Przedborski, R. Burke, and R. Hen Resistance of alpha-synuclein null mice to the parkinsonian neurotoxin MPTP Proc. Natl. Acad. Sci. U. S. A. 99 2002 14524 14529
62. L.J. Martin, Y. Pan, A.C. Price, W. Sterling, N.G. Copeland, N.A. Jenkins, D.L. Price, and M.K. Lee Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death J. Neurosci. 26 2006 41 50
63. K. Nakamura, V.M. Nemani, F. Azarbal, G. Skibinski, J.M. Levy, K. Egami, L. Munishkina, J. Zhang, B. Gardner, J. Wakabayashi, H. Sesaki, Y. Cheng, S. Finkbeiner, R.L. Nussbaum, E. Masliah, and R.H. Edwards Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein J. Biol. Chem. 286 2011 20710 20726
64. A.J. Gauci, M. Caruana, A. Giese, C. Scerri, and N. Vassallo Identification of polyphenolic compounds and black tea extract as potent inhibitors of lipid membrane destabilization by Abeta aggregates J. Alzheimers Dis. 27 2011 767 779
65. M. Caruana, J. Neuner, T. Hogen, F. Schmidt, F. Kamp, C. Scerri, A. Giese, and N. Vassallo Polyphenolic compounds are novel protective agents against lipid membrane damage by alpha-synuclein aggregates in vitro Biochim. Biophys. Acta 1818 2012 2502 2510
66. S. Schaffer, H. Asseburg, S. Kuntz, W.E. Muller, and G.P. Eckert Effects of polyphenols on brain ageing and Alzheimer's disease: focus on mitochondria Mol. Neurobiol. 46 2012 161 178
67. N. Vassallo, and C. Scerri Mediterranean diet and dementia of the Alzheimer type Curr. Aging Sci. 2012 10.2174/10001 (Electronic publication ahead of print)
68. X. Gao, A. Cassidy, M.A. Schwarzschild, E.B. Rimm, and A. Ascherio Habitual intake of dietary flavonoids and risk of Parkinson disease Neurology 78 2012 1138 1145
69. R.F. Epand, J.C. Martinou, S. Montessuit, R.M. Epand, and C.M. Yip Direct evidence for membrane pore formation by the apoptotic protein Bax Biochem. Biophys. Res. Commun. 298 2002 744 749
70. B. Nuscher, F. Kamp, T. Mehnert, S. Odoy, C. Haass, P.J. Kahle, and K. Beyer Alpha-synuclein has a high affinity for packing defects in a bilayer membrane: a thermodynamics study J. Biol. Chem. 279 2004 21966 21975
71. M. Necula, R. Kayed, S. Milton, and C.G. Glabe Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct J. Biol. Chem. 282 2007 10311 10324
72. S. Huls, T. Hogen, N. Vassallo, K.M. Danzer, B. Hengerer, A. Giese, and J. Herms AMPA-receptor-mediated excitatory synaptic transmission is enhanced by iron-induced alpha-synuclein oligomers J. Neurochem. 117 2011 868 878
73. B. Bader, G. Nubling, A. Mehle, S. Nobile, H. Kretzschmar, and A. Giese Single particle analysis of tau oligomer formation induced by metal ions and organic solvents Biochem. Biophys. Res. Commun. 411 2011 190 196
74. 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
75. V. Kozjak-Pavlovic, E.A. Dian-Lothrop, M. Meinecke, O. Kepp, K. Ross, K. Rajalingam, A. Harsman, E. Hauf, V. Brinkmann, D. Gunther, I. Herrmann, R. Hurwitz, J. Rassow, R. Wagner, and T. Rudel Bacterial porin disrupts mitochondrial membrane potential and sensitizes host cells to apoptosis PLoS Pathog. 5 2009 e1000629
76. M. Ott, J.D. Robertson, V. Gogvadze, B. Zhivotovsky, and S. Orrenius Cytochrome c release from mitochondria proceeds by a two-step process Proc. Natl. Acad. Sci. U. S. A. 99 2002 1259 1263
77. P.X. Petit, M. Goubern, P. Diolez, S.A. Susin, N. Zamzami, and G. Kroemer Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition FEBS Lett. 426 1998 111 116
78. A.W. Leung, and A.P. Halestrap Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore Biochim. Biophys. Acta 1777 2008 946 952
79. H.S. Kim, J.H. Lee, J.P. Lee, E.M. Kim, K.A. Chang, C.H. Park, S.J. Jeong, M.C. Wittendorp, J.H. Seo, S.H. Choi, and Y.H. Suh Amyloid beta peptide induces cytochrome C release from isolated mitochondria NeuroReport 13 2002 1989 1993
80. M. Sinha, P. Behera, P. Bhowmick, K. Banerjee, S. Basu, and S. Chakrabarti Aging promotes amyloid-beta peptide induced mitochondrial dysfunctions in rat brain: a molecular link between aging and Alzheimer's disease J. Alzheimers Dis. 27 2011 753 765
81. T. Umeda, T. Tomiyama, N. Sakama, S. Tanaka, M.P. Lambert, W.L. Klein, and H. Mori Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo J. Neurosci. Res. 89 2011 1031 1042
82. K. Banerjee, M. Sinha, L. Pham Cle, S. Jana, D. Chanda, R. Cappai, and S. Chakrabarti 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
83. M. Hartmann, M. Berditsch, J. Hawecker, M.F. Ardakani, D. Gerthsen, and A.S. Ulrich Damage of the bacterial cell envelope by antimicrobial peptides gramicidin S and PGLa as revealed by transmission and scanning electron microscopy Antimicrob. Agents Chemother. 54 2010 3132 3142
84. C.W. Bertoncini, C.O. Fernandez, C. Griesinger, T.M. Jovin, and M. Zweckstetter Familial mutants of alpha-synuclein with increased neurotoxicity have a destabilized conformation J. Biol. Chem. 280 2005 30649 30652
85. E. Giannakis, J. Pacifico, D.P. Smith, L.W. Hung, C.L. Masters, R. Cappai, J.D. Wade, and K.J. Barnham Dimeric structures of alpha-synuclein bind preferentially to lipid membranes Biochim. Biophys. Acta 1778 2008 1112 1119
86. 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
87. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
88. T.T. Yang, C.T. Hsu, and Y.M. Kuo Cell-derived soluble oligomers of human amyloid-beta peptides disturb cellular homeostasis and induce apoptosis in primary hippocampal neurons J. Neural Transm. 116 2009 1561 1569
89. S.R. Slone, M. Lesort, and T.A. Yacoubian 14-3-3Theta protects against neurotoxicity in a cellular Parkinson's disease model through inhibition of the apoptotic factor Bax PLoS One 6 2011 e21720
90. B.D. van Rooijen, M.M. Claessens, and V. Subramaniam Lipid bilayer disruption by oligomeric alpha-synuclein depends on bilayer charge and accessibility of the hydrophobic core Biochim. Biophys. Acta 1788 2009 1271 1278
91. 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 1818 2012 512 519
92. A. Chauhan, I. Ray, and V.P. Chauhan Interaction of amyloid beta-protein with anionic phospholipids: possible involvement of Lys28 and C-terminus aliphatic amino acids Neurochem. Res. 25 2000 423 429
93. Z.T. Schug, and E. Gottlieb Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis Biochim. Biophys. Acta 1788 2009 2022 2031
94. T. Kuwana, M.R. Mackey, G. Perkins, M.H. Ellisman, M. Latterich, R. Schneiter, D.R. Green, and D.D. Newmeyer Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane Cell 111 2002 331 342
95. A. Muller, D. Gunther, V. Brinkmann, R. Hurwitz, T.F. Meyer, and T. Rudel Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells EMBO J. 19 2000 5332 5343
96. P. Matarrese, L. Falzano, A. Fabbri, L. Gambardella, C. Frank, B. Geny, M.R. Popoff, W. Malorni, and C. Fiorentini Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels J. Biol. Chem. 282 2007 9029 9041
97. G. Domanska, C. Motz, M. Meinecke, A. Harsman, P. Papatheodorou, B. Reljic, E.A. Dian-Lothrop, A. Galmiche, O. Kepp, L. Becker, K. Gunnewig, R. Wagner, and J. Rassow Helicobacter pylori VacA toxin/subunit p34: targeting of an anion channel to the inner mitochondrial membrane PLoS Pathog. 6 2010 e1000878
98. B.L. Kagan Membrane pores in the pathogenesis of neurodegenerative disease Prog. Mol. Biol. Transl. Sci. 107 2012 295 325
99. G. Grelle, A. Otto, M. Lorenz, R.F. Frank, E.E. Wanker, and J. Bieschke Black tea theaflavins inhibit formation of toxic amyloid-beta and alpha-synuclein fibrils Biochemistry 50 2011 10624 10636
100. M. Caruana, T. Hogen, J. Levin, A. Hillmer, A. Giese, and N. Vassallo Inhibition and disaggregation of alpha-synuclein oligomers by natural polyphenolic compounds FEBS Lett. 585 2011 1113 1120
101. S.A. Mandel, T. Amit, O. Weinreb, and M.B. Youdim Understanding the broad-spectrum neuroprotective action profile of green tea polyphenols in aging and neurodegenerative diseases J. Alzheimers Dis. 25 2011 187 208
102. G. Hu, S. Bidel, P. Jousilahti, R. Antikainen, and J. Tuomilehto Coffee and tea consumption and the risk of Parkinson's disease Mov. Disord. 22 2007 2242 2248
103. L.C. Tan, W.P. Koh, J.M. Yuan, R. Wang, W.L. Au, J.H. Tan, E.K. Tan, and M.C. Yu Differential effects of black versus green tea on risk of Parkinson's disease in the Singapore Chinese Health Study Am. J. Epidemiol. 167 2008 553 560
104. O. Fadel, K. El Kirat, and S. Morandat The natural antioxidant rosmarinic acid spontaneously penetrates membranes to inhibit lipid peroxidation in situ Biochim. Biophys. Acta 1808 2011 2973 2980
105. R. Kato, K. Kajiya, H. Tokumoto, S. Kumazawa, and T. Nakayama Affinity of isoflavonoids for lipid bilayers evaluated with liposomal systems Biofactors 19 2003 179 187
106. J.A. Lemkul, and D.R. Bevan Morin inhibits the early stages of amyloid beta-peptide aggregation by altering tertiary and quaternary interactions to produce "off-pathway" structures Biochemistry 51 2012 5990 6009
107. T. Hogen, J. Levin, F. Schmidt, M. Caruana, N. Vassallo, H. Kretzschmar, K. Botzel, F. Kamp, and A. Giese Two different binding modes of alpha-synuclein to lipid vesicles depending on its aggregation state Biophys. J. 102 2012 1646 1655
108. J. Bieschke, J. Russ, R.P. Friedrich, D.E. Ehrnhoefer, H. Wobst, K. Neugebauer, and E.E. Wanker EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity Proc. Natl. Acad. Sci. U. S. A. 107 2010 7710 7715
109. M.F. Engel, C.C. vandenAkker, M. Schleeger, K.P. Velikov, G.H. Koenderink, and M. Bonn The polyphenol EGCG inhibits amyloid formation less efficiently at phospholipid interfaces than in bulk solution J. Am. Chem. Soc. 134 2012 14781 14788
110. A. Smith, B. Giunta, P.C. Bickford, M. Fountain, J. Tan, and R.D. Shytle Nanolipidic particles improve the bioavailability and alpha-secretase inducing ability of epigallocatechin-3-gallate (EGCG) for the treatment of Alzheimer's disease Int. J. Pharm. 389 2010 207 212
111. R.L. Frozza, A. Bernardi, J.B. Hoppe, A.B. Meneghetti, A. Matte, A.M. Battastini, A.R. Pohlmann, S.S. Guterres, and C. Salbego Neuroprotective effects of resveratrol against abeta administration in rats are improved by lipid-core nanocapsules Mol. Neurobiol. 47 2013 1066 1080
112. M.P. Mattson, J.N. Keller, and J.G. Begley Evidence for synaptic