Discrete molecular dynamics study of oligomer formation by N-terminally truncated amyloid β-protein

Journal of Molecular Biology

Volumn 425, Issue 12, 2013, Pages 2260-2275

  Meral, Derya ^a   Urbanc, Brigita ^a  

^a DREXEL UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; amyloid protein; discrete molecular dynamics; N terminal truncation; structure toxicity relationship

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[11-40]; AMYLOID BETA PROTEIN[11-42]; AMYLOID BETA PROTEIN[3-40]; AMYLOID BETA PROTEIN[3-42]; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR DYNAMICS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION;

EID: 84878245350     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.03.010     Document Type: Article

References (87)

1. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
2. J. Hardy Alzheimer's disease: genetic evidence points to a single pathogenesis Ann. Neurol. 54 2003 143 144
3. R. Roychaudhuri, M. Yang, M.M. Hoshi, and D.B. Teplow Amyloid β-protein assembly and Alzheimer disease J. Biol. Chem. 284 2008 4749 4753
4. M.D. Kirkitadze, G. Bitan, and D.B. Teplow Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies J. Neurosci. Res. 69 2002 567 577
5. W.L. Klein ADDLs & protofibrils - the missing links? Neurobiol. Aging 23 2002 231 233
6. W.L. Klein, W.B. Stine, and D.B. Teplow Small assemblies of unmodified amyloid β-protein are the proximate neurotoxin in Alzheimer's disease Neurobiol. Aging 25 2004 569 580
7. C.G. Glabe Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Aβ Subcell. Biochem. 38 2005 167 177
8. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
9. D.J. Selkoe Alzheimer disease: mechanistic understanding predicts novel therapies Ann. Int. Med. 140 2004 627 638
10. J.T. Jarrett, E.P. Berger, and P.T. Lansbury The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease Biochemistry 32 1993 4693 4697
11. J.T. Jarrett, E.P. Berger, and P.T. Lansbury The C-terminus of the β protein is critical in amyloidogenesis Ann. N. Y. Acad. Sci. 695 1993 144 148 (NIL)
12. N. Sawamura, M. Morishima-Kawashima, H. Waki, K. Kobayashi, T. Kuramochi, and M.P. Frosch Mutant Presenilin 2 Transgenic Mice. A large increase in the levels of Aβ 42 is presumably associated with the low density membrane domain that contains decreased levels of glycerophospholipids and sphingomyelin J. Biol. Chem. 275 2000 27901 27908
13. K.N. Dahlgren, A.M. Manelli, W.B. Stine, L.K. Baker, G.A. Krafft, and M.J. LaDu Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability J. Biol. Chem. 277 2002 32046 32053
14. H. Mori, K. Takio, M. Ogawara, and D.J. Selkoe Mass spectrometry of purified amyloid β protein in Alzheimer's disease J. Biol. Chem. 267 1992 17082 17086
15. J. Näslund, A. Schierhorn, U. Hellman, L. Lannfelt, A.D. Roses, and L.O. Tjernberg Relative abundance of Alzheimer Aβ amyloid peptide variants in Alzheimer disease and normal aging Proc. Natl Acad. Sci. USA 91 1994 8378 8382
16. Y. Harigaya, T.C. Saido, C.B. Eckman, C.-M. Prada, M. Shoji, and S.G. Younkin Amyloid β protein starting pyroglutamate at position 3 is a major component of the amyloid deposits in the Alzheimer's disease brain Biochem. Biophys. Res. Commun. 276 2000 422 427
17. K. Liu, I. Solano, D. Mann, C. Lemere, M. Mercken, J. Trojanowski, and V. Lee Characterization of Aβ1-40/42 peptide deposition in Alzheimer's disease and young down's syndrome brains: Implication of N-terminally truncated Aβ species in the pathogenesis of Alzheimer's disease Acta Neuropathol. 112 2006 163 174
18. N. Sergeant, S. Bombois, A. Ghestem, H. Drobecq, V. Kostanjevecki, and C. Missiaen Truncated β-amyloid peptide species in pre-clinical Alzheimer's disease as new targets for the vaccination approach J. Neurochem. 85 2003 1581 1591
19. A. Güntert, H. Döbeli, and B. Bohrmann High sensitivity analysis of amyloid-β peptide composition in amyloid deposits from human and PS2APP mouse brain Neuroscience 143 2006 461 475
20. N3(pE), in senile plaques Neuron 14 1995 457 466
21. C. Russo, T.C. Saido, L.M. DeBusk, M. Tabaton, P. Gambetti, and J.K. Teller Heterogeneity of water-soluble amyloid β-peptide in Alzheimer's disease and Down's syndrome brains FEBS Lett. 409 1997 411 416
22. T. Tekirian, T. Saido, W. Markesbery, M. Russell, D. Wekstein, E. Patel, and J. Geddes N-terminal heterogeneity of parenchymal and cerebrovascular Aβ deposits J. Neuropathol. Exp. Neurol. 57 1998 76 94
23. T.C. Saido, W. Yamao-Harigaya, T. Iwatsubo, and S. Kawashima Amino- and carboxyl-terminal heterogeneity of β-amyloid peptides deposited in human brain Neurosci. Lett. 215 1996 173 176
24. B. Urbanc, L. Cruz, D.B. Teplow, and H.E. Stanley Computer simulations of Alzheimer's amyloid β-protein folding and assembly Curr. Alzheimer Res. 3 2006 493 504
25. D.B. Teplow, N.D. Lazo, G. Bitan, S. Bernstein, T. Wyttenbach, and M.T. Bowers Elucidating amyloid β-protein folding and assembly: a multidisciplinary approach Acc. Chem. Res. 39 2006 635 645
26. A. Baumketner, S.L. Bernstein, T. Wyttenbach, G. Bitan, D.B. Teplow, M.T. Bowers, and J.-E. Shea Amyloid β-protein monomer structure: a computational and experimental study Protein Sci. 15 2006 420 428
27. M. Yang, and D.B. Teplow Amyloid β-protein monomer folding: free-energy surfaces reveal alloform-specific differences J. Mol. Biol. 384 2008 450 464
28. S. Kim, T. Takeda, and D.K. Klimov Mapping conformational ensembles of aβ oligomers in molecular dynamics simulations Biophys. J. 99 2010 1949 1958
29. O. Wise Scira, L. Xu, T. Kitahara, G. Perry, and O. Coskuner Amyloid-β peptide structure in aqueous solution varies with fragment size J. Chem. Phys. 135 2011 205101-1 205101-13
30. Y. Xu, J. Shen, X. Luo, W. Zhu, K. Chen, J. Ma, and H. Jiang Conformational transition of amyloid β-peptide Proc. Natl Acad. Sci. USA 102 2005 5403 5407
31. E. Luttmann, and G. Fels All-atom molecular dynamics studies of the full-length β-amyloid peptides Chem. Phys. 323 2006 138 147
32. S. Tomaselli, V. Esposito, P. Vangone, N.A.J. van Nuland, A.M.J.J. Bonvin, and R. Guerrini The α-to-β conformational transition of Alzheimer's Aβ-(1-42) peptide in aqueous media is reversible: a step by step conformational analysis suggests the location of β conformation seeding ChemBioChem 7 2006 257 267
33. D.F. Raffa, and A. Rauk Molecular dynamics study of the β amyloid peptide of Alzheimer's disease and its divalent copper complexes J. Phys. Chem. B 111 2007 3789 3799
34. N. Sgourakis, Y. Yan, S. McCallum, C. Wang, and A. Garcia The Alzheimer's peptides aβ40 and 42 adopt distinct conformations in water: a combined MD/NMR study J. Mol. Biol. 368 2007 1448 1457
35. L. Triguero, R. Singh, and R. Prabhakar Comparative molecular dynamics studies of wild-type and oxidized forms of full-length Alzheimer amyloid β-peptides Aβ(1-40) and Aβ(1-42) J. Phys. Chem. B 112 2008 7123 7131
36. C. Yang, X. Zhu, J. Li, and K. Chen Molecular dynamics simulation study on conformational behavior of Aβ(1-40) and Aβ(1-42) in water and methanol J. Mol. Struct. 907 2009 51 56
37. R.P. Bora, and R. Prabhakar Translational, rotational and internal dynamics of amyloid β-peptides (Aβ40 and Aβ42) from molecular dynamics simulations J. Chem. Phys. 131 2009 155103
38. C.H. Davis, and M.L. Berkowitz Structure of the amyloid-β(1-42) monomer absorbed to model phospholipid bilayers: a molecular dynamics study Biophys. J. 96 2009 785 797
39. A. Rubinstein, Y.L. Lyubchenko, and S. Sherman Dynamic properties of pH-dependent structural organization of the amyloidogenic β-protein (1-40) Prion 3 2009 31 43
40. C. Lee, and S. Ham Characterizing amyloid-beta protein misfolding from molecular dynamics simulations with explicit water J. Comput. Chem. 32 2011 349 355
41. N. Sgourakis, M. Merced-Serrano, C. Boutsidis, P. Drineas, Z. Du, C. Wang, and A. Garcia Atomic-level characterization of the ensemble of the Aβ(1-42) monomer in water using unbiased molecular dynamics simulations and spectral algorithms J. Mol. Biol. 368 2011 1448 1457
42. C. Velez-Vega, and F. Escobedo Characterizing the structural behavior of selected Aβ42 monomers with different solubilities J. Phys. Chem. B 115 2011 4900 4910
43. K.A. Ball, A.H. Phillips, P.S. Nerenberg, N.L. Fawzi, D.E. Wemmer, and T. Head Gordon Homogeneous and heterogeneous tertiary structure ensembles of amyloid-β peptides Biochemistry 50 2011 7612 7628
44. Y.-S. Lin, G.R. Bowman, K.A. Beauchamp, and V.S. Pande Investigating how peptide length and a pathogenic mutation modify the structural ensemble of amyloid beta monomer Biophys. J. 102 2012 315 324
45. B. Barz, and B. Urbanc Dimer formation enhances structural differences between amyloid β-protein (1-40) and (1-42): an explicit-solvent molecular dynamics study PLoS One 7 2012 e34345
46. C. Wu, and J.E. Shea Coarse-grained models for protein aggregation Curr. Opin. Struct. Biol. 21 2011 209 220
47. B. Urbanc, L. Cruz, S. Yun, S.V. Buldyrev, G. Bitan, D.B. Teplow, and H.E. Stanley In silico study of amyloid β-protein folding and oligomerization Proc. Natl Acad. Sci. USA 101 2004 17345 17350
48. B. Urbanc, J.M. Borreguero, L. Cruz, and H.E. Stanley Ab initio discrete molecular dynamics approach to protein folding and aggregation Methods Enzymol. 412 2006 314 338
49. S. Yun, B. Urbanc, L. Cruz, G. Bitan, D.B. Teplow, and H.E. Stanley Role of electrostatic interactions in Amyloid β-protein (Aβ) oligomer formation: a discrete molecular dynamics study Biophys. J. 92 2007 4064 4077
50. B. Urbanc, M. Betnel, L. Cruz, G. Bitan, and D.B. Teplow Elucidation of amyloid β-protein oligomerization mechanisms: discrete molecular dynamics study J. Am. Chem. Soc. 132 2010 4266 4280
51. 1-40(D23N) J. Chem. Theory Comput. 7 2011 2584 2592
52. S. Côté, R. Laghaei, P. Derreumaux, and N. Mousseau Distinct dimerization for various alloforms of the amyloid-β protein: Aβ(1-40), Aβ(1-42), and Aβ(1-40)(D23N) J. Phys. Chem. B 116 2012 4043 4055
53. A. Lam, D.B. Teplow, H.E. Stanley, and B. Urbanc Effects of the Arctic (E22→G) mutation on amyloid β-protein folding: discrete molecular dynamics study J. Am. Chem. Soc. 130 2008 17413 17422
54. G. Bitan, M.D. Kirkitadze, A. Lomakin, S.S. Vollers, G.B. Benedek, and D.B. Teplow Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways Proc. Natl Acad. Sci. USA 100 2003 330 335 PMCID:PMC140968
55. S.L. Bernstein, N.F. Dupuis, N.D. Lazo, T. Wyttenbach, M.M. Condron, and G. Bitan Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Nat. Chem. 1 2009 326 331
56. N.D. Lazo, M.A. Grant, M.M. Condron, A.C. Rigby, and D.B. Teplow On the nucleation of amyloid β-protein monomer folding Protein Sci. 14 2005 1581 1596
57. K. Murakami, K. Irie, H. Ohigashi, H. Hara, M. Nagao, T. Shimizu, and T. Shirasawa Formation and stabilization model of the 42-mer Aβ radical: implications for the long-lasting oxidative stress in Alzheimer's disease J. Am. Chem. Soc. 127 2005 15168 15174
58. G. Krafft, J. Joyce, J. Jerecic, R. Lowe, R. Hepler, and D.D. Nahas Design of arrested-assembly Aβ1-42 peptide variants to elucidate the ADDL oligomerization pathway and conformational specificity of anti-ADDL antibodies. Abstract of The Annual Meeting of the Society for Neuroscience, Atlanta 2006 Neuroscience Meeting Planner, Society for Neuroscience, Atlanta, GA (2006) Program No. 509.5 2006
59. Y. Yan, and C. Wang Aβ42 is more rigid than Aβ40 at the C terminus: implications for Aβ aggregation and toxicity J. Mol. Biol. 364 2006 853 862
60. K. Kamino, H.T. Orr, H. Payami, E.M. Wijsman, E. Alonso, and S.M. Pulst Linkage and mutational analysis of familial alzheimer disease kindreds for the app gene region Am. J. Hum. Genet. 51 1992 998 1014
61. C. Nilsberth, A. Westlind-Danielsson, C.B. Eckman, M.M. Condron, K. Axelman, and C. Forsell The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Aβ protofibril formation Nat. Neurosci. 4 2001 887 893
62. K. Murakami, K. Irie, A. Morimoto, H. Ohigashi, M. Shindo, and M. Nagao Neurotoxicity and physicochemical properties of a beta mutant peptides from cerebral amyloid angiopathy - implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer's disease J. Biol. Chem. 278 2003 46179 46187
63. A. Päiviö, J. Jarvet, A. Gräslund, L. Lannfelt, and A. Westlind-Danielsson Unique physicochemical profile of β-amyloid peptide variant Aβ1-40 E22G protofibrils: conceivable neuropathogen in Arctic mutant carriers J. Mol. Biol. 339 2004 145 159
64. B. Whalen, D. Selkoe, and D. Hartley Small non-fibrillar assemblies of amyloid β-protein bearing the Arctic mutation induce rapid neuritic degeneration Neurobiol. Dis. 20 2005 254 266
65. G. Bitan, S.S. Vollers, and D.B. Teplow Elucidation of primary structure elements controlling early amyloid β-protein oligomerization J. Biol. Chem. 278 2003 34882 34889
66. G. Bitan, A. Lomakin, and D.B. Teplow Amyloid β-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins J. Biol. Chem. 276 2001 35176 35184
67. G. Bitan Structural study of metastable amyloidogenic protein oligomers by photo-induced cross-linking of unmodified proteins Methods Enzymol. 413 2006 217 236
68. 1-42 toxicity inhibition by Aβ C-terminal fragments: discrete molecular dynamics study J. Mol. Biol. 410 2011 316 328
69. J. Lee, E. Culyba, E. Powers, and J. Kelly Amyloid-β forms fibrils by nucleated conformational conversion of oligomers Nat. Chem. Biol. 7 2011 602 609
70. S. Schilling, T. Lauber, M. Schaupp, S. Manhart, E. Scheel, G. Böhm, and H.-U. Demuth On the seeding and oligomerization of pGlu-amyloid peptides in vitro Biochemistry 45 2006 12393 12399
71. J. Nussbaum, S. Schilling, H. Cynis, A. Silva, E. Swanson, and T. Wangsanut Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-β Nature 485 2012 651 655
72. 1-40 peptides J. Phys. Chem. B 113 2009 6692 6702
73. T. Takeda, and D. Klimov Interpeptide interactions induce helix to strand structural transition in Aβ peptides Proteins 77 2009 1 13
74. H.R. LeVine Thioflavine T interaction with synthetic Alzheimer's disease β-amyloid peptides: detection of amyloid aggregation in solution Protein Sci. 2 1993 404 410
75. E. Fradinger, B.H. Monien, B. Urbanc, A. Lomakin, M. Tan, and H. Li C-terminal peptides coassemble into Aβ42 oligomers and protect neurons against Aβ42-induced neurotoxicity Proc. Natl Acad. Sci. USA 105 2008 14175 14180 PMCID:PMC2544597
76. H. Li, B.H. Monien, E.A. Fradinger, B. Urbanc, and G. Bitan Biophysical characterization of Aβ42 C-terminal fragments: inhibitors of Aβ42 neurotoxicity Biochemistry 49 2010 1259 1267 PMCID:PMC2831638
77. H. Li, B.H. Monien, A. Lomakin, R. Zemell, E.A. Fradinger, and M. Tan Mechanistic investigation of the inhibition of Aβ42 assembly and neurotoxicity by C-terminal Aβ42 fragments Biochemistry 49 2010 6358 6364
78. M.M. Gessel, C. Wu, H. Li, G. Bitan, J.-E. Shea, and M.T. Bowers Aβ(39-42) modulates Aβ42 oligomerization but not fibril formation Biochemistry 51 2011 108 117
79. G. DiFede, M. Catania, M. Morbin, G. Rossi, S. Suardi, and G. Mazzoleni A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis Science 323 2009 1473 1477
80. T. Jonsson, J.K. Atwal, S. Steinberg, J. Snaedal, P.V. Jonsson, and S. Bjornsson A mutation in APP protects against Alzheimer's disease and age-related cognitive decline Nature 488 2012 96 99
81. I. Youssef, S. Florent-Béchard, C. Malaplate-Armand, V. Koziel, B. Bihain, and J.-L. Olivier N-truncated amyloid-β oligomers induce learning impairment and neuronal apoptosis Neurobiol. Aging 29 2008 1319 1333
82. T.L. Tekirian, A.Y. Yang, C. Glabe, and J.W. Geddes Toxicity of pyroglutaminated amyloid β-peptides 3(pE)-40 and -42 is similar to that of Aβ1-40 and -42 J. Neurochem. 73 1999 1584 1589
83. C. Russo, E. Violani, S. Salis, V. Venezia, V. Dolcini, and G. Damonte Pyroglutamate-modified amyloid β-peptides AβN3(pE) strongly affect cultured neuron and astrocyte survival J. Neurochem. 82 2002 1480 1489
84. D.C. Rapaport The Art of Molecular Dynamics Simulation 1997 Cambridge University Press Cambridge
85. F. Ding, J.M. Borreguero, S.V. Buldyrev, H.E. Stanley, and N.V. Dokholyan Mechanism for the α-helix to β-hairpin transition Proteins: Struct. Funct. Genet. 53 2003 220 228
86. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucleic Acids Res. 28 2000 235 242 URL http://www.rcsb.org/pdb
87. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132