What does make an amyloid toxic: Morphology, structure or interaction with membrane?

Biochimie

Volumn 95, Issue 1, 2013, Pages 12-19

  Berthelot, Karine ^a   Cullin, Christophe ^b   Lecomte, Sophie ^c  

^a UNIVERSITÉ BORDEAUX 1   (France)

^b Institut de Biochimie et Genetique Cellulaires   (France)

^c CNRS   (France)

Author keywords

Amyloid; Antiparallel sheet; Membrane; Oligomers; Toxicity

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PROTEIN; LYSOZYME; MEMBRANE LIPID; OLIGOMER; PRION PROTEIN; PROTEASOME;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID TOXICITY; APOPTOSIS; ATOMIC FORCE MICROSCOPY; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; CELLULAR DISTRIBUTION; GENE MUTATION; HUMAN; IN VITRO STUDY; MEMBRANE STRUCTURE; MORPHOLOGY; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRION DISEASE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; TOXICITY; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR AMYLOIDOSIS; X RAY DIFFRACTION;

EID: 84870565641     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.07.011     Document Type: Short Survey

References (60)

1. R. Virchow Ueber eine im Gehirn und Ruckenmark des Menschen aufgefundene Substanz mit der chemischen Reaktin der Cellulose Virchows Arch. Path. Anat. 6 1853 135
2. K.L. Morris, and L.C. Serpell X-ray fibre diffraction studies of amyloid fibrils E.M. Sigurdsson, Amyloid Proteins: Methods and Protocols, Methods in Molecular Biology 2012 121 135
3. E.J. Bennett, T.A. Shaler, B. Woodman, K.Y. Ryu, T.S. Zaitseva, C.H. Becker, G.P. Bates, H. Schulman, and R.R. Kopito Global changes to the ubiquitin system in Huntington's disease Nature 448 2007 704 708
4. J.T. Jarrett, and P.J. Lansbury Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73 1993 1055 1058
5. T.R. Serio, A.G. Cashikar, A.S. Kowal, G.J. Sawicki, J.J. Moslehi, L.C. Serpell, M.F. Arnsdorf, and S.L. Lindquist Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289 2000 1317 1321
6. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699
7. S.K. Maji, M.H. Perrin, M.R. Sawaya, S. Jessberger, K. Vadodaria, R.A. Rissman, P.S. Singru, K.P.R. Nilsson, R. Simon, D. Schubert, D. Eisenberg, J. Rivier, P. Sawchenko, W. Vale, and R. Riek Functional amyloids as natural storage of peptide hormones in pituitary secretory granules Science 325 2009 328 332
8. R. Halfmann, S. Alberti, and S. Lindquist Prions, protein homeostasis, and phenotypic diversity Trends Cell. Biol. 20 2010 125 133
9. C. Haass, and D.J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell. Biol. 8 2007 101 112
10. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
11. J.C. Stroud, C. Liu, P. Teng, and D. Eisenberg Toxic fibrillar oligomers of amyloid-β have cross-β structure Proc. Natl. Acad. Sci. U.S.A. 109 2012 7717 7722
12. C. Zhang, A.P. Jackson, Z.R. Zhang, Y. Han, S. Yu, R. He, and S. Perrett Amyloid-like aggregates of the yeast prion protein ure2 enter vertebrate cells by specific endocytosis pathways and induce apoptosis PLoS One 5 9 2010 e12529
13. J. Couthouis, K. Rébora, F. Immel, K. Berthelot, M. Castroviejo, and C. Cullin Screening for toxic amyloid in yeast exemplifies the role of alternative pathway responsible for cytotoxicity PLoS One 4 2009 e4539
14. K. Berthelot, H.P. Ta, J. Géan, S. Lecomte, and C. Cullin In vivo and In vitro analyses of toxic mutants of HET-s: FTIR antiparallel signature Correlates with amyloid toxicity J. Mol. Biol. 412 2011 137 152
15. V. Coustou, C. Deleu, S. Saupe, and J. Begueret The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog Proc. Natl. Acad. Sci. U.S.A. 94 1997 9773 9778
16. C. Wasmer, A. Lange, H. Van Melckebeke, A.B. Siemer, B. Riek, and H. Meier Amyloid fibrils of the HET-s(218-289) prion form a β soleinoid with a triangle hydrophobic core Science 319 2008 1523 1526
17. K. Berthelot, F. Immel, J. Géan, S. Lecomte, R. Oda, B. Kauffmann, and C. Cullin Driving amyloid toxicity in a yeast model by structural changes: a molecular approach FASEB J. 23 2009 2254 2263
18. Y. Nagai, T. Inui, H.A. Popiel, N. Fujikake, K. Hasegawa, Y. Urade, Y. Goto, H. Naiki, and T. Toda A toxic monomeric conformer of the polyglutamine protein Nat. Struct. Mol. Biol. 14 2007 332 340
19. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, N. Taddei, G. Ramponi, C.M. Dobson, and M. Stefani Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511
20. R. Kayed, A. Pensalfini, L. Margol, Y. Sokolov, F. Sarsoza, E. Head, J. Hall, and C. Glabe Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer J. Biol. Chem. 284 2009 4230 4237
21. A.T. Petkova, R.D. Leapman, Z. Guo, W.M. Yau, M.P. Mattson, and R. Tycko Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils Science 307 2005 262 265
22. W.F. Xue, A.L. Hellewell, W.S. Gosal, S.W. Homans, E.W. Hewitt, and S.E. Radford Fibril fragmentation enhances amyloid cytotoxicity J. Biol. Chem. 284 2009 34272 34282
23. A. Jan, O. Adolfsson, I. Allaman, A.-L. Buccarello, P.J. Magistretti, A. Pfeifer, A. Muhs, and H.A. Lashuel Aβ42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Aβ42 species J. Biol. Chem. 286 2011 8585 8596
24. K. Berthelot, S. Lecomte, J. Géan, F. Immel, and C. Cullin A yeast toxic mutant of HET-s(218-289) prion displays alternative intermediate of amyloidogenesis Biophys. J. 99 2010 1239 1246
25. Y.N. Chirgadze, and N.A. Nevskaya Infrared spectra and resonance interaction of amide-I vibration of the antiparallel-chain pleated sheet Biopolymers 15 1976 607 625
26. Y.N. Chirgadze, and N.A. Nevskaya Infrared spectra and resonance interaction of amide-I vibration of the parallel-chain pleated sheet Biopolymers 15 1976 627 636
27. R.B. Wickner, H.K. Edskes, D. Kryndushkin, R. McGlinchey, D. Bateman, and A. Kelly Prion diseases of yeast: amyloid structure and biology Semi. Cell. Develop. Biol. 22 2011 469 475
28. P.T.J. Lansbury, P.R. Costa, J.M. Griffiths, E.J. Simon, M. Auger, K.J. Halverson, D.A. Kocisko, Z.S. Hendsch, T.T. Ashburn, R.G.S. Spencer, B. Tidor, and R.G. Griffin Structural model for the β-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide Nature 1995 990 998
29. M.R. Sawaya, S. Sambashivan, R. Nelson, M.I. Ivanova, S.A. Sievers, M.I. Apostol, M.J. Thompson, M. Balbirnie, J.J.W. Wiltzius, H.T. McFarlane, A. Madsen, C. Riekel, and D. Eisenberg Atomic structures of amyloid cross-b spines reveal varied steric zippers Nature 447 2007 453 457
30. G. Habicht, C. Haupt, R.P. Friedrich, P. Hortschansky, C. Sachse, J. Meinhardt, K. Wieligmann, G.P. Gellermann, M. Brodhun, J. Götz, K.-J. Halbhuber, C. Röcken, U. Horn, and M. Frändrich Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Aβ protofibrils Proc. Natl. Acad. Sci. U.S.A. 104 2007 19232 19237
31. E. Cerf, R. Sarroukh, S. Tamamizu-Kato, L. Breydo, S. Derclaye, Y.F. Dufrêne, V. Narayanaswami, E. Goormaghtigh, J.-M. Ruysschaert, and V. Raussens Antiparallel beta-sheet: a signature of the oligomeric amyloid beta-peptide Biochem. J. 421 2009 415 423
32. M.S. Celej, R. Sarroukh, E. Goormaghtigh, G.D. Fidelio, J.-M. Ruysschaert, and V. Raussens Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure Biochem. J. 443 2012 719 726
33. E. Frare, M.F. Mossuto, P. Polverino de Laureto, S. Tolin, L. Menzer, M. Dumoulin, C.M. Dobson, and A. Fontana Characterization of oligomeric species on the aggregation pathway of human lysozyme J. Mol. Biol. 387 2009 17 27
34. A. Natalello, V.V. Prokorov, F. Tagliavini, M. Morbin, G. Forloni, M. Beeg, C. Manzoni, L. Colombo, M. Gobbi, M. Salmona, and S.L. Doglia Conformational plasticity of the Gerstmann-Sträussler-Scheinker disease peptide as indicated by its multiple aggregation pathways J. Mol. Biol. 381 2008 1349 1361
35. K. Ono, M.M. Condrona, and D.B. Teplowa Structure-neurotoxicity relationships of amyloid beta-protein oligomers Proc. Natl. Acad. Sci. U.S.A. 106 2009 14745 14750
36. A.P. Minton Implications of macromolecular crowding for protein assembly Curr. Opin. Struct. Biol. 10 2000 34 39
37. A. Laganowsky, C. Liu, M.R. Sawaya, J.P. Whitelegge, J. Park, M. Zhao, A. Pensalfini, A.B. Soriaga, M. Landau, P. Teng, D. Cascio, C. Glabe, and D. Eisenberg Atomic view of a toxic amyloid small oligomer Science 335 2012 1227 1231
38. K.C. Chou, M. Pottle, G. Némethy, Y. Ueda, and H.A. Scheraga Structure of beta-sheets. Origin of the right-handed twist and of the increased stability of antiparallel over parallel sheets J. Mol. Biol. 162 1982 82 112
39. M. Necula, C.N. Chirita, and J. Kuret Rapid anionic micelle-mediated α-synuclein fibrillization in vitro J. Biol. Chem. 278 2003 46674 46680
40. J.D. Knight, and A.D. Miranker Phospholipid catalysis of diabetic amyloid assembly J. Mol. Biol. 341 2004 1175 1187
41. L.P. Choo-Smith, W. Garzon-Rodriguez, C.G. Glabe, and W.K. Surewicz Acceleration of amyloid fibril formation by specific binding of Abeta-(1-40) peptide to ganglioside-containing membrane vesicles J. Biol. Chem. 272 1997 22987 22990
42. R. Sabaté, M. Gallardo, and J. Estelrich Spontaneous incorporation of β-amyloid peptide into neutral liposomes Colloids Surf. A 270-271 2005 13 17
43. H.P. Ta, K. Berthelot, B. Coulary-Salin, S. Castano, B. Desbat, P. Bonnafous, O. Lambert, I. Alves, C. Cullin, and S. Lecomte A yeast toxic mutant of HET-s amyloid disrupts membrane integrity Biochim. Biophys. Acta Biomembrane 1818 2012 2325 2334
44. H.P. Ta, K. Berthelot, B. Coulary-Salin, B. Desbat, J. Géan, L. Servant, C. Cullin, and S. Lecomte Comparative studies of nontoxic and toxic amyloids interacting with membrane models at the air-water interface Langmuir 27 2011 4797 4807
45. 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
46. I.C. Martins, I. Kuperstein, H. Wilkinson, E. Maes, M. Vanbraban, W. Jonckheere, P. Van Gelder, D. Hartmann, R. D'Hooge, B. De Strooper, J. Schymkowitz, and F. Rousseau Lipids revert inert Aβ amyloid fibrils to neurotoxic protofibrils that affect learning in mice EMBO J. 27 2008 224 233
47. Y. Zhang, J.M. Shi, C.J. Cai-Juan Bai, H. Wang, H.Y. Li, Y. Wu, and S.R. Ji Intra-membrane oligomerization and extra-membrane oligomerization of amyloid-β peptide are competing processes as a result of distinct patterns of Motif interplay J. Biol. Chem. 287 2012 748 756
48. J. Couthouis, C. Marchal, F. D'Angelo, K. Berthelot, and C. Cullin The toxicity of an "artificial" amyloid is related to how it interacts with membranes Prion 4 4 2010 283 291
49. M.F. Engel, L. Khemtémourian, C.C. Kleijer, H.J. Meeldijk, J. Jacobs, A.J. Verkleij, B. de Kruijff, J.A. Killian, and J.W.M. Höppener Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane Proc. Natl. Acad. Sci. U.S.A. 105 2008 6033 6038
50. T.L. Williams, and L.C. Serpell Membrane and surface interactions of the Alzheimer's Aβ peptide: insights into the mechanism of cytotoxicity FEBS J. 278 2011 3905 3917
51. S.M. Butterfield, and H.A. Lashuel Amyloidogenic Protein-Membrane interactions: mechanistic insight from model systems Angew. Chem. Int. Ed. 49 2010 5628 5654
52. H.A. Lashuel, and P.T.J. Lansbury Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Quart. Rev. Biophys. 39 2005 167 201
53. G. Bitan, E.A. Frandinger, S.M. Spring, and D.B. Teplow Neurotoxic protein oligomers - what you see is not what you get Amyloid 12 2005 88 95
54. R.P. Friedrich, K. Tepper, R. Ronicke, M. Soon, M. Westermann, K. Reymann, C. Kaether, and M. Fändrich Mechanism of amyloid plaque formation suggests an intracellular basis of Aβ pathogenicity Proc. Natl. Acad. Sci. U.S.A. 107 2010 1942 1947
55. A. Eckert, S. Hauptmann, I. Scherping, J. Meinhardt, V. Rhein, S. Dröse, U. Brandt, M. Fändrich, W.E. Müller, and J. Götz Oligomeric and fibrillar species of β-amyloid (Aβ42) both impair mitochondrial function in P301L tau transgenic mice J. Mol. Med. 86 2008 1255 1267
56. L. Yu, R. Edalji, John E. Harlan, T.F. Holzman, A.P. Lopez, B. Labkovsky, H. Hillen, S. Barghorn, U. Ebert, P.L. Richardson, L. Miesbauer, L. Solomon, D. Bartley, K. Walter, R.W. Johnson, P.J. Hajduk, and E.T. Olejniczak Structural characterization of a soluble amyloid β-peptide oligomer Biochemistry 48 2009 1870 1877
57. D.M. Walsh, I. Klyubin, J.V. Fadeeva, W.K. Cullen, R. Anwyl, M.S. Wolfe, M.J. Rowan, and D.J. Selkoe Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 2002 535 539
58. W. Qiang, W.-M. Yau, Y. Luo, M.P. Mattson, and R. Tycko Antiparallel β-sheet architecture in Iowa-mutant β-amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 109 2012 4443 4448
59. A. Perálvarez-Marín, L. Mateos, C. Zhang, S. Singh, A. Cedazo-Mínguez, N. Visa, L. Morozova-Roche, A. Gräslund, and A. Barth Influence of residue 22 on the folding, aggregation profile, and toxicity of the Alzheimer's amyloid beta peptide Biophys. J. 97 2009 277 285
60. M.F. Mossuto, A. Dhulesia, G. Devlin, E. Frare, J.R. Kumita, P. Polverino de Laureto, M. Dumoulin, A. Fontana, C.M. Dobson, and X. Salvatella The non-core regions of human lysozyme amyloid fibrils influence cytotoxicity J. Mol. Biol. 402 2010 783 796