Structural diversity of alzheimer's disease amyloid-β dimers and their role in oligomerization and fibril formation

Journal of Alzheimer's Disease

Volumn 39, Issue 3, 2014, Pages 583-600

  Tsigelny, Igor F ^a,b,c   Sharikov, Yuriy ^a,c   Kouznetsova, Valentina L ^a,b   Greenberg, Jerry P ^a   Wrasidlo, Wolfgang ^b,c   Gonzalez, Tania ^c   Desplats, Paula ^c   Michael, Sarah E ^c   Trejo Morales, Margarita ^c   Overk, Cassia R ^c   Masliah, Eliezer ^b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dimers; molecular dynamics; neurodegeneration; oligomers; synaptoxicity

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; DIMER;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; FIBRIL FORMATION; FREQUENCY ANALYSIS; MOLECULAR DYNAMICS; NEURAL STEM CELL; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RAT; WILD TYPE;

DIMERS; MOLECULAR DYNAMICS; NEURODEGENERATION; OLIGOMERS; SYNAPTOXICITY;

AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; DIMERIZATION; HIPPOCAMPUS; HUMANS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NEURAL STEM CELLS; POINT MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RATS;

EID: 84894039447     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131589     Document Type: Article

References (80)

1. Lashuel HA, Hartley DM, Petre BM, Wall JS, Simon MN, Walz T, Lansbury PT Jr (2003) Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J Mol Biol 332, 795-808.
2. Klein WL (2002) ADDLs & protofibrils-the missing links? Neurobiol Aging 23, 231-235.
3. Klein WL, Krafft GA, Finch CE (2001) Targeting small Abeta oligomers: The solution to an Alzheimer's disease conundrum? Trends Neurosci 24, 219-224.
4. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N, Ihara I (1994) Visualization of Abeta 42 (43) and A beta 40 in senile plaques with end-specific A beta monoclonals: Evidence that an initially deposited species in A beta 42 (43). Neuron 13, 45-53.
5. Sakono M, Zako T (2010) Amyloid oligomers: Formation and toxicity of Abeta oligomers. FEBS J 277, 1348-1358.
6. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357.
7. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95, 6448-6453.
8. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8, 101-112.
9. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shep-ardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
10. Klyubin I, Betts V, Welzel AT, Blennow K, Zetterberg H, Wallin A, Lemere CA, Cullen WK, Peng Y, Wisniewski T, Selkoe DJ, Anwyl R, Walsh DM, Rowan MJ (2008) Amyloid beta protein dimer-containing human CSF disrupts synap-tic plasticity: Prevention by systemic passive immunization. J Neurosci 28, 4231-4237.
11. Lansbury PT Jr (1999) Evolution of amyloid: What normal protein folding may tell us about fibrillogenesis and disease. Proc Natl Acad Sci USA 96, 3342-3344.
12. Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm. J Mol Biol 293, 321-331.
13. Barrow C, Yasuda A, Kenny P, Zagorski M (1992) Solution conformations and aggregational properties of synthetic amyloid beta-peptidesof Alzheimer's disease. Analysisofcircular dichroism spectra. J Mol Biol 225, 1075-1093.
14. Jarrett JT, Lansbury PT Jr (1993) Seeding "one-dimensional crystallization" of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058.
15. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, Teplow DB (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci USA 100, 330-335.
16. Riek R, Guntert P, Dobeli H, Wipf B, Wuthrich K (2001) NMR studies in aqueous solution fail to identify significant confor-mational differences between the monomeric forms of two Alzheimer peptides with widely differentplaque-competence, A beta (1-40) (ox) and A beta (1-42) (ox). Eur J Biochem 268, 5930-5936.
17. Baumketner A, Krone MG, Shea JE (2008) Role of the familial Dutch mutation E22Q in the folding and aggregation of the 15-28 fragment of the Alzheimer amyloid-beta protein. Proc Natl Acad Sci USA 105, 6027-6032.
18. Cruz L, Urbanc B, Borreguero JM, Lazo ND, Teplow DB, Stanley HE (2005) Solvent and mutation effects on the nucle-ation of amyloid beta-protein folding. Proc Natl Acad Sci USA 102, 18258-18263.
19. Fawzi NL, Phillips AH, Ruscio JZ, Doucleff M, Wemmer DE, Head-Gordon T (2008) Structure and dynamics of the Abeta (21-30) peptide from the interplay of NMR experiments and molecular simulations. J Am Chem Soc 130, 6145-6158.
20. Gnanakaran S, Nussinov R, Garcia AE (2006) Atomic-level description of amyloid beta-dimer formation. J Am Chem Soc 128, 2158-2159.
21. Han W, Wu YD (2005) A strand-loop-strand structure is a possible intermediate in fibril elongation: Long time simulations of amyloid-beta peptide (10-35). J Am Chem Soc 127, 15408-15416.
22. Khandogin J, Brooks CL, 3rd (2007) Linking folding with aggregation in Alzheimer's beta-amyloid peptides. Proc Natl Acad Sci USA 104, 16880-16885.
23. Klimov DK, Straub JE, Thirumalai D (2004) Aqueous urea solution destabilizes Abeta (16-22) oligomers.Proc Natl Acad Sci USA 101, 14760-14765.
24. Krone MG, Hua L, Soto P, Zhou R, Berne BJ, Shea JE (2008) Role of water in mediating the assembly of Alzheimer amyloid-beta Abeta16-22 protofilaments. J Am Chem Soc 130, 11066-11072.
25. Lakdawala AS, Morgan DM, Liotta DC, Lynn DG, Snyder JP (2002) Dynamics and fluidity of amyloid fibrils: A model of fibrous protein aggregates. J Am Chem Soc 124, 15150-15151.
26. Ma B, Nussinov R (2002) Stabilities and conformations of Alzheimer's beta-amyloid peptide oligomers (Abeta 16-22, Abeta 16-35, and Abeta 10-35): Sequence effects. Proc Natl Acad Sci USA 99, 14126-14131.
27. 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 USA 104, 111-116.
28. Santini S, Mousseau N, Derreumaux P (2004) In silico assembly of Alzheimer's Abeta16-22 peptide into beta-sheets. J Am Chem Soc 126, 11509-11516.
29. Tarus B, Straub JE, Thirumalai D (2006) Dynamics of Asp23-Lys28 salt-bridge formation in Abeta10-35 monomers. J Am Chem Soc 128, 16159-16168.
30. Wu C, Wang Z, Lei H, Zhang W, Duan Y (2007) Dual binding modes of Congo red toamyloid protofibril surface observed in molecular dynamics simulations. J Am Chem Soc 129, 1225-1232.
31. Bernstein SL, Wyttenbach T, Baumketner A, Shea JE, Bitan G, Teplow DB, Bowers MT (2005) Amyloid beta-protein: Monomer structure and early aggregation states of Abeta42 and its Pro19 alloform. J Am Chem Soc 127, 2075-2084.
32. Dong X, Chen W, Mousseau N, Derreumaux P (2008) Energy landscapes of the monomer and dimer of the Alzheimer's peptide Abeta (1-28). J Chem Phys 128, 125108.
33. Itoh SG, Okamoto Y (2008) Amyloid-beta (29-42) dimer formations studied by a multicanonical-multioverlap molecular dynamics simulation. J Phys Chem B 112, 2767-2770.
34. Jang S, Shin S (2006) Amyloid beta-peptide oligomerization in silico: Dimer and trimer. J Phys Chem B 110, 1955-1958.
35. Lam AR, Teplow DB, Stanley HE, Urbanc B (2008) Effects of the Arctic (E22G) mutation on amyloid beta-protein folding: Discrete molecular dynamics study. J Am Chem Soc 130, 17413-17422.
36. Urbanc B, Cruz L, Yun S, Buldyrev SV, Bitan G, Teplow DB, Stanley HE (2004) In silico study of amyloid beta-protein folding and oligomerization. Proc Natl Acad Sci USA 101, 17345-17350.
37. Borreguero JM, Urbanc B, Lazo ND, Buldyrev SV, Teplow DB, Stanley HE (2005) Folding events in the 21-30 region of amyloid beta-protein (Abeta) studied in silico. Proc Natl Acad Sci USA 102, 6015-6020.
38. Jang H, Hall CK, Zhou Y (2004) Assembly and kinetic folding pathways of a tetrameric beta-sheet complex: Molecular dynamics simulationsonsimplified off-lattice protein models. Biophys J 86, 31-49.
39. Peng S, Ding F, Urbanc B, Buldyrev SV, Cruz L, Stanley HE, Dokholyan NV (2004) Discrete molecular dynamics simulations of peptide aggregation. Phys Rev E Stat Nonlin Soft Matter Phys 69, 041908.
40. Urbanc B, Cruz L, Ding F, Sammond D, Khare S, Buldyrev SV, Stanley HE, Dokholyan NV (2004) Molecular dynamics simulation of amyloid beta dimer formation. Biophys J 87, 2310-2321.
41. Yun S, Urbanc B, Cruz L, Bitan G, Teplow DB, Stanley HE (2007) Role of electrostatic interactions in amyloid beta-protein (A beta) oligomer formation: A discrete molecular dynamics study. Biophys J 92, 4064-4077.
42. Lee C, Ham S (2011) Characterizing amyloid-beta protein misfolding from molecular dynamics simulations with explicit water. J Comput Chem 32, 349-355.
43. Zheng J, Jang H, Ma B, Nussinov R (2008) Annular structures as intermediates in fibril formation of Alzheimer Abeta17-42. J Phys Chem B 112, 6856-6865.
44. Zheng J, Jang H, Ma B, Tsai CJ, Nussinov R (2007) Modeling the Alzheimer Abeta17-42 fibril architecture: Tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophys J 93, 3046-3057.
45. Anand P, Nandel FS, Hansmann UH (2008) The Alzheimer's beta amyloid (Abeta1-39) monomer in an implicit solvent. J Chem Phys 128, 165102.
46. Petkova AT, Yau WM, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer's beta-amyloid fibrils. Biochemistry (Mosc) 45, 498-512.
47. Takeda T, Klimov DK (2009) Interpeptide interactions induce helix to strand structural transition in Abeta peptides. Proteins 77, 1-13.
48. Cote S, Laghaei R, Derreumaux P, Mousseau N (2012) Distinct dimerization for various alloforms of the amyloid-beta protein: Abeta (1-40), Abeta (1-42), and Abeta (1-40) (D23N). J Phys Chem B 116, 4043-4055.
49. Yu X, Zheng J (2011) Polymorphic structures of Alzheimer's beta-amyloid globulomers. PloS one 6, e20575.
50. Barz B, Urbanc B (2012) Dimer formation enhances structural differences between amyloid beta-protein (1-40) and (1-42): An explicit-solvent molecular dynamics study. PloS one 7, e34345.
51. Zhu X, Bora RP, Barman A, Singh R, Prabhakar R (2012) Dimerization of the full-length Alzheimer amyloid beta-peptide (Abeta42) in explicit aqueous solution: A molecular dynamics study. J Phys Chem B 116, 4405-4416.
52. Tsigelny IF, Bar-On P, Sharikov Y, Crews L, Hashimoto M, Miller MA, Keller SH, Platoshyn O, Yuan JX, Masliah E (2007) Dynamics of alpha-synuclein aggregation and inhibition of pore-like oligomer development by beta-synuclein. FEBS J 274, 1862-1877.
53. Tsigelny IF, Crews L, Desplats P, Shaked GM, Sharikov Y, Mizuno H, Spencer B, Rockenstein E, Trejo M, Platoshyn O, Yuan JX, Masliah E (2008) Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PloS one 3, e3135.
54. Crescenzi O, Tomaselli S, Guerrini R, Salvadori S, D'Ursi AM, Temussi PA, Picone D (2002) Solution structure of the Alzheimer amyloid beta-peptide (1-42) in an apolar microen-vironment. Similarity with a virus fusion domain. Eur J Biochem 269, 5642-5648.
55. Kalé L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, Krawetz N, Phillips J, Shinozaki A, Varadarajan K, Schulten K (1999) NAMD2: Greater scalability for parallel molecular dynamics. J Comput Phys 151, 282-312.
56. Feller S, MacKerell A (2000) Animproved empirical potential energy function for molecular simulations of phospholipids. J Phys Chem B 104, 7510-7515.
57. Tu K, Tobias DJ, Klein ML (1995) Constant pressure and temperature molecular dynamics simulation of a fully hydrated liquid crystal phase dipalmitoylphosphatidylcholine bilayer. Biophys J 69, 2558-2562.
58. Feller S, Zhang Y, Pastor RW, Brooks BR (1995) Constant pressure molecular dynamics simulation: The Langevin piston method. J Chem Phys 103, 4613-4621.
59. Essmann U, Perera L, Berkowitz ML (1995) A smooth particle mesh Ewald method. J Chem Phys 103, 8577-8593.
60. Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 11, 739-747.
61. Macindoe G, Mavridis L, Venkatraman V, Devignes MD, Ritchie DW (2010) HexServer: An FFT-based protein docking server powered by graphics processors. Nucleic Acids Res 38, W445-W449.
62. Sharikov Y, Walker RC, Greenberg J, Kouznetsova V, Nigam SK, Miller MA, Masliah E, Tsigelny IF (2008) MAPAS: A tool for predicting membrane-contacting protein surfaces. Nat Methods 5, 119.
63. Lomize MA, Pogozheva ID, Joo H, Mosberg HI, Lomize AL (2012) OPM database and PPM web server: Resources for positioning of proteins in membranes. Nucleic Acids Res 40, D370-D376.
64. Kucerka N, Nagle JF, Sachs JN, Feller SE, Pencer J, Jackson A, Katsaras J (2008) Lipid bilayer structure determinedbythe simultaneous analysis of neutron and X-ray scattering data. Biophys J 95, 2356-2367.
65. Marsh D (2002) Membrane water-penetration profiles from spin labels. Eur Biophys J 31, 559-562.
66. Lomize AL, Pogozheva ID, Mosberg HI (2011) Anisotropic solvent model of the lipid bilayer. 2. Energetics of insertion of small molecules, peptides, and proteins in membranes. J Chem Inf Model 51, 930-946.
67. van Rooijen BD, Claessens MM, Subramaniam V (2009) Lipid bilayer disruption by oligomeric alpha-synuclein depends on bilayer charge and accessibility of the hydropho-bic core. Biochim Biophys Acta 1788, 1271-1278.
68. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow DB (2010) Elucidation of amyloid beta-protein oligomerization mechanisms: Discrete molecular dynamics study. J Am Chem Soc 132, 4266-4280.
69. Mitternacht S, Staneva I, Hard T, Irback A (2011) Monte Carlo study of the formation and conformational properties of dimers of Abeta42 variants. J Mol Biol 410, 357-367.
70. Armen R, Alonso DO, Daggett V (2003) The role of alpha-, 3 (10)-, and pi-helix in helixcoil transitions. Prot Sci 12, 1145-1157.
71. Espinoza-Fonseca LM, Kast D, Thomas DD (2007) Molecular dynamics simulations reveal a disorder-to-order transition on phosphorylation of smooth muscle myosin. Biophys J 93, 2083-2090.
72. Masman MF, Eisel UL, Csizmadia IG, Penke B, Enriz RD, Marrink SJ, Luiten PG (2009) In silico study of full-length amyloid beta 1-42 tri-and penta-oligomers in solution. J Phys Chem B 113, 11710-11719.
73. Zhao J, Wang Q, Liang G, Zheng J (2011) Molecular dynamics simulations of low-ordered Alzheimer beta-amyloid oligomers from dimer to hexamer on self-assembled mono-layers. Langmuir 27, 14876-14887.
74. Wang Q, Zhao J, Yu X, Zhao C, Li L, Zheng J (2010) Alzheimer Abeta (1-42) monomer adsorbed on the self-assembled monolayers. Langmuir 26, 12722-12732.
75. Wang Q, Zhao C, Zhao J, Wang J, Yang JC, Yu X, Zheng J (2010) Comparative molecular dynamics study of Abeta adsorption on the self-assembled monolayers. Langmuir 26, 3308-3316.
76. Davis CH, Berkowitz ML (2010) A molecular dynamics study of the early stages of amyloid-beta (1-42) oligomerization: The role of lipid membranes. Proteins 78, 2533-2545.
77. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 30, 572-580.
78. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 27, 457-464.
79. Freir DB, Fedriani R, Scully D, Smith IM, Selkoe DJ, Walsh DM, Regan CM (2011) Abeta oligomers inhibit synapse remodelling necessary for memory consolidation. Neurobiol Aging 32, 2211-2218.
80. O'Nuallain B, Freir DB, Nicoll AJ, Risse E, Ferguson N, Herron CE, Collinge J, Walsh DM (2010) Amyloid beta-protein dimers rapidly form stable synaptotoxic protofibrils. J Neurosci 30, 14411-14419.