Structural, morphological, and functional diversity of amyloid oligomers

FEBS Letters

Volumn 589, Issue 19, 2015, Pages 2640-2648

  Breydo, Leonid ^a   Uversky, Vladimir N ^a,b,c  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Amyloid fibril; Amyloid oligomer; Cytotoxicity; Protein aggregation; Protein misfolding

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PROTEIN; TAR DNA BINDING PROTEIN; TAU PROTEIN; AMYLOID; PROTEIN AGGREGATE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CYTOTOXICITY; HUMAN; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN CONTENT; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN UNFOLDING; REVIEW; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEINOSIS;

AMYLOID; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING;

EID: 84942292545     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.07.013     Document Type: Review

References (181)

1. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
2. A. Mukherjee, D. Morales-Scheihing, P.C. Butler, and C. Soto Type 2 diabetes as a protein misfolding disease Trends Mol. Med. 21 2015 439 449
3. M. Verma, A. Vats, and V. Taneja Toxic species in amyloid disorders: oligomers or mature fibrils Ann. Indian Acad. Neurol. 18 2015 138 145
4. S.K. Maji, and et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules Science 325 2009 328 332
5. K. Si, S. Lindquist, and E.R. Kandel A neuronal isoform of the aplysia CPEB has prion-like properties Cell 115 2003 879 891
6. C.H. Bailey, E.R. Kandel, and K. Si The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth Neuron 44 2004 49 57
7. K. Si, Y.B. Choi, E. White-Grindley, A. Majumdar, and E.R. Kandel Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation Cell 140 2010 421 435
8. C.G. Glabe Common mechanisms of amyloid oligomer pathogenesis in degenerative disease Neurobiol. Aging 27 2006 570 575
9. M. Jucker, and L.C. Walker Self-propagation of pathogenic protein aggregates in neurodegenerative diseases Nature 501 2013 45 51
10. S.E. Lesne Breaking the code of amyloid-beta oligomers Int. J. Cell Biol. 2013 2013 950783
11. B. O'Nuallain, D.B. Freir, A.J. Nicoll, E. Risse, N. Ferguson, C.E. Herron, J. Collinge, and D.M. Walsh Amyloid beta-protein dimers rapidly form stable synaptotoxic protofibrils J. Neurosci. 30 2010 14411 14419
12. F. Rahimi, and G. Bitan Overview of fibrillar and oligomeric assemblies of amyloidogenic proteins F. Rahimi, G. Bitan, Non-fi brillar Amyloidogenic Protein Assemblies - Common Cytotoxins Underlying Degenerative Diseases 2012 Springer 1 37
13. A. Frydman-Marom, Y. Bram, and E. Gazit Preparation and structural characterization of pre-fibrillar assemblies of amyloidogenic proteins F. Rahimi, G. Bitan, Non-fi brillar Amyloidogenic Protein Assemblies - Common Cytotoxins Underlying Degenerative Diseases 2012 Springer 1 37
14. D. Huang, M.I. Zimmerman, P.K. Martin, A.J. Nix, T.L. Rosenberry, and A.K. Paravastu Antiparallel beta-sheet structure within the C-terminal region of 42-residue Alzheimer's beta-amyloid peptides when they form 150 kDa oligomers J. Mol. Biol. 427 2015 2319 2328
15. A. Laganowsky, and et al. Atomic view of a toxic amyloid small oligomer Science 335 2012 1228 1231
16. E. Cerf, and et al. Antiparallel beta-sheet: a signature structure of the oligomeric amyloid beta-peptide Biochem. J. 421 2009 415 423
17. 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
18. W.M. Tay, D. Huang, T.L. Rosenberry, and A.K. Paravastu The Alzheimer's amyloid-beta(1-42) peptide forms off-pathway oligomers and fibrils that are distinguished structurally by intermolecular organization J. Mol. Biol. 425 2013 2494 2508
19. B.H. Meier, and A. Bockmann The structure of fibrils from 'misfolded' proteins Curr. Opin. Struct. Biol. 30 2015 43 49
20. P.J. Davis, D. Holmes, J.P. Waltho, and R.A. Staniforth Limited proteolysis reveals that amyloids from the 3D domain-swapping cystatin b have a non-native beta-sheet topology J. Mol. Biol. 2015 (in press)
21. Breydo, L., Uversky, V.N., 2014. Molecular mechanisms of protein misfolding. In: Uversky, V.N., Lyubchenko, Y.L. (Eds), Bionanoimaging in Protein Misfolding and Aggregation.
22. I. Benilova, E. Karran, and B. De Strooper The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes Nat. Neurosci. 15 2012 349 357
23. G.M. Shankar, and et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14 2008 837 842
24. M. Jin, N. Shepardson, T. Yang, G. Chen, D. Walsh, and D.J. Selkoe Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration Proc. Natl. Acad. Sci. U.S.A. 108 2011 5819 5824
25. M.N. Reed, and et al. Cognitive effects of cell-derived and synthetically derived Abeta oligomers Neurobiol. Aging 32 2011 1784 1794
26. K. Ono, M.M. Condron, and D.B. Teplow Structure-neurotoxicity relationships of amyloid beta-protein oligomers Proc. Natl. Acad. Sci. U.S.A. 106 2009 14745 14750
27. B. Ma, and R. Nussinov Polymorphic C-terminal beta-sheet interactions determine the formation of fibril or amyloid beta-derived diffusible ligand-like globulomer for the alzheimer A{beta}42 dodecamer J. Biol. Chem. 285 2010 37102 37110
28. J.W. Wu, L. Breydo, J.M. Isas, J. Lee, Y.G. Kuznetsov, R. Langen, and C. Glabe Fibrillar oligomers nucleate the oligomerization of monomeric amyloid beta but do not seed fibril formation J. Biol. Chem. 285 2010 6071 6079
29. 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
30. C.A. Lasagna-Reeves, C.G. Glabe, and R. Kayed Amyloid-beta annular protofibrils evade fibrillar fate in Alzheimer disease brain J. Biol. Chem. 286 2011 22122 22130
31. D.E. Ehrnhoefer, and et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15 2008 558 566
32. J.M. Lopez del Amo, U. Fink, M. Dasari, G. Grelle, E.E. Wanker, J. Bieschke, and B. Reif Structural properties of EGCG-induced, nontoxic Alzheimer's disease Abeta oligomers J. Mol. Biol. 421 2012 517 524
33. L. Yu, and et al. Structural characterization of a soluble amyloid beta-peptide oligomer Biochemistry 48 2009 1870 1877
34. H.Y. Kim, and et al. Structural properties of pore-forming oligomers of alpha-synuclein J. Am. Chem. Soc. 131 2009 17482 17489
35. B.D. van Rooijen, K.A. van Leijenhorst-Groener, M.M. Claessens, and V. Subramaniam Tryptophan fluorescence reveals structural features of alpha-synuclein oligomers J. Mol. Biol. 394 2009 826 833
36. J. Kaylor, N. Bodner, S. Edridge, G. Yamin, D.P. Hong, and A.L. Fink Characterization of oligomeric intermediates in alpha-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F alpha-synuclein J. Mol. Biol. 353 2005 357 372
37. F.S. Ruggeri, J. Adamcik, J.S. Jeong, H.A. Lashuel, R. Mezzenga, and G. Dietler Influence of the beta-sheet content on the mechanical properties of aggregates during amyloid fibrillization Angew. Chem. Int. Ed. Engl. 54 2015 2462 2466
38. N. Lorenzen, 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
39. S.W. Chen, and et al. Structural characterization of toxic oligomers that are kinetically trapped during alpha-synuclein fibril formation Proc. Natl. Acad. Sci. U.S.A. 112 2015 E1994 E2003
40. K. Neupane, A. Solanki, I. Sosova, M. Belov, and M.T. Woodside Diverse metastable structures formed by small oligomers of α-synuclein probed by force spectroscopy PLoS One 9 2014 e86495
41. W. Paslawski, S. Mysling, K. Thomsen, T.J. Jorgensen, and D.E. Otzen Co-existence of two different alpha-synuclein oligomers with different core structures determined by hydrogen/deuterium exchange mass spectrometry Angew. Chem. Int. Ed. Engl. 53 2014 7560 7563
42. S. Mysling, C. Betzer, P.H. Jensen, and T.J. Jorgensen Characterizing the dynamics of alpha-synuclein oligomers using hydrogen/deuterium exchange monitored by mass spectrometry Biochemistry 52 2013 9097 9103
43. J.I. Gallea, and M.S. Celej Structural insights into amyloid oligomers of the Parkinson disease-related protein alpha-synuclein J. Biol. Chem. 289 2014 26733 26742
44. I. Horvath, and et al. Mechanisms of protein oligomerization: inhibitor of functional amyloids templates alpha-synuclein fibrillation J. Am. Chem. Soc. 134 2012 3439 3444
45. W. Paslawski, M. Andreasen, S.B. Nielsen, N. Lorenzen, K. Thomsen, J.D. Kaspersen, J.S. Pedersen, and D.E. Otzen High stability and cooperative unfolding of alpha-synuclein oligomers Biochemistry 53 2014 6252 6263
46. T. Nasstrom, T. Wahlberg, M. Karlsson, F. Nikolajeff, L. Lannfelt, M. Ingelsson, and J. Bergstrom The lipid peroxidation metabolite 4-oxo-2-nonenal cross-links alpha-synuclein causing rapid formation of stable oligomers Biochem. Biophys. Res. Commun. 378 2009 872 876
47. T. Nasstrom, and et al. The lipid peroxidation products 4-oxo-2-nonenal and 4-hydroxy-2-nonenal promote the formation of alpha-synuclein oligomers with distinct biochemical, morphological, and functional properties Free Radic. Biol. Med. 50 2011 428 437
48. Z. Qin, D. Hu, S. Han, S.H. Reaney, D.A. Di Monte, and A.L. Fink Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation J. Biol. Chem. 282 2007 5862 5870
49. E.J. Bae, and et al. Lipid peroxidation product 4-hydroxy-2-nonenal promotes seeding-capable oligomer formation and cell-to-cell transfer of alpha-synuclein Antioxid. Redox Signal. 18 2013 770 783
50. 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
51. N. Lorenzen, and et al. How epigallocatechin gallate can inhibit alpha-synuclein oligomer toxicity in vitro J. Biol. Chem. 289 2014 21299 21310
52. D.P. Hong, A.L. Fink, and V.N. Uversky Structural characteristics of alpha-synuclein oligomers stabilized by the flavonoid baicalein J. Mol. Biol. 383 2008 214 223
53. H.J. Lee, S.M. Baek, D.H. Ho, J.E. Suk, E.D. Cho, and S.J. Lee Dopamine promotes formation and secretion of non-fibrillar alpha-synuclein oligomers Exp. Mol. Med. 43 2011 216 222
54. A. Rekas, and et al. The structure of dopamine induced alpha-synuclein oligomers Eur. Biophys. J. 39 2010 1407 1419
55. R. Cappai, and et al. Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway FASEB J. 19 2005 1377 1379
56. X. Meng, L.A. Munishkina, A.L. Fink, and V.N. Uversky Effects of various flavonoids on the alpha-synuclein fibrillation process Parkinsons Dis. 2010 2010 650794
57. 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
58. M.S. Wang, S. Boddapati, S. Emadi, and M.R. Sierks Curcumin reduces alpha-synuclein induced cytotoxicity in Parkinson's disease cell model BMC Neurosci. 11 2010 57
59. K. Ono, M. Hirohata, and M. Yamada Alpha-synuclein assembly as a therapeutic target of Parkinson's disease and related disorders Curr. Pharm. Des. 14 2008 3247 3266
60. N. Pandey, J. Strider, W.C. Nolan, S.X. Yan, and J.E. Galvin Curcumin inhibits aggregation of alpha-synuclein Acta Neuropathol. 115 2008 479 489
61. C.A. Braga, and et al. The anti-Parkinsonian drug selegiline delays the nucleation phase of alpha-synuclein aggregation leading to the formation of nontoxic species J. Mol. Biol. 405 2011 254 273
62. K. Sivanesam, A. Byrne, M. Bisaglia, L. Bubacco, and N. Andersen Binding interactions of agents that alter alpha-synuclein aggregation RSC Adv. 5 2015 11577 11590
63. M. Masuda, and et al. Small molecule inhibitors of alpha-synuclein filament assembly Biochemistry 45 2006 6085 6094
64. R.A. Bodner, and et al. Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases Proc. Natl. Acad. Sci. U.S.A. 103 2006 4246 4251
65. 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 2008 e3394
66. V.N. Uversky, G. Yamin, P.O. Souillac, J. Goers, C.B. Glaser, and A.L. Fink Methionine oxidation inhibits fibrillation of human alpha-synuclein in vitro FEBS Lett. 517 2002 239 244
67. W. Zhou, C. Long, S.H. Reaney, D.A. Di Monte, A.L. Fink, and V.N. Uversky Methionine oxidation stabilizes non-toxic oligomers of alpha-synuclein through strengthening the auto-inhibitory intra-molecular long-range interactions Biochim. Biophys. Acta 1802 2010 322 330
68. A.W. Schmid, D. Chiappe, V. Pignat, V. Grimminger, I. Hang, M. Moniatte, and H.A. Lashuel Dissecting the mechanisms of tissue transglutaminase-induced cross-linking of alpha-synuclein: implications for the pathogenesis of Parkinson disease J. Biol. Chem. 284 2009 13128 13142
69. I.M. Segers-Nolten, M.M. Wilhelmus, G. Veldhuis, B.D. van Rooijen, B. Drukarch, and V. Subramaniam Tissue transglutaminase modulates alpha-synuclein oligomerization Protein Sci. 17 2008 1395 1402
70. L. Chen, Y. Wei, X. Wang, and R. He Ribosylation rapidly induces alpha-synuclein to form highly cytotoxic molten globules of advanced glycation end products PLoS One 5 2010 e9052
71. V. Padmaraju, J.J. Bhaskar, U.J. Prasada Rao, P.V. Salimath, and K.S. Rao Role of advanced glycation on aggregation and DNA binding properties of alpha-synuclein J. Alzheimers Dis. 24 2011 211 221
72. G. Yamin, V.N. Uversky, and A.L. Fink Nitration inhibits fibrillation of human alpha-synuclein in vitro by formation of soluble oligomers FEBS Lett. 542 2003 147 152
73. V.N. Uversky, G. Yamin, L.A. Munishkina, M.A. Karymov, I.S. Millett, S. Doniach, Y.L. Lyubchenko, and A.L. Fink Effects of nitration on the structure and aggregation of alpha-synuclein Brain Res. Mol. Brain Res. 134 2005 84 102
74. G.G. Kovacs, and et al. Intracellular processing of disease-associated alpha-synuclein in the human brain suggests prion-like cell-to-cell spread Neurobiol. Dis. 69 2014 76 92
75. J. Varkey, N. Mizuno, B.G. Hegde, N. Cheng, A.C. Steven, and R. Langen Alpha-synuclein oligomers with broken helical conformation form lipoprotein nanoparticles J. Biol. Chem. 288 2013 17620 17630
76. E.S. Luth, T. Bartels, U. Dettmer, N.C. Kim, and D.J. Selkoe Purification of alpha-synuclein from human brain reveals an instability of endogenous multimers as the protein approaches purity Biochemistry 54 2015 279 292
77. D. Selkoe, U. Dettmer, E. Luth, N. Kim, A. Newman, and T. Bartels Defining the native state of alpha-synuclein Neurodegener. Dis. 13 2014 114 117
78. T. Bartels, J.G. Choi, and D.J. Selkoe Alpha-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation Nature 477 2011 107 110
79. B. Fauvet, 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
80. M.M. Apetri, N.C. Maiti, M.G. Zagorski, P.R. Carey, and V.E. Anderson Secondary structure of alpha-synuclein oligomers: characterization by raman and atomic force microscopy J. Mol. Biol. 355 2006 63 71
81. D. Ghosh, and et al. Structure based aggregation studies reveal the presence of helix-rich intermediate during alpha-synuclein aggregation Sci. Rep. 5 2015 9228
82. T. Eichner, and S.E. Radford Understanding the complex mechanisms of beta2-microglobulin amyloid assembly FEBS J. 278 2011 3868 3883
83. C.M. Eakin, J.D. Knight, C.J. Morgan, M.A. Gelfand, and A.D. Miranker Formation of a copper specific binding site in non-native states of beta-2-microglobulin Biochemistry 41 2002 10646 10656
84. G. Verdone, and et al. The solution structure of human beta2-microglobulin reveals the prodromes of its amyloid transition Protein Sci. 11 2002 487 499
85. M.F. Calabrese, C.M. Eakin, J.M. Wang, and A.D. Miranker A regulatable switch mediates self-association in an immunoglobulin fold Nat. Struct. Mol. Biol. 15 2008 965 971
86. W.F. Xue, S.W. Homans, and S.E. Radford Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly Proc. Natl. Acad. Sci. U.S.A. 105 2008 8926 8931
87. K.W. Tipping, and et al. PH-induced molecular shedding drives the formation of amyloid fibril-derived oligomers Proc. Natl. Acad. Sci. U.S.A. 112 2015 5691 5696
88. M. Colombo, M. de Rosa, V. Bellotti, S. Ricagno, and M. Bolognesi A recurrent D-strand association interface is observed in beta-2 microglobulin oligomers FEBS J. 279 2012 1131 1143
89. A.C. Leney, C.L. Pashley, C.A. Scarff, S.E. Radford, and A.E. Ashcroft Insights into the role of the beta-2 microglobulin D-strand in amyloid propensity revealed by mass spectrometry Mol. BioSyst. 10 2014 412 420
90. I.V. Baskakov, G. Legname, M.A. Baldwin, S.B. Prusiner, and F.E. Cohen Pathway complexity of prion protein assembly into amyloid J. Biol. Chem. 277 2002 21140 21148
91. M.I. Apostol, K. Perry, and W.K. Surewicz Crystal structure of a human prion protein fragment reveals a motif for oligomer formation J. Am. Chem. Soc. 135 2013 10202 10205
92. T.C. Bjorndahl, and et al. Detailed biophysical characterization of the acid-induced PrP(c) to PrP(beta) conversion process Biochemistry 50 2011 1162 1173
93. L.L. Hosszu, and et al. Conformational properties of beta-PrP J. Biol. Chem. 284 2009 21981 21990
94. F. Eghiaian, T. Daubenfeld, Y. Quenet, M. van Audenhaege, A.P. Bouin, G. van der Rest, J. Grosclaude, and H. Rezaei Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage Proc. Natl. Acad. Sci. U.S.A. 104 2007 7414 7419
95. N. Chakroun, S. Prigent, C.A. Dreiss, S. Noinville, C. Chapuis, F. Fraternali, and H. Rezaei The oligomerization properties of prion protein are restricted to the H2H3 domain FASEB J. 24 2010 3222 3231
96. C. Liu, and et al. Out-of-register beta-sheets suggest a pathway to toxic amyloid aggregates Proc. Natl. Acad. Sci. U.S.A. 109 2012 20913 20918
97. L. Wei, and et al. The molecular basis of distinct aggregation pathways of islet amyloid polypeptide J. Biol. Chem. 286 2011 6291 6300
98. N. Carulla, M. Zhou, M. Arimon, M. Gairi, E. Giralt, C.V. Robinson, and C.M. Dobson Experimental characterization of disordered and ordered aggregates populated during the process of amyloid fibril formation Proc. Natl. Acad. Sci. U.S.A. 106 2009 7828 7833
99. C. Bleiholder, N.F. Dupuis, T. Wyttenbach, and M.T. Bowers Ion mobility-mass spectrometry reveals a conformational conversion from random assembly to beta-sheet in amyloid fibril formation Nat. Chem. 3 2011 172 177
100. E. Kachooei, A.A. Moosavi-Movahedi, F. Khodagholi, H. Ramshini, F. Shaerzadeh, and N. Sheibani Oligomeric forms of insulin amyloid aggregation disrupt outgrowth and complexity of neuron-like PC12 cells PLoS One 7 2012 e41344
101. B. Vestergaard, and et al. A helical structural nucleus is the primary elongating unit of insulin amyloid fibrils PLoS Biol. 5 2007 e134
102. L. Banci, and et al. From an inactive prokaryotic SOD homologue to an active protein through site-directed mutagenesis J. Am. Chem. Soc. 127 2005 13287 13292
103. K. Pagano, F. Bemporad, F. Fogolari, G. Esposito, P. Viglino, F. Chiti, and A. Corazza Structural and dynamics characteristics of acylphosphatase from Sulfolobus solfataricus in the monomeric state and in the initial native-like aggregates J. Biol. Chem. 285 2010 14689 14700
104. F. Bemporad, and F. Chiti Protein misfolded oligomers: experimental approaches, mechanism of formation, and structure-toxicity relationships Chem. Biol. 19 2012 315 327
105. T. Miti, M. Mulaj, J.D. Schmit, and M. Muschol Stable, metastable, and kinetically trapped amyloid aggregate phases Biomacromolecules 16 2015 326 335
106. D. Thirumalai, G. Reddy, and J.E. Straub Role of water in protein aggregation and amyloid polymorphism Acc. Chem. Res. 45 2012 83 92
107. C. Eugene, R. Laghaei, and N. Mousseau Early oligomerization stages for the non-amyloid component of alpha-synuclein amyloid J. Chem. Phys. 141 2014 135103
108. C. Capitini, and et al. TDP-43 inclusion bodies formed in bacteria are structurally amorphous, non-amyloid and inherently toxic to neuroblastoma cells PLoS One 9 2014 e86720
109. A. Levin, and et al. Ostwald's rule of stages governs structural transitions and morphology of dipeptide supramolecular polymers Nat. Commun. 5 2014 5219
110. J. Nyvlt The Ostwald rule of stages Cryst. Res. Technol. 30 1995 443 449
111. H.C. Zeng Ostwald ripening: a synthetic approach for hollow nanomaterials Curr. Nanosci. 3 2007 177 181
112. A. Orte, N.R. Birkett, R.W. Clarke, G.L. Devlin, C.M. Dobson, and D. Klenerman Direct characterization of amyloidogenic oligomers by single-molecule fluorescence Proc. Natl. Acad. Sci. U.S.A. 105 2008 14424 14429
113. G. Plakoutsi, F. Bemporad, M. Calamai, N. Taddei, C.M. Dobson, and F. Chiti Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates J. Mol. Biol. 351 2005 910 922
114. S.L. Bernstein, and et al. Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Nat. Chem. 1 2009 326 331
115. H.A. Lashuel, B.M. Petre, J. Wall, M. Simon, R.J. Nowak, T. Walz, and P.T. Lansbury Jr. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils J. Mol. Biol. 322 2002 1089 1102
116. D.L. Pountney, N.H. Voelcker, and W.P. Gai Annular alpha-synuclein oligomers are potentially toxic agents in alpha-synucleinopathy Hypothesis. Neurotox Res. 7 2005 59 67
117. S. Feng, X.H. Song, and C.M. Zeng Inhibition of amyloid fibrillation of lysozyme by phenolic compounds involves quinoprotein formation FEBS Lett. 586 2012 3951 3955
118. M.A. Poirier, H. Li, J. Macosko, S. Cai, M. Amzel, and C.A. Ross Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrillization J. Biol. Chem. 277 2002 41032 41037
119. F. Langer, Y.S. Eisele, S.K. Fritschi, M. Staufenbiel, L.C. Walker, and M. Jucker Soluble Abeta seeds are potent inducers of cerebral beta-amyloid deposition J. Neurosci. 31 2011 14488 14495
120. L.C. Walker, M.I. Diamond, K.E. Duff, and B.T. Hyman Mechanisms of protein seeding in neurodegenerative diseases JAMA Neurol. 70 2013 304 310
121. J.W. Wu, and et al. Small misfolded Tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons J. Biol. Chem. 288 2013 1856 1870
122. L. Liu, V. Drouet, J.W. Wu, M.P. Witter, S.A. Small, C. Clelland, and K. Duff Trans-synaptic spread of tau pathology in vivo PLoS One 7 2012 e31302
123. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, M.J. Guerrero-Munoz, T. Kiritoshi, V. Neugebauer, G.R. Jackson, and R. Kayed Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau Sci. Rep. 2 2012 700
124. E. Illes-Toth, M.R. Ramos, R. Cappai, C. Dalton, and D.P. Smith Structural characterisation of high order alpha-synuclein oligomers capable of inducing intracellular aggregation Biochem. J. 2015 (in press)
125. C.A. Lasagna-Reeves, and et al. A native interactor scaffolds and stabilizes toxic Ataxin-1 oligomers in SCA1 Elife 4 2015 e07558
126. K. Pauwels, and et al. Structural basis for increased toxicity of pathological abeta42:abeta40 ratios in Alzheimer disease J. Biol. Chem. 287 2012 5650 5660
127. Y.S. Fang, and et al. Full-length TDP-43 forms toxic amyloid oligomers that are present in frontotemporal lobar dementia-TDP patients Nat. Commun. 5 2014 4824
128. M. Zhang, R. Hu, H. Chen, Y. Chang, X. Gong, F. Liu, and J. Zheng Interfacial interaction and lateral association of cross-seeding assemblies between hIAPP and rIAPP oligomers Phys. Chem. Chem. Phys. 17 2015 10373 10382
129. U. Sengupta, and et al. Pathological interface between oligomeric alpha-synuclein and tau in synucleinopathies Biol. Psychiatry 2015 in press
130. M.J. Guerrero-Munoz, and et al. Amyloid-beta oligomers as a template for secondary amyloidosis in Alzheimer's disease Neurobiol. Dis. 71 2014 14 23
131. P.O. Souillac, V.N. Uversky, and A.L. Fink Structural transformations of oligomeric intermediates in the fibrillation of the immunoglobulin light chain LEN Biochemistry 42 2003 8094 8104
132. W.S. Gosal, I.J. Morten, E.W. Hewitt, D.A. Smith, N.H. Thomson, and S.E. Radford Competing pathways determine fibril morphology in the self-assembly of beta2-microglobulin into amyloid J. Mol. Biol. 351 2005 850 864
133. B. Mannini, and et al. Toxicity of protein oligomers is rationalized by a function combining size and surface hydrophobicity ACS Chem. Biol. 9 2014 2309 2317
134. H. Tian, E. Davidowitz, P. Lopez, S. Emadi, J. Moe, and M. Sierks Trimeric tau is toxic to human neuronal cells at low nanomolar concentrations Int. J. Cell Biol. 2013 2013 260787
135. S. Campioni, and et al. A causative link between the structure of aberrant protein oligomers and their toxicity Nat. Chem. Biol. 6 2010 140 147
136. A.R. Ladiwala, J.S. Dordick, and P.M. Tessier Aromatic small molecules remodel toxic soluble oligomers of amyloid beta through three independent pathways J. Biol. Chem. 286 2011 3209 3218
137. A.R. Ladiwala, M. Mora-Pale, J.C. Lin, S.S. Bale, Z.S. Fishman, J.S. Dordick, and P.M. Tessier Polyphenolic glycosides and aglycones utilize opposing pathways to selectively remodel and inactivate toxic oligomers of amyloid beta ChemBioChem 12 2011 1749 1758
138. D.H. Lopes, and et al. Molecular tweezers inhibit islet amyloid polypeptide assembly and toxicity by a new mechanism ACS Chem. Biol. 10 2015 1555 1569
139. G. Herzog, and et al. The Lys-specific molecular tweezer, CLR01, modulates aggregation of mutant p53 DNA binding domain and inhibits its toxicity Biochemistry 54 2015 3729 3738
140. A. Attar, and G. Bitan Disrupting self-assembly and toxicity of amyloidogenic protein oligomers by "molecular tweezers" - from the test tube to animal models Curr. Pharm. Des. 20 2014 2469 2483
141. N. Ferreira, and et al. Molecular tweezers targeting transthyretin amyloidosis Neurotherapeutics 11 2014 450 461
142. T. Liu, and G. Bitan Modulating self-assembly of amyloidogenic proteins as a therapeutic approach for neurodegenerative diseases: strategies and mechanisms ChemMedChem 7 2012 359 374
143. X. Zheng, D. Liu, F.G. Klarner, T. Schrader, G. Bitan, and M.T. Bowers Amyloid beta-protein assembly: The effect of molecular tweezers CLR01 and CLR03 J. Phys. Chem. B 119 2015 4831 4841
144. A. Jan, O. Adolfsson, I. Allaman, A.L. Buccarello, P.J. Magistretti, A. Pfeifer, A. Muhs, and H.A. Lashuel Abeta42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Abeta42 species J. Biol. Chem. 286 2011 8585 8596
145. M. Wogulis, S. Wright, D. Cunningham, T. Chilcote, K. Powell, and R.E. Rydel Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death J. Neurosci. 25 2005 1071 1080
146. E.B. Lee, L.Z. Leng, B. Zhang, L. Kwong, J.Q. Trojanowski, T. Abel, and V.M. Lee Targeting amyloid-beta peptide (Abeta) oligomers by passive immunization with a conformation-selective monoclonal antibody improves learning and memory in Abeta precursor protein (APP) transgenic mice J. Biol. Chem. 281 2006 4292 4299
147. M.P. Lambert, and et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U.S.A. 95 1998 6448 6453
148. M.P. Lambert, and et al. Monoclonal antibodies that target pathological assemblies of Abeta J. Neurochem. 100 2007 23 35
149. B.A. Chromy, and et al. Self-assembly of Abeta(1-42) into globular neurotoxins Biochemistry 42 2003 12749 12760
150. V. Venkataramani, O. Wirths, H. Budka, W. Hartig, G.G. Kovacs, and T.A. Bayer Antibody 9D5 recognizes oligomeric pyroglutamate amyloid-beta in a fraction of amyloid-beta deposits in Alzheimer's disease without cross-reactivity with other protein aggregates J. Alzheimers Dis. 29 2012 361 371
151. G.G. Kovacs, and et al. An antibody with high reactivity for disease-associated alpha-synuclein reveals extensive brain pathology Acta Neuropathol. 124 2012 37 50
152. I. Morgado, and et al. Molecular basis of beta-amyloid oligomer recognition with a conformational antibody fragment Proc. Natl. Acad. Sci. U.S.A. 109 2012 12503 12508
153. A. Noguchi, and et al. Isolation and characterization of patient-derived, toxic, high mass amyloid beta-protein (Abeta) assembly from Alzheimer disease brains J. Biol. Chem. 284 2009 32895 32905
154. H. Hillen, and et al. Generation and therapeutic efficacy of highly oligomer-specific beta-amyloid antibodies J. Neurosci. 30 2010 10369 10379
155. K. Murakami, and et al. Monoclonal antibody against the turn of the 42-residue amyloid beta-protein at positions 22 and 23 ACS Chem. Neurosci. 1 2010 747 756
156. H. Tian, E. Davidowitz, P. Lopez, P. He, P. Schulz, J. Moe, and M.R. Sierks Isolation and characterization of antibody fragments selective for toxic oligomeric tau Neurobiol. Aging 36 2015 1342 1355
157. S.M. Williams, L. Venkataraman, H. Tian, G. Khan, B.T. Harris, and M.R. Sierks Novel atomic force microscopy based biopanning for isolation of morphology specific reagents against TDP-43 variants in amyotrophic lateral sclerosis J. Vis. Exp. 2015 e52584
158. 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
159. R. Kayed, and et al. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers Mol. Neurodegener. 2 2007 18
160. J.M. Isas, V. Luibl, L.V. Johnson, R. Kayed, R. Wetzel, C.G. Glabe, R. Langen, and J. Chen Soluble and mature amyloid fibrils in drusen deposits Invest. Ophthalmol. Vis. Sci. 51 2010 1304 1310
161. T. Gurlo, and et al. Evidence for proteotoxicity in beta cells in type 2 diabetes: toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway Am. J. Pathol. 176 2010 861 869
162. A.L. Clos, C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, G.R. Jackson, B. Kelly, T.M. Beachkofsky, and R. Kayed Formation of immunoglobulin light chain amyloid oligomers in primary cutaneous nodular amyloidosis Br. J. Dermatol. 165 2011 1349 1354
163. C. Liu, and et al. Out-of-register beta-sheets suggest a pathway to toxic amyloid aggregates Proc. Natl. Acad. Sci. U.S.A. 2012
164. S. Emadi, H. Barkhordarian, M.S. Wang, P. Schulz, and M.R. Sierks Isolation of a human single chain antibody fragment against oligomeric alpha-synuclein that inhibits aggregation and prevents alpha-synuclein-induced toxicity J. Mol. Biol. 368 2007 1132 1144
165. M.S. Wang, A. Zameer, S. Emadi, and M.R. Sierks Characterizing antibody specificity to different protein morphologies by AFM Langmuir 25 2009 912 918
166. S. Emadi, S. Kasturirangan, M.S. Wang, P. Schulz, and M.R. Sierks Detecting morphologically distinct oligomeric forms of alpha-synuclein J. Biol. Chem. 284 2009 11048 11058
167. E. Kvam, B.L. Nannenga, M.S. Wang, Z. Jia, M.R. Sierks, and A. Messer Conformational targeting of fibrillar polyglutamine proteins in live cells escalates aggregation and cytotoxicity PLoS One 4 2009 e5727
168. B.L. Nannenga, A. Zameer, and M.R. Sierks Anti-oligomeric single chain variable domain antibody differentially affects huntingtin and alpha-synuclein aggregates FEBS Lett. 582 2008 517 522
169. A. Hatami, R. Albay 3rd, S. Monjazeb, S. Milton, and C. Glabe Monoclonal antibodies against Abeta42 fibrils distinguish multiple aggregation state polymorphisms in vitro and in Alzheimer disease brain J. Biol. Chem. 289 2014 32131 32143
170. 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
171. C.G. Glabe Structural classification of toxic amyloid oligomers J. Biol. Chem. 283 2008 29639 29643
172. J.C. Stroud, C. Liu, P.K. Teng, and D. Eisenberg Toxic fibrillar oligomers of amyloid-beta have cross-beta structure Proc. Natl. Acad. Sci. U.S.A. 109 2012 7717 7722
173. R. Kayed, and et al. Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Abeta oligomers Mol. Neurodegener. 5 2010 57
174. M.H. Ali, and B. Imperiali Protein oligomerization: how and why Bioorg. Med. Chem. 13 2005 5013 5020
175. A. Loquet, B. Habenstein, and A. Lange Structural investigations of molecular machines by solid-state NMR Acc. Chem. Res. 46 2013 2070 2079
176. E.M. Redwan, B. Xue, H.A. Almehdar, and V.N. Uversky Disorder in milk proteins: caseins, intrinsically disordered colloids Curr. Protein Pept. Sci. 16 2015 228 242
177. M.V. Sudnitsyna, E.V. Mymrikov, A.S. Seit-Nebi, and N.B. Gusev The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins Curr. Protein Pept. Sci. 13 2012 76 85
178. M. Haslbeck, and E. Vierling A first line of stress defense: small heat shock proteins and their function in protein homeostasis J. Mol. Biol. 427 2015 1537 1548
179. A.P. Arrigo Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update FEBS Lett. 587 2013 1959 1969
180. S.P. Delbecq, and R.E. Klevit One size does not fit all: the oligomeric states of alphaB crystallin FEBS Lett. 587 2013 1073 1080
181. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, and P.T. Lansbury Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291