Molecular mechanism of misfolding and aggregation of Aβ(13-23)

Journal of Physical Chemistry B

Volumn 117, Issue 20, 2013, Pages 6175-6186

  Lovas, Sándor ^a   Zhang, Yuliang ^b   Yu, Junping ^b   Lyubchenko, Yuri L ^b  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; ATOMIC FORCE MICROSCOPY; CONFORMATIONS; HYDROGEN BONDS; MOLECULAR DYNAMICS; MONOMERS; PEPTIDES; SELF ASSEMBLY;

ALZHEIMER'S DISEASE; ANTIPARALLEL ORIENTATIONS; CONFORMATIONAL FLEXIBILITY; CONFORMATIONAL SPACE; DYNAMIC FORCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR SIGNATURES; WEAKLY POLAR INTERACTIONS;

DIMERS;

EID: 84878027204     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp402938p     Document Type: Article

References (81)

1. Dobson, C. M. Principles of Protein Folding, Misfolding and Aggregation Semin. Cell. Dev. Biol. 2004, 15, 3-16
2. Madine, J.; Jack, E.; Stockley, P. G.; Radford, S. E.; Serpell, L. C.; Middleton, D. A. Structural Insights into the Polymorphism of Amyloid-Like Fibrils Formed by Region 20-29 of Amylin Revealed by Solid-State NMR and X-ray Fiber Diffraction J. Am. Chem. Soc. 2008, 130, 14990-15001
3. Lynn, D. G.; Meredith, S. C. Review: Model Peptides and the Physicochemical Approach to β-Amyloids J. Struct. Biol. 2000, 130, 153-173
4. Fernandez-Busquets, X.; de Groot, N. S.; Fernandez, D.; Venture, S. Recent Structural and Computational Insights Into Conformational Diseases Curr. Med. Chem. 2008, 15, 1336-1349
5. Munishkina, L. A.; Fink, A. L. Fluorescence as a Method to Reveal Structures and Membrane-Interactions of Amyloidogenic Proteins Biochim. Biophys. Acta 2007, 1768, 1862-1885
6. Petkova, A. T.; Ishii, Y.; Balbach, J. J.; Antzutkin, O. N.; Leapman, R. D.; Delaglio, F.; Tycko, R. A Structural Model for Alzheimer's β-amyloid Fibrils Based on Experimental Constraints from Solid State NMR Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16742-16747
7. Balbach, J. J.; Petkova, A. T.; Oyler, N. A.; Antzutkin, O. N.; Gordon, D. J.; Meredith, S. C.; Tycko, R. Supramolecular Structure in Full-Length Alzheimer's β-Amyloid Fibrils: Evidence for a Parallel β-Sheet Organization from Solid-State Nuclear Magnetic Resonance Biophys. J. 2002, 83, 1205-1216
8. Petkova, A. T.; Buntkowsky, G.; Dyda, F.; Leapman, R. D.; Yau, W. M.; Tycko, R. Solid State NMR Reveals a pH-dependent Antiparallel β-Sheet Registry in Fibrils Formed by a β-Amyloid Peptide J. Mol. Biol. 2004, 335, 247-260
9. Klimov, D. K.; Thirumalai, D. Dissecting the Assembly of Aβ16-22 Amyloid Peptides into Antiparallel β Sheets Structure 2003, 11, 295-307
10. Nguyen, P. H.; Li, M. S.; Stock, G.; Straub, J. E.; Thirumalai, D. Monomer adds to preformed structured oligomers of Aβ-peptides by a two-stage dock-lock mechanism Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 111-116
11. Gnanakaran, S.; Nussinov, R.; Garcia, A. E. Atomic-Level Description of Amyloid β-Dimer Formation J. Am. Chem. Soc. 2006, 128, 2158-2159
12. Rojas, A. V.; Liwo, A.; Scheraga, H. A. A Study of the α-Helical Intermediate Preceding the Aggregation of the Amino-Terminal Fragment of the β Amyloid Peptide (Aβ1-28) J. Phys. Chem. B 2011, 115, 12978-12983
13. Yankner, B. A.; Lu, T. Amyloid β-Protein Toxicity and the Pathogenesis of Alzheimer Disease J. Biol. Chem. 2009, 284, 4755-4759
14. Li, S.; Shankar, G. M.; Selkoe, D. How Do Soluble Oligomers of Amyloid Beta-protein Impair Hippocampal Synaptic Plasticity? Front. Cell Neurosci. 2010, 4, 1-2
15. Li, S.; Hong, S.; Shepardson, N. E.; Walsh, D. M.; Shankar, G. M.; Selkoe, D. Soluble Oligomers of Amyloid β Protein Facilitate Hippocampal Long-Term Depression by Disrupting Neuronal Glutamate Uptake Neuron 2009, 62, 788-801
16. Bernstein, S. L.; Dupuis, N. F.; Lazo, N. D.; Wyttenbach, T.; Condron, M. M.; Bitan, G.; Teplow, D. B.; Shea, J.-E.; Ruotolo, B. T.; Robinson, C. V.; Bowers, M. T. Amyloid-β Protein Oligomerization and the Importance of Tetramers and Dodecamers in the Eetiology of Alzheimer's Disease Nat. Chem. 2009, 1, 326-331
17. He, X.; Giurleo, J. T.; Talaga, D. S. Role of Small Oligomers on the Amyloidogenic Aggregation Free-Energy Landscape J. Mol. Biol. 2010, 395, 134-154
18. Jin, M.; Shepardson, N.; Yang, T.; Chen, G.; Walsh, D.; Selkoe, D. J. Soluble Amyloid Beta-protein Dimers Isolated from Alzheimer Cortex Directly Induce Tau Hyperphosphorylation and Neuritic Degeneration Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 5819-5824
19. Lyubchenko, Y. L.; Kim, B. H.; Krasnoslobodtsev, A. V.; Yu, J. Nanoimaging for Protein Misfolding Diseases Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2010, 2, 526-543
20. McAllister, C.; Karymov, M. A.; Kawano, Y.; Lushnikov, A. Y.; Mikheikin, A.; Uversky, V. N.; Lyubchenko, Y. L. Protein Interactions and Misfolding Analyzed by AFM Force Spectroscopy J. Mol. Biol. 2005, 354, 1028-1042
21. Lyubchenko, Y. L.; Sherman, S.; Shlyakhtenko, L. S.; Uversky, V. N. Nanoimaging for Protein Misfolding and Related Diseases J. Cell Biochem. 2006, 99, 52-70
22. Evans, E. Probing the Relation Between Force-Lifetime and Chemistry in Single Molecular Bonds Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 105-128
23. Yu, J.; Malkova, S.; Lyubchenko, Y. L. Alpha-Synuclein Misfolding: Single Molecule AFM Force Spectroscopy Study J. Mol. Biol. 2008, 384, 992-1001
24. Yu, J.; Lyubchenko, Y. L. Early Stages for Parkinson's Sevelopment: Alpha-Synuclein Misfolding and Aggregation J. Neuroimmun. Pharmacol. 2009, 4, 10-16
25. Kim, B. H.; Palermo, N. Y.; Lovas, S.; Zaikova, T.; Keana, J. F.; Lyubchenko, Y. L. Single-Molecule Atomic Force Microscopy Force Spectroscopy Study of Abeta-40 Interactions Biochemistry 2011, 50, 5154-5162
26. Santini, S.; Wei, G.; Mousseau, N.; Derreumaux, P. Pathway Complexity of Alzheimer's beta-Amyloid Abeta16-22 Peptide Assembly Structure 2004, 12, 1245-1255
27. Balbach, J. J.; Ishii, Y.; Antzutkin, O. N.; Leapman, R. D.; Rizzo, N. W.; Dyda, F.; Reed, J.; Tycko, R. Amyloid Fibril Formation by Aβ16-22, a Seven-Residue Fragment of the Alzheimer's β-Amyloid Peptide, and Structural Characterization by Solid State NMR Biochemistry 2000, 39, 13748-13759
28. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
29. Hatfield, M. P. D.; Murphy, R. F.; Lovas, S. Molecular Dynamics Analysis of the Conformations of a Beta-Hairpin Miniprotein J. Phys. Chem. B 2010, 114, 3028-3037
30. Hatfield, M. P. D.; Murphy, R. F.; Lovas, S. VCD Spectroscopic Properties of the β-Hairpin Forming Miniprotein CLN025 in Various Solvents Biopolymers 2010, 93, 442-450
31. Kaminski, G. A.; Friesner, R. A.; Tirado-Rives, J.; Jorgensen, W. L. Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides J. Phys. Chem. B 2001, 105, 6474-6487
32. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-242
33. Zhang, S.; Iwata, K.; Lachenmann, M. J.; Peng, J. W.; Li, S.; Stimson, E. R.; Lu, Y. A.; Felix, A. M.; Maggio, J. E.; Lee, J. P. The Alzheimer's Peptide Aβ Adopts a Collapsed Coil Structure in Water J. Struct. Biol. 2000, 130, 130-141
34. Tomaselli, S.; Esposito, V.; Vangone, P.; van Nuland, N. A. J.; Bonvin, A. M. J. J.; Guerrini, R.; Tancredi, T.; Temussi, P. A.; Picone, D. 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 2006, 7, 257-267
35. Petkova, A. T.; Yau, W. M.; Tycko, R. Experimental Constraints on Quaternary Structure in Alzheimer's Beta-Amyloid Fibrils Biochemistry 2006, 45, 498-512
36. Jorgensen, W. L.; Madura, J. D. Temperature and Size Dependence for Monte Carlo Simulations of TIP4P Water Mol. Phys. 1985, 56, 1381-1392
37. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A Linear Constraint Solver for Molecular Simulations J. Comput. Chem. 1997, 18, 1463-1472
38. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684-3690
39. Kabsch, W.; Sander, C. Dictionary of Protein Secondary Structure: Pattern Recognition of Hydrogen-Bonded and Geometrical Features Biopolymers 1983, 22, 2577-2637
40. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2011.
41. Lovell, S. C.; Davis, I. W.; Arendall, W. B., III; de Bakker, P. I. W.; Word, J. M.; Prisant, M. G.; Richardson, J. S.; Richardson, D. C. Structure Validation by Cα Geometry: ∥,ψ and Cβ Deviation Proteins 2003, 50, 437-450
42. Daura, X.; Gademann, K.; Jaun, B.; Seebach, D.; van Gunsteren, W. F.; Mark, A. E. Peptide Folding: When Simulation Meets Experiment Angew. Chem., Int. Ed. 1999, 38, 236-240
43. Amadei, A.; Ceruso, M. A.; Di Nola, A. On the Convergence of the Conformational Coordinates Basis Set Obtained by the Essential Dynamics Analysis of Proteins' Molecular Dynamics Simulations Proteins 1999, 36, 419-424
44. Hayward, S.; de Groot, B. L. Normal Modes and Essential Dynamics. In Methods in Molecular Biology, Kukol, A., Ed.; Humana Press: Totowa, NJ, 2008; Vol. 443, Molecular Modeling of Proteins, pp 89-106.
45. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graph. 1996, 14, 33-38
46. Kortvelyesi, T.; Murphy, R. F.; Lovas, S. Secondary Structures and Intramolecular Interactions in Fragments of the B-loops of Naturally Occurring Analogs of Epidermal Growth Factor J. Biomol. Struct. Dyn. 1999, 17, 393-407
47. Toth, G.; Watts, C. R.; Murphy, R. F.; Lovas, S. Significance of Aromatic-Backbone Amide Interactions in Protein Structure Proteins 2001, 43, 373-381
48. Nosé, S.; Klein, M. L. Constant Pressure Molecular Dynamics for Molecular Systems Mol. Phys. 1983, 50, 1055-1076
49. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190
50. Nose, S. A Unified Formulation of the Constant Temperature Molecular Dynamics Methods J. Chem. Phys. 1984, 81, 511-519
51. Hoover, W. G. Canonical dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
52. Patey, G. N.; Valleau, J. P. The Free Energy of Spheres with Dipoles: Monte Carlo with Multistage Sampling Chem. Phys. Lett. 1973, 21, 297-300
53. Torrie, G. M.; Valleau, J. P. Monte Carlo Free Energy Estimates Using Non-Boltzmann Sampling: Application to the Sub-Critical Lennard-Jones Fluid Chem. Phys. Lett. 1974, 28, 578-581
54. Torrie, G. M.; Valleau, J. P. Nonphysical Sampling Distributions in Monte Carlo Free-Energy Estimation: Umbrella Sampling J. Comput. Phys. 1977, 23, 187-199
55. Kumar, S.; Rosenberg, J. M.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A. The Weighted Histogram Analysis Method for Free-Energy Calculations on Biomolecules. I J. Comput. Chem. 1992, 13, 1011-1021
56. Jarzynski, C. Nonequilibrium Equality for Free Energy Differences Phys. Rev. Lett. 1997, 78, 2690-2693
57. Hub, J. S.; de Groot, B. L.; van der Spoel, D. J. g-wham: A Free Weighted Histogram Analysis Implementation Including Robust Error and Autocorrelation Estimates J. Chem. Theory Comput. 2010, 6, 3713-3720
58. Klimov, D. K.; Thirumalai, D. Dissecting the Assembly of Aβ16-22 Amyloid Peptides into Antiparallel β Sheets Structure 2003, 11, 295-307
59. Nguyen, P. H.; Li, M. S.; Stock, G.; Straub, J. E.; Thirumalai, D. Monomer Adds to Preformed Structured Oligomers of Aβ-peptides by a Two-Stage Dock-Lock Mechanism Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 111-116
60. Eker, F.; Griebenow, K.; Schweitzer-Stenner, R. Aβ1-28 Fragment of the Amyloid Peptide Predominantly Adopts a Polyproline II Conformation in an Acidic Solution Biochemistry 2004, 43, 6893-6898
61. Gnanakaran, S.; Nussinov, R.; García, A. E. Atomic-Level Description of Amyloid β-Dimer Formation J. Am. Chem. Soc. 2006, 128, 2158-2159
62. Tjernberg, L. O.; Callaway, D. J.; Tjernberg, A.; Hahne, S.; Lilliehöök, C.; Terenius, L.; Thyberg, J.; Nordstedt, C. A Molecular Model of Alzheimer Amyloid Beta-Peptide Fibril Formation J. Biol. Chem. 1999, 274, 12619-12625
63. Palermo, N. Y.; Csontos, J.; Owen, M. C.; Murphy, R. F.; Lovas, S. Aromatic-Backbone Interactions in Model α-Helical Peptides J. Comput. Chem. 2007, 28, 1208-1214
64. Csontos, J.; Palermo, N. Y.; Murphy, R. F.; Lovas, S. Calculation of Weakly Polar Interaction Energies in Polypeptides Using Density Functional and Local Møller-Plesset Perturbation Theory J. Comput. Chem. 2008, 29, 1344-1352
65. Hatfield, M. P. D.; Palermo, N. Y.; Csontos, J.; Murphy, R. F.; Lovas, S. Quantum Chemical Quantification of Weakly Polar Interaction Energies in the TC5b Miniprotein J. Phys. Chem. B 2008, 112, 3503-3508
66. Palermo, N. Y.; Csontos, J.; Murphy, R. F.; Lovas, S. Role of Aromatic Residues in Stabilizing the Secondary and Tertiary Structure of Avian Pancreatic Polypeptide Int. J. Quantum Chem. 2008, 108, 814-819
67. Hatfield, M. P. D.; Murphy, R. F.; Lovas, S. The CLN025 Decapeptide Retains a β-Hairpin Conformation in Urea and Guanidinium Chloride J. Phys. Chem. B 2011, 115, 4971-4981
68. Mothana, B.; Roy, S.; Rauk, A. Molecular Dynamics Study of the Interaction of Aβ (13-23) with β-sheet Inhibitors ARKIVOC 2009, 2009, 116-134
69. Lemkul, J. A.; Bevan, D. R. Assessing the Stability of Alzheimer's Amyloid Protofibrils Using Molecular Dynamics J. Phys. Chem. B 2010, 114, 1652-1660
70. Bu, Z.; Shi, Y.; Callaway, D. J. E.; Tycko, R. Molecular Alignment within β-Sheets in Aβ14-23 Fibrils: Solid-State NMR Experiments and Theoretical Predictions Biophys. J. 2007, 92, 594-602
71. Straub, J. E.; Thirumalai, D. Principles Governing Oligomer Formation in Amyloidogenic Peptides Curr. Opin. Struct. Biol. 2010, 20, 187-195
72. Takeda, T.; Klimov, D. E. Interpeptide Interactions Induce Helix to Strand Structural Transition in Aβ Peptides Proteins 2009, 77, 1-13
73. Rojas, A.; Liwo, A.; Browne, D.; Scheraga, H. A. Mechanism of Fiber Assembly: Treatment of Aβ Peptide Aggregation with a Coarse-Grained United-Residue Force Field J. Mol. Biol. 2010, 404, 537-552
74. Lührs, T.; Ritter, C.; Adrian, M.; Riek-Loher, D.; Bohrmann, B.; Döbeli, H.; Schubert, D.; Riek, R. 3D Structure of Alzheimer's Amyloid-β(1-42) fibrils Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17342-17347
75. Nguyen, P. H.; Li, M. S.; Derreumaux, P. Effects of All-Atom Force Fields on Amyloid Oligomerization: Replica Exchange Molecular Dynamics Simulations of the Aβ16-22 Dimer and Trimer Phys. Chem. Chem. Phys. 2011, 13, 9778-9788
76. Xu, W.; Zhang, C.; Derreumaux, P.; Gräslund, A.; Morozova-Roche, L.; Mu, Y. Intrinsic Determinants of Aβ 12-24 pH-Dependent Self-Assembly Revealed by Combined Computational and Experimental Studies PLoS One 2011, 6, e24329
77. Chebaro, Y.; Mousseau, N.; Derreumaux, P. Structures and Thermodynamics of Alzheimer's Amyloid-β Aβ (16-35) Monomer and Dimer by Replica Exchange Molecular Dynamics Simulations: Implication for Full-Length Aβ Fibrillation J. Phys. Chem. B 2009, 113, 7668-7675
78. Sarroukh, R.; Cerf, E.; Derclaye, S.; Dufrene, Y. F.; Goormaghtigh, E.; Ruysschaert, J.; Raussens, V. Transformation of Amyloid β(1-40) Oligomers into Fibrils is Characterized by a Major Change in Secondary Structure Cell. Mol. Life Sci. 2011, 68, 1429-1438
79. Mitternacht, S.; Staneva, I.; Härd, T.; Irbäck, A. Monte Carlo Study of the Formation and Conformational Properties of Dimers of Aβ42 Variants J. Mol. Biol. 2011, 410, 357-367
80. Baftizadeh, F.; Biarnes, X.; Pietrucci, F.; Affinito, F.; Laio, A. Multidimensional View of Amyloid Fibril Nucleation in Atomistic Detail J. Am. Chem. Soc. 2012, 134, 3886-3894
81. Coîté, S.; Laghaei, R.; Derreumaux, P.; Mousseau, N. Distinct Dimerization for Various Alloforms of the Amyloid-Beta Protein: Aβ1-40, Aβ1-42, and Aβ1-40(D23N) J Phys Chem B 2012, 116, 4043-4055