Structural Conversion of Aβ17–42 Peptides from Disordered Oligomers to U-Shape Protofilaments via Multiple Kinetic Pathways

PLoS Computational Biology

Volumn 11, Issue 5, 2015, Pages

  Cheon, Mookyung ^a   Hall, Carol K ^b   Chang, Iksoo ^a  

^a Daegu Gyeongbuk Institute of Science and Technology   (South Korea)

^b North Carolina State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINETICS; MOLECULAR DYNAMICS; NEURODEGENERATIVE DISEASES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES;

ALZHEIMER; DISCONTINOUS MOLECULAR DYNAMICS SIMULATIONS; KINETIC PATHWAY; LEVEL PROCESS; MOLECULAR LEVELS; PROTEIN AGGREGATES; PROTEIN AGGREGATION; PROTOFILAMENTS; STRUCTURAL CONVERSION; U SHAPE;

OLIGOMERS;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[17-42]; MONOMER; OLIGOMER; UNCLASSIFIED DRUG; AMYLOID BETA-PROTEIN (17-42); PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOTOXICITY; DEGENERATIVE DISEASE; KINETICS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PARKINSON DISEASE; PROTEIN AGGREGATION; PROTEIN CONFORMATION; ALGORITHM; BIOLOGY; CHEMICAL PHENOMENA; CHEMISTRY; COMPUTER SIMULATION; HUMAN; METABOLISM; PROCEDURES; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SOFTWARE; TEMPERATURE;

ALGORITHMS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SOFTWARE; TEMPERATURE;

EID: 84930608351     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004258     Document Type: Article

References (57)

1. Hamley IW, (2012) The Amyloid Beta Peptide: A Chemist's Perspective. Role in Alzheimer's and Fibrillization. Chemical Reviews 112: 5147–5192. doi: 10.1021/cr3000994 22813427
2. Tycko R, (2011) Solid-State NMR Studies of Amyloid Fibril Structure. Annual Review of Physical Chemistry, Vol 62 62: 279–299. doi: 10.1146/annurev-physchem-032210-103539 21219138
3. Bertini I, Gonnelli L, Luchinat C, Mao JF, Nesi A, (2011) A New Structural Model of A beta(40) Fibrils. Journal of the American Chemical Society 133: 16013–16022. doi: 10.1021/ja2035859 21882806
4. Paravastu AK, Leapman RD, Yau WM, Tycko R, (2008) Molecular structural basis for polymorphism in Alzheimer's beta-amyloid fibrils. Proceedings of the National Academy of Sciences of the United States of America 105: 18349–18354. doi: 10.1073/pnas.0806270105 19015532
5. Meinhardt J, Sachse C, Hortschansky P, Grigorieff N, Fandrich M, (2009) A beta(1–40) Fibril Polymorphism Implies Diverse Interaction Patterns in Amyloid Fibrils. Journal of Molecular Biology 386: 869–877. doi: 10.1016/j.jmb.2008.11.005 19038266
6. Miller Y, Ma B, Nussinov R, (2010) Polymorphism in Alzheimer A beta Amyloid Organization Reflects Conformational Selection in a Rugged Energy Landscape. Chemical Reviews 110: 4820–4838. doi: 10.1021/cr900377t 20402519
7. Colletier JP, Laganowsky A, Landau M, Zhao ML, Soriaga AB, et al. (2011) Molecular basis for amyloid-beta polymorphism. Proceedings of the National Academy of Sciences of the United States of America 108: 16938–16943. doi: 10.1073/pnas.1112600108 21949245
8. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, et al. (2010) Structural conversion of neurotoxic amyloid-beta(1–42) oligomers to fibrils. Nat Struct Mol Biol 17: 561–567. doi: 10.1038/nsmb.1799 20383142
9. Lee J, Culyba EK, Powers ET, Kelly JW, (2011) Amyloid-β forms fibrils by nucleated conformational conversion of oligomers. Nat Chem Biol 7: 602–609. doi: 10.1038/nchembio.624 21804535
10. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, et al. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci U S A 100: 330–335. 12506200
11. Bernstein SL, Dupuis NF, Lazo ND, Wyttenbach T, Condron MM, et al. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat Chem 1: 326–331. doi: 10.1038/nchem.247 20703363
12. Laganowsky A, Liu C, Sawaya MR, Whitelegge JP, Park J, et al. (2012) Atomic View of a Toxic Amyloid Small Oligomer. Science 335: 1228–1231. doi: 10.1126/science.1213151 22403391
13. Ladiwala ARA, Litt J, Kane RS, Aucoin DS, Smith SO, et al. (2012) Conformational Differences between Two Amyloid beta Oligomers of Similar Size and Dissimilar Toxicity. Journal of Biological Chemistry 287: 24765–24773. doi: 10.1074/jbc.M111.329763 22547072
14. Roychaudhuri R, Yang MF, Deshpande A, Cole GM, Frautschy S, et al. (2013) C-Terminal Turn Stability Determines Assembly Differences between A beta 40 and A beta 42. Journal of Molecular Biology 425: 292–308. doi: 10.1016/j.jmb.2012.11.006 23154165
15. Jang H, Arce FT, Ramachandran S, Capone R, Lal R, et al. (2010) Structural Convergence Among Diverse, Toxic beta-Sheet Ion Channels. Journal of Physical Chemistry B 114: 9445–9451. doi: 10.1021/jp104073k 20608696
16. Jang HB, Zheng J, Lal R, Nussinov R, (2008) New structures help the modeling of toxic amyloid beta ion channels. Trends in Biochemical Sciences 33: 91–100. doi: 10.1016/j.tibs.2007.10.007 18182298
17. Rajadas J, Liu CW, Novick P, Kelley NW, Inayathullah M, et al. (2011) Rationally Designed Turn Promoting Mutation in the Amyloid-beta Peptide Sequence Stabilizes Oligomers in Solution. Plos One 6.
18. Wei WL, Norton DD, Wang XT, Kusiak JW, (2002) A beta 17–42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis. Brain 125: 2036–2043. 12183349
19. Miller Y, Ma BY, Nussinov R, (2009) Polymorphism of Alzheimer's A beta(17–42) (p3) Oligomers: The Importance of the Turn Location and Its Conformation. Biophysical Journal 97: 1168–1177. doi: 10.1016/j.bpj.2009.05.042 19686665
20. Petkova AT, Yau WM, Tycko R, (2006) Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry 45: 498–512. 16401079
21. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, et al. (2005) 3D structure of Alzheimer's amyloid-beta(1–42) fibrils. Proceedings of the National Academy of Sciences of the United States of America 102: 17342–17347. 16293696
22. Zhang R, Hu XY, Khant H, Ludtke SJ, Chiu W, et al. (2009) Interprotofilament interactions between Alzheimer's A beta(1–42) peptides in amyloid fibrils revealed by cryoEM. Proceedings of the National Academy of Sciences of the United States of America 106: 4653–4658. doi: 10.1073/pnas.0901085106 19264960
23. Miller Y, Ma BY, Tsai CJ, Nussinov R, (2010) Hollow core of Alzheimer's A beta(42) amyloid observed by cryoEM is relevant at physiological pH. Proceedings of the National Academy of Sciences of the United States of America 107: 14128–14133. doi: 10.1073/pnas.1004704107 20660780
24. Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, et al. (2013) Molecular Structure of beta-Amyloid Fibrils in Alzheimer's Disease Brain Tissue. Cell 154: 1257–1268. doi: 10.1016/j.cell.2013.08.035 24034249
25. Di Fede G, Catania M, Morbin M, Gobbi M, Colombo L, et al. (2009) A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis: a new perspective for AD therapeutics. European Journal of Neurology 16: 336–336.
26. Jonsson T, Atwal JK, Steinberg S, Snaedal J, Jonsson PV, et al. (2012) A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488: 96–99. doi: 10.1038/nature11283 22801501
27. Nguyen PH, Tarus B, Derreumaux P, (2014) Familial Alzheimer A2 V Mutation Reduces the Intrinsic Disorder and Completely Changes the Free Energy Landscape of the A beta 1–28 Monomer. Journal of Physical Chemistry B 118: 501–510. doi: 10.1021/jp4115404 24372615
28. Zheng J, Jang H, Ma B, Nussinov R, (2008) Annular structures as intermediates in fibril formation of Alzheimer A beta(17–42). Journal of Physical Chemistry B 112: 6856–6865. doi: 10.1021/jp711335b 18457440
29. Zheng J, Jang H, Ma B, Tsai CJ, Nussinov R, (2007) Modeling the Alzheimer A beta(17–42) fibril architecture: Tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophysical Journal 93: 3046–3057. 17675353
30. Masman MF, Eisel ULM, Csizmadia IG, Penke B, Enriz RD, et al. (2009) In Silico Study of Full-Length Amyloid beta 1–42 Tri- and Penta-Oligomers in Solution. Journal of Physical Chemistry B 113: 11710–11719. doi: 10.1021/jp901057w 19645414
31. Urbanc B, Cruz L, Yun S, Buldyrev SV, Bitan G, et al. (2004) In silico study of amyloid beta-protein folding and oligomerization. Proceedings of the National Academy of Sciences of the United States of America 101: 17345–17350. 15583128
32. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow DB, (2010) Elucidation of Amyloid beta-Protein Oligomerization Mechanisms: Discrete Molecular Dynamics Study. Journal of the American Chemical Society 132: 4266–4280. doi: 10.1021/ja9096303 20218566
33. Melquiond A, Dong X, Mousseau N, Derreumaux P, (2008) Role of the region 23–28 in A beta fibril formation: Insights from simulations of the monomers and dimers of Alzheimer's peptides A beta 40 and A beta 42. Current Alzheimer Research 5: 244–250. 18537541
34. Chebaro Y, Jiang P, Zang T, Mu YG, Nguyen PH, et al. (2012) Structures of A beta 17–42 Trimers in Isolation and with Five Small-Molecule Drugs Using a Hierarchical Computational Procedure. Journal of Physical Chemistry B 116: 8412–8422. doi: 10.1021/jp2118778 22283547
35. Han W, Schulten K, (2014) Fibril Elongation by A beta(17–42): Kinetic Network Analysis of Hybrid-Resolution Molecular Dynamics Simulations. Journal of the American Chemical Society 136: 12450–12460. doi: 10.1021/ja507002p 25134066
36. Nguyen PH, Li MS, Stock G, Straub JE, Thirumalai D, (2007) Monomer adds to preformed structured oligomers of Abeta-peptides by a two-stage dock-lock mechanism. Proc Natl Acad Sci U S A 104: 111–116. 17190811
37. Zhang T, Xu WX, Mu YG, Derreumaux P, (2014) Atomic and Dynamic Insights into the Beneficial Effect of the 1,4-Naphthoquinon-2-yl-L-tryptophan Inhibitor on Alzheimer's A beta 1–42 Dimer in Terms of Aggregation and Toxicity. Acs Chemical Neuroscience 5: 148–159. doi: 10.1021/cn400197x 24246047
38. Cheon M, Chang I, Hall CK, (2010) Extending the PRIME model for protein aggregation to all 20 amino acids. Proteins-Structure Function and Bioinformatics 78: 2950–2960. doi: 10.1002/prot.22817 20740494
39. Cheon M, Chang I, Hall CK, (2012) Influence of temperature on formation of perfect tau fragment fibrils using PRIME20/DMD simulations. Protein Science 21: 1514–1527. doi: 10.1002/pro.2141 22887126
40. Cheon M, Chang I, Hall CK, (2011) Spontaneous Formation of Twisted A beta(16–22) Fibrils in Large-Scale Molecular-Dynamics Simulations. Biophysical Journal 101: 2493–2501. doi: 10.1016/j.bpj.2011.08.042 22098748
41. Park J, Kahng B, Hwang W, (2009) Thermodynamic Selection of Steric Zipper Patterns in the Amyloid Cross-beta Spine. Plos Computational Biology 5.
42. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447: 453–457. 17468747
43. Petkova AT, Leapman RD, Guo ZH, Yau WM, Mattson MP, et al. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307: 262–265. 15653506
44. Williams AD, Portelius E, Kheterpal I, Guo JT, Cook KD, et al. (2004) Mapping A beta amyloid fibril secondary structure using scanning proline mutagenesis. Journal of Molecular Biology 335: 833–842. 14687578
45. Shivaprasad S, Wetzel R, (2004) Mapping abeta amyloid topology using cysteine mutants. Neurobiology of Aging 25: S160–S160.
46. Ma BY, Nussinov R, (2006) Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Current Opinion in Chemical Biology 10: 445–452. 16935548
47. Frishman D, Argos P, (1995) Knowledge-based protein secondary structure assignment. Proteins-Structure Function and Genetics 23: 566–579. 8749853
48. Xue WF, Homans SW, Radford SE, (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proceedings of the National Academy of Sciences of the United States of America 105: 8926–8931. doi: 10.1073/pnas.0711664105 18579777
49. Reddy G, Straubb JE, Thirumalai D, (2009) Dynamics of locking of peptides onto growing amyloid fibrils. Proceedings of the National Academy of Sciences of the United States of America 106: 11948–11953. doi: 10.1073/pnas.0902473106 19581575
50. Alder BJ, Wainwright TE, (1959) Studies in Molecular Dynamics. 1. General Method. Journal of Chemical Physics 31: 459–466.
51. Nguyen HD, Hall CK, (2004) Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proceedings of the National Academy of Sciences of the United States of America 101: 16180–16185. 15534217
52. Smith AV, Hall CK, (2001) alpha-helix formation: Discontinuous molecular dynamics on an intermediate-resolution protein model. Proteins-Structure Function and Genetics 44: 344–360. 11455608
53. Nguyen HD, Marchut AJ, Hall CK, (2004) Solvent effects on the conformational transition of a model polyalanine peptide. Protein Science 13: 2909–2924. 15498937
54. Wagoner VA, Cheon M, Chang I, Hall CK, (2011) Computer simulation study of amyloid fibril formation by palindromic sequences in prion peptides. Proteins-Structure Function and Bioinformatics 79: 2132–2145.
55. Wagoner VA, Cheon M, Chang I, Hall CK, (2012) Fibrillization Propensity for Short Designed Hexapeptides Predicted by Computer Simulation. Journal of Molecular Biology 416: 598–609. doi: 10.1016/j.jmb.2011.12.038 22227390
56. Tarus B, Straub JE, Thirumalai D, (2006) Dynamics of Asp23-Lys28 salt-bridge formation in A beta(10–35) monomers. Journal of the American Chemical Society 128: 16159–16168. 17165769
57. Sciarretta KL, Gordon DJ, Petkova AT, Tycko R, Meredith SC, (2005) A beta 40-Lactam(D23/K28) models a conformation highly favorable for nucleation of amyloid. Biochemistry 44: 6003–6014. 15835889