Computer simulation studies of Aβ37-42 aggregation thermodynamics and kinetics in water and salt solution

Journal of Physical Chemistry B

Volumn 119, Issue 3, 2015, Pages 662-670

  Yang, Y Isaac ^a   Gao, Yi Qin ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; FREE ENERGY; GLYCOPROTEINS; MOLECULAR DYNAMICS; SELF ASSEMBLY; THERMODYNAMICS;

AGGREGATION IN SOLUTIONS; FREE ENERGY LANDSCAPE; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; REVERSIBLE FORMATION; SOLUTION CONDITIONS; THERMODYNAMICS AND KINETICS; TRANSITION PATH THEORIES;

PROTEINS;

AMYLOID BETA PROTEIN; SODIUM CHLORIDE; SOLUTION AND SOLUBILITY; WATER;

CHEMISTRY; DRUG EFFECTS; KINETICS; MOLECULAR DYNAMICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; THERMODYNAMICS;

AMYLOID BETA-PEPTIDES; KINETICS; MOLECULAR DYNAMICS SIMULATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SODIUM CHLORIDE; SOLUTIONS; THERMODYNAMICS; WATER;

EID: 84921527087     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp502169b     Document Type: Article

References (74)

1. Lin, C. Y.; Gurlo, T.; Kayed, R.; Butler, A. E.; Haataja, L.; Glabe, C. G.; Butler, P. C. Toxic Human Islet Amyloid Polypeptide (h-IAPP) Oligomers Are Intracellular, and Vaccination to Induce Anti-Toxic Oligomer Antibodies Does Not Prevent h-IAPP-Induced Beta-Cell Apoptosis in h-IAPP Transgenic Mice Diabetes 2007, 56, 1324-32
2. Irvine, G. B.; El-Agnaf, O. M.; Shankar, G. M.; Walsh, D. M. Protein Aggregation in the Brain: The Molecular Basis for Alzheimers and Parkinsons Diseases Mol. Med. 2008, 14, 451-464
3. Prelli, F.; Castano, E.; Glenner, G. G.; Frangione, B. Differences between Vascular and Plaque Core Amyloid in Alzheimers Disease J. Neurochem. 1988, 51, 648-651
4. Strittmatter, W. J.; Saunders, A. M.; Schmechel, D.; Pericak-Vance, M.; Enghild, J.; Salvesen, G. S.; Roses, A. D. Apolipoprotein E: High-Avidity Binding to Beta-Amyloid and Increased Frequency of Type 4 Allele in Late-Onset Familial Alzheimer Disease Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 1977-1981
5. Hensley, K.; Carney, J. M.; Mattson, M. P.; Aksenova, M.; Harris, M.; Wu, J. F.; Floyd, R. A.; Butterfield, D. A. A Model for Beta-Amyloid Aggregation and Neurotoxicity Based on Free Radical Generation by the Peptide: Relevance to Alzheimer Disease Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 3270-3274
6. Scheuner, D.; Eckman, C.; Jensen, M.; Song, X.; Citron, M.; Suzuki, N.; Bird, T. D.; Hardy, J.; Hutton, M.; Kukull, W. Secreted Amyloid β-Protein Similar to That in the Senile Plaques of AlzheimerS Disease Is Increased in Vivo by the Presenilin 1 and 2 and APP Mutations Linked to Familial Alzheimers Disease Nat. Med. 1996, 2, 864-870
7. Mattson, M. P. Cellular Actions of Beta-Amyloid Precursor Protein and Its Soluble and Fibrillogenic Derivatives Physiol. Rev. 1997, 77, 1081-1132
8. Lahiri, D. K.; Maloney, B. Beyond the Signaling Effect Role of Amyloid-β42 on the Processing of APP, and Its Clinical Implications Exp. Neurol. 2010, 225, 51-54
9. Vivekanandan, S.; Brender, J. R.; Lee, S. Y.; Ramamoorthy, A. A Partially Folded Structure of Amyloid-Beta(1-40) In an Aqueous Environment Biochem. Biophys. Res. Commun. 2011, 411, 312-316
10. Lambert, M. P.; Barlow, A. K.; Chromy, B. A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T. E.; Rozovsky, I.; Trommer, B.; Viola, K. L. Diffusible, Nonfibrillar Ligands Derived from Aβ1-42 Are Potent Central Nervous System Neurotoxins Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 6448-6453
11. Mucke, L.; Masliah, E.; Yu, G.-Q.; Mallory, M.; Rockenstein, E. M.; Tatsuno, G.; Hu, K.; Kholodenko, D.; Johnson-Wood, K.; McConlogue, L. High-Level Neuronal Expression of Aβ1-42 in Wild-Type Human Amyloid Protein Precursor Transgenic Mice: Synaptotoxicity without Plaque Formation J. Neurosci. 2000, 20, 4050-4058
12. Chromy, B. A.; Nowak, R. J.; Lambert, M. P.; Viola, K. L.; Chang, L.; Velasco, P. T.; Jones, B. W.; Fernandez, S. J.; Lacor, P. N.; Horowitz, P. Self-Assembly of Aβ1-42 into Globular Neurotoxins Biochemistry 2003, 42, 12749-12760
13. Li, H.; Monien, B. H.; Fradinger, E. A.; Urbanc, B.; Bitan, G. Biophysical Characterization of Aβ42 C-Terminal Fragments: Inhibitors of Aβ42 Neurotoxicity Biochemistry 2010, 49, 1259-1267
14. Wu, C.; Murray, M. M.; Bernstein, S. L.; Condron, M. M.; Bitan, G.; Shea, J.-E.; Bowers, M. T. The Structure of Aβ42 C-Terminal Fragments Probed by a Combined Experimental and Theoretical Study J. Mol. Biol. 2009, 387, 492-501
15. Yan, Y.; Wang, C. Aβ42 is More Rigid than Aβ40 at the C Terminus: Implications for Aβ Aggregation and Toxicity J. Mol. Biol. 2006, 364, 853-862
16. Eisenberg, D.; Jucker, M. The Amyloid State of Proteins in Human Diseases Cell 2012, 148, 1188-1203
17. Nelson, R.; Sawaya, M. R.; Balbirnie, M.; Madsen, A. O.; Riekel, C.; Grothe, R.; Eisenberg, D. Structure of the Cross-Beta Spine of Amyloid-Like Fibrils Nature 2005, 435, 773-778
18. Sawaya, M. R.; Sambashivan, S.; Nelson, R.; Ivanova, M. I.; Sievers, S. A.; Apostol, M. I.; Thompson, M. J.; Balbirnie, M.; Wiltzius, J. J. W.; McFarlane, H. T. Atomic Structures of Amyloid Cross-Beta Spines Reveal Varied Steric Zippers Nature 2007, 447, 453-457
19. Colletier, J.-P.; Laganowsky, A.; Landau, M.; Zhao, M.; Soriaga, A. B.; Goldschmidt, L.; Flot, D.; Cascio, D.; Sawaya, M. R.; Eisenberg, D. Molecular Basis for Amyloid-β Polymorphism Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16938-16943
20. Fandrich, M.; Meinhardt, J.; Grigorieff, N. Structural Polymorphism of Alzheimer Aβ and Other Amyloid Fibrils Prion 2009, 3, 89-93
21. 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
22. Berryman, J. T.; Radford, S. E.; Harris, S. A. Systematic Examination of Polymorphism in Amyloid Fibrils by Molecular-Dynamics Simulation Biophys. J. 2011, 100, 2234-2242
23. Nguyen, H. D.; Hall, C. K. Molecular Dynamics Simulations of Spontaneous Fibril Formation by Random-Coil Peptides Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 16180-16185
24. Pellarin, R.; Caflisch, A. Interpreting the Aggregation Kinetics of Amyloid Peptides J. Mol. Biol. 2006, 360, 882-892
25. Pellarin, R.; Guarnera, E.; Caflisch, A. Pathways and Intermediates of Amyloid Fibril Formation J. Mol. Biol. 2007, 374, 917-924
26. Chebaro, Y.; Derreumaux, P. Targeting the Early Steps of Aβ16-22 Protofibril Disassembly by N-Methylated Inhibitors: A Numerical Study Proteins 2009, 75, 442-452
27. Shea, J.-E.; Urbanc, B. Insights into Aβ Aggregation: A Molecular Dynamics Perspective Curr. Top. Med. Chem. 2012, 12, 2596-2610
28. Mu, Y.; Gao, Y. Q. Self-Assembly of Polypeptides into Left-Handedly Twisted Fibril-Like Structures Phys. Rev. E 2009, 80, 041927
29. 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
30. Baftizadeh, F.; Pietrucci, F.; Biarnes, X.; Laio, A. Nucleation Process of a Fibril Precursor in the C-Terminal Segment of Amyloid-Beta Phys. Rev. Lett. 2013, 110, 168103
31. Nguyen, P. H.; Derreumaux, P. Conformational Ensemble and Polymorphism of the All-Atom Alzheimers Aβ37-42 Amyloid Peptide Oligomers J. Phys. Chem. B 2013, 117, 5831-5840
32. Chiti, F.; Webster, P.; Taddei, N.; Clark, A.; Stefani, M.; Ramponi, G.; Dobson, C. M. Designing Conditions for in Vitro Formation of Amyloid Protofilaments and Fibrils Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3590-3594
33. Chiti, F.; Bucciantini, M.; Capanni, C.; Taddei, N.; Dobson, C. M.; Stefani, M. Solution Conditions Can Promote Formation of Either Amyloid Protofilaments or Mature Fibrils from the HypF N-Terminal Domain Protein Sci. 2001, 10, 2541-2547
34. Zurdo, J.; Guijarro, J. I.; Jiménez, J. L.; Saibil, H. R.; Dobson, C. M. Dependence on Solution Conditions of Aggregation and Amyloid Formation by an SH3 Domain J. Mol. Biol. 2001, 311, 325-340
35. Yoshimura, Y.; Lin, Y. X.; Yagi, H.; Lee, Y. H.; Kitayama, H.; Sakurai, K.; So, M.; Ogi, H.; Naiki, H.; Goto, Y. Distinguishing Crystal-Like Amyloid Fibrils and Glass-Like Amorphous Aggregates from Their Kinetics of Formation Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 14446-14451
36. Bowman, G. R.; Beauchamp, K. A.; Boxer, G.; Pande, V. S. Progress and Challenges in the Automated Construction of Markov State Models for Full Protein Systems J. Chem. Phys. 2009, 131, 124101
37. Bowman, G. R.; Huang, X.; Pande, V. S. Using Generalized Ensemble Simulations and Markov State Models to Identify Conformational States Methods 2009, 49, 197-201
38. Bowman, G. R.; Huang, X.; Pande, V. S. Network Models for Molecular Kinetics and Their Initial Applications to Human Health Cell Res. 2010, 20, 622-630
39. Huang, X.; Bowman, G. R.; Bacallado, S.; Pande, V. S. Rapid Equilibrium Sampling Initiated from Nonequilibrium Data Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 19765-19769
40. Noé, F.; Krachtus, D.; Smith, J. C.; Fischer, S. Transition Networks for the Comprehensive Characterization of Complex Conformational Change in Proteins J. Chem. Theory Comput. 2006, 2, 840-857
41. Noé, F.; Horenko, I.; Schutte, C.; Smith, J. C. Hierarchical Analysis of Conformational Dynamics in Biomolecules: Transition Networks of Metastable States J. Chem. Phys. 2007, 126, 155102
42. Noé, F.; Fischer, S. Transition Networks for Modeling the Kinetics of Conformational Change in Macromolecules Curr. Opin. Struct. Biol. 2008, 18, 154-162
43. Lu, Y.; Derreumaux, P.; Guo, Z.; Mousseau, N.; Wei, G. Thermodynamics and Dynamics of Amyloid Peptide Oligomerization Are Sequence Dependent Proteins 2009, 75, 954-963
44. Matthes, D.; Gapsys, V.; Daebel, V.; de Groot, B. L. Mapping the Conformational Dynamics and Pathways of Spontaneous Steric Zipper Peptide Oligomerization PLoS One 2011, 6, e19129
45. Paci, E.; Gsponer, J.; Salvatella, X.; Vendruscolo, M. Molecular Dynamics Studies of the Process of Amyloid Aggregation of Peptide Fragments of Transthyretin J. Mol. Biol. 2004, 340, 555-569
46. Riccardi, L.; Nguyen, P. H.; Stock, G. Construction of the Free Energy Landscape of Peptide Aggregation from Molecular Dynamics Simulations J. Chem. Theory Comput. 2012, 8, 1471-1479
47. Qiao, Q.; Bowman, G. R.; Huang, X. Dynamics of an Intrinsically Disordered Protein Reveal Metastable Conformations That Potentially Seed Aggregation J. Am. Chem. Soc. 2013, 135, 16092-16101
48. Vanden-Eijnden, E. Transition Path Theory. In Computer Simulations in Condensed Matter Systems: From Materials to Chemical Biology, Ferrario, M.; Ciccotti, G.; Binder, K., Eds.; Springer-Verlag: Berlin, Germany, 2006; Vol. 703, pp 453-493.
49. Metzner, P.; Schutte, C.; Vanden-Eijnden, E. Transition Path Theory for Markov Jump Processes Multiscale Model. Simul. 2009, 7, 1192-1219
50. Noé, F.; Schutte, C.; Vanden-Eijnden, E.; Reich, L.; Weikl, T. R. Constructing the Equilibrium Ensemble of Folding Pathways from Short off-Equilibrium Simulations Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 19011-19016
51. E, W.; Vanden-Eijnden, E. Transition-Path Theory and Path-Finding Algorithms for the Study of Rare Events Annu. Rev. Phys. Chem. 2010, 61, 391-420
52. E, W.; Vanden-Eijnden, E. Towards a Theory of Transition Paths J. Stat. Phys. 2006, 123, 503-523
53. Gao, Y. Q. An Integrate-over-Temperature Approach for Enhanced Sampling J. Chem. Phys. 2008, 128, 064105
54. Gao, Y. Q. Self-Adaptive Enhanced Sampling in the Energy and Trajectory Spaces: Accelerated Thermodynamics and Kinetic Calculations J. Chem. Phys. 2008, 128, 134111
55. Still, W. C.; Tempczyk, A.; Hawley, R. C.; Hendrickson, T. Semianalytical Treatment of Solvation for Molecular Mechanics and Dynamics J. Am. Chem. Soc. 1990, 112, 6127-6129
56. Qiu, D.; Shenkin, P. S.; Hollinger, F. P.; Still, W. C. The GB/SA Continuum Model for Solvation. A Fast Analytical Method for the Calculation of Approximate Born Radii J. Phys. Chem. A 1997, 101, 3005-3014
57. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Merz, K. M.; Pearlman, D. A.; Crowley, M.; AMBER 9; University of California: San Francisco, CA, 2006.
58. Kollman, P.; Dixon, R.; Cornell, W.; Fox, T.; Chipot, C.; Pohorille, A. The Development/Application of a Minimalist Organic/Biochemical Molecular Mechanic Force Field Using a Combination of Ab Initio Calculations and Experimental Data. In Computer Simulation of Biomolecular Systems: Theoretical and Experimental Applications; van Gunsteren, W. F.; Weiner, P. K.; Wilkinson, A. J., Eds.; Kluwer: Dordrecht, The Netherlands, 1997; Vol. 3, pp 83-96.
59. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A Second Generation Force-Field for the Simulation of Proteins, Nucleic-Acids, and Organic-Molecules J. Am. Chem. Soc. 1995, 117, 5179-5197
60. Price, D. J.; Brooks, C. L. A Modified TIP3P Water Potential for Simulation with Ewald Summation J. Chem. Phys. 2004, 121, 10096-10103
61. Case, D.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C.; Wang, J.; Duke, R.; Luo, R.; Crowley, M.; Walker, R.; Zhang, W.; AMBER 11; University of California: San Francisco, CA, 2010.
62. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters Proteins 2006, 65, 712-725
63. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. C. Numerical-Integration of Cartesian Equations of Motion of a System with Constraints-Molecular-Dynamics of N-Alkanes J. Comput. Phys. 1977, 23, 327-341
64. Sanderson, C. Armadillo: An Open Source C++ Linear Algebra Library for Fast Prototyping and Computationally Intensive Experiments, Technical Report; NICTA: Australia, 2010.
65. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics Modell. 1996, 14, 33-38
66. Gansner, E. R.; North, S. C. An Open Graph Visualization System and Its Applications to Software Engineering Software Pract. Exper. 2000, 30, 1203-1233
67. Tarjan, R. Depth-First Search and Linear Graph Algorithms SIAM J. Comput. 1972, 1, 146-160
68. Lewis, G. N.; Boynton, N. J.; Burton, F. W. Expected Complexity of Fast Search with Uniformly Distributed Data Inform. Process. Lett. 1981, 13, 4-7
69. Nelson, R.; Eisenberg, D. Recent Atomic Models of Amyloid Fibril Structure Curr. Opin. Struct. Biol. 2006, 16, 260-265
70. Chang, L.-K.; Zhao, J.-H.; Liu, H.-L.; Liu, K.-T.; Chen, J.-T.; Tsai, W.-B.; Ho, Y. Molecular Dynamics Simulations to Investigate the Structural Stability and Aggregation Behavior of the GGVVIA Oligomers Derived from Amyloid β Peptide J. Biomol. Struct. Dyn. 2009, 26, 731-740
71. Nasica-Labouze, J.; Meli, M.; Derreumaux, P.; Colombo, G.; Mousseau, N. A Multiscale Approach to Characterize the Early Aggregation Steps of the Amyloid-Forming Peptide GNNQQNY from the Yeast Prion Sup-35 PLoS Comput. Biol. 2011, 7, e1002051
72. Yang, L.; Shao, Q.; Gao, Y. Q. Thermodynamics and Folding Pathways of Trpzip2: An Accelerated Molecular Dynamics Simulation Study J. Phys. Chem. B 2008, 113, 803-808
73. Yang, L.; Shao, Q.; Gao, Y. Q. Comparison between Integrated and Parallel Tempering Methods in Enhanced Sampling Simulations J. Chem. Phys. 2009, 130, 124111
74. Zhang, C.; Ma, J. Enhanced Sampling and Applications in Protein Folding in Explicit Solvent J. Chem. Phys. 2010, 132, 244101