A kinetic approach to the sequence-aggregation relationship in disease-related protein assembly

Journal of Physical Chemistry B

Volumn 118, Issue 4, 2014, Pages 1003-1011

  Barz, Bogdan ^a   Wales, David J ^b   Strodel, Birgit ^a,c  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DIMERS; MOLECULAR DYNAMICS; MONOMERS;

AGGREGATION STATE; AMYLOIDOGENIC PROTEINS; CHARGED AMINO ACIDS; DISCONNECTIVITY GRAPHS; FIRST PASSAGE TIME DISTRIBUTIONS; MOLECULAR DYNAMICS SIMULATIONS; PEPTIDE AGGREGATION; PRIMARY STRUCTURES;

PEPTIDES;

AMYLOID PROTEIN;

ARTICLE; CHEMISTRY; DEGENERATIVE DISEASE; KINETICS; MOLECULAR DYNAMICS; PROTEIN FOLDING;

AMYLOIDOGENIC PROTEINS; KINETICS; MOLECULAR DYNAMICS SIMULATION; NEURODEGENERATIVE DISEASES; PROTEIN FOLDING;

EID: 84893468812     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp412648u     Document Type: Article

References (62)

1. Hardy, J.; Selkoe, D. J. The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics Science 2002, 297, 353-356
2. Kirkitadze, M. D.; Bitan, G.; Teplow, D. B. Paradigm Shifts in Alzheimer's Disease and Other Neurodegenerative Disorders: The Emerging Role of Oligomeric Assemblies J. Neurosci. Res. 2002, 69, 567-577
3. Silveira, J. R.; Raymond, G. J.; Hughson, A. G.; Race, R. E.; Sim, V. L.; Hayes, S. F.; Caughey, B. The Most Infectious Prion Protein Particles Nature 2005, 437, 257-261
4. Haass, C.; Selkoe, D. J. Soluble Protein Oligomers in Neurodegeneration: Lessons from the Alzheimer's Amyloid β -Peptide Nat. Rev. Mol. Cell Biol. 2007, 8, 101-112
5. Klein, W. L.; Stine, W. B.; Teplow, D. B. Small Assemblies of Unmodified Amyloid β -Protein are the Proximate Neurotoxin in Alzheimer's Disease Neurobiol. Aging 2004, 25, 569-580
6. Bitan, G.; Kirkitadze, M. D.; Lomakin, A.; Vollers, S. S.; Benedek, G. B.; Teplow, D. B. Amyloid β -Protein (A β) Assembly: A β 40 and A β 42 Oligomerize through Distinct Pathways Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 330-335
7. Urbanc, B.; Betnel, M.; Cruz, L.; Bitan, G.; Teplow, D. B. Elucidation of Amyloid β -Protein Oligomerization Mechanisms: Discrete Molecular Dynamics Study J. Am. Chem. Soc. 2010, 132, 4266-4280
8. Barz, B.; Urbanc, B. Dimer Formation Enhances Structural Differences between Amyloid β -Protein (1-40) and (1-42): An Explicit-Solvent Molecular Dynamics Study PLoS One 2012, 7, e34345
9. Melquiond, A.; Dong, X.; Mousseau, N.; Derreumaux, P. Role of the Region 23-28 in A β Fibril Formation: Insights from Simulations of the Monomers and Dimers of Alzheimer's Peptides A β 40 and A β 42 Curr. Alzheimer. Res. 2008, 5, 244-250
10. Sekijima, M.; Motono, C.; Yamasaki, S.; Kaneko, K.; Akiyama, Y. Molecular Dynamics Simulation of Dimeric and Monomeric Forms of Human Prion Protein: Insight into Dynamics and Properties Biophys. J. 2003, 85, 1176-1185
11. Balbirnie, M.; Grothe, R.; Eisenberg, D. S. An Amyloid-Forming Peptide from the Yeast Prion Sup35 Reveals a Dehydrated β -Sheet Structure for Amyloid Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 2375-2380
12. Yvinec, R.; D'Orsogna, M. R.; Chou, T. First Passage Times in Homogeneous Nucleation and Self-Assembly J. Chem. Phys. 2012, 137, 244107
13. Wales, D. J. Energy Landscapes: Some New Horizons Curr. Opin. Struct. Biol. 2010, 20, 3-10
14. Strodel, B.; Whittleston, C. S.; Wales, D. J. Thermodynamics and Kinetics of Aggregation for the GNNQQNY Peptide J. Am. Chem. Soc. 2007, 129, 16005-16014
15. Becker, O. M.; Karplus, M. The Topology of Multidimensional Potential Energy Surfaces: Theory and Application to Peptide Structure and Kinetics J. Chem. Phys. 1997, 106, 1495-1517
16. Wales, D. J.; Miller, M. A.; Walsh, T. R. Archetypal Energy Landscapes Nature 1998, 394, 758-760
17. Krivov, S. V.; Karplus, M. Hidden Complexity of Free Energy Surfaces for Peptide (Protein) Folding Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 14766-14770
18. Rao, F.; Karplus, M. Protein Dynamics Investigated by Inherent Structure Analysis Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 9152-9157
19. Baba, A.; Komatsuzaki, T. Construction of Effective Free Energy Landscape from Single-Molecule Time Series Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 19297-19302
20. Gfeller, D.; Rios, P. D. L.; Caflisch, A.; Rao, F. Complex Network Analysis of Free-Energy Landscapes Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1817-1822
21. 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
22. Nelson, R.; Sawaya, M. R.; Balbirnie, M.; Madsen, A.; Riekel, C.; Grothe, R.; Eisenberg, D. Structure of the Cross- β Spine of Amyloid-like Fibrils Nature 2005, 435, 773-778
23. Nasica-Labouze, J.; Mousseau, N. Kinetics of Amyloid Aggregation: A Study of the GNNQQNY Prion Sequence PLoS Comput. Biol. 2012, 8, e1002782
24. 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
25. Ford, L. R.; Fulkerson, D. R. Maximal Flow through a Network Can. J. Math. 1956, 8, 399-404
26. Krivov, S. V.; Karplus, M. Free Energy Disconnectivity Graphs: Application to Peptide Models J. Chem. Phys. 2002, 117, 10894-10903
27. Gomory, R. E.; Hu, T. C. Multi-Terminal Network Flows J. Soc. Ind. Appl. Math. 1961, 9, 551-570
28. Cheon, M.; Chang, I.; Hall, C. K. Spontaneous Formation of Twisted A β (16-22) Fibrils in Large-Scale Molecular-Dynamics Simulations Biophys. J. 2011, 101, 2493-2501
29. Osborne, K. L.; Bachmann, M.; Strodel, B. Thermodynamic Analysis of Structural Transitions During GNNQQNY Aggregation Proteins 2013, 81, 1141-1155
30. Gsponer, J.; Haberthr, U.; Caflisch, A. The Role of Side-Chain Interactions in the Early Steps of Aggregation: Molecular Dynamics Simulations of an Amyloid-Forming Peptide from the Yeast Prion Sup35 Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 5154-5159
31. Vitagliano, L.; Esposito, L.; Pedone, C.; De Simone, A. Stability of Single Sheet GNNQQNY Aggregates Analyzed by Replica Exchange Molecular Dynamics: Antiparallel Versus Parallel Association Biochem. Biophys. Res. Commun. 2008, 377, 1036-1041
32. Nguyen, P. H.; Li, M. S.; Stock, G.; Straub, J. E.; Thirumalai, D. Monomer Adds to Preformed Structured Oligomers of A β -Peptides by a Two-Stage Dock-Lock Mechanism Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 111-116
33. Berendsen, H. J. C.; Postma, J. P. M.; Gunsteren, W. F. v.; Hermans, J. Interaction Models for Water in Relation to Protein Hydration. In Intermolecular Forces; Pullman, B., Ed.; The Jerusalem Symposia on Quantum Chemistry and Biochemistry 14; Springer: Houten, The Netherlands, 1981; pp 331-342.
34. 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
35. Scott, W. R. P.; Hnenberger, P. H.; Tironi, I. G.; Mark, A. E.; Billeter, S. R.; Fennen, J.; Torda, A. E.; Huber, T.; Krger, P.; van Gunsteren, W. F. The GROMOS Biomolecular Simulation Program Package J. Phys. Chem. A 1999, 103, 3596-3607
36. Feenstra, K. A.; Hess, B.; Berendsen, H. J. C. Improving Efficiency of Large Time-Scale Molecular Dynamics Simulations of Hydrogen-Rich Systems J. Comput. Chem. 1999, 20, 786-798
37. Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling J. Chem. Phys. 2007, 126, 014101
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. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An N×log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
40. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method J. Chem. Phys. 1995, 103, 8577-8593
41. 16-22 Amyloid Peptides into Antiparallel β Sheets Structure 2003, 11, 295-307
42. Brandes, U.; Wagner, D. Visone-Analysis and Visualization of Social Networks. Graph Drawing Software; Springer-Verlag Berlin: Heidelberg, Germany, 2003; pp 321-340.
43. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
44. Baftizadeh, F.; Pietrucci, F.; Biarns, X.; Laio, A. Nucleation Process of a Fibril Precursor in the C-Terminal Segment of Amyloid- β Phys. Rev. Lett. 2013, 110, 168103
45. 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
46. 16-22 Aggregates Protein Sci. 2012, 21, 1837-1848
47. Laganowsky, A.; Liu, C.; Sawaya, M. R.; Whitelegge, J. P.; Park, J.; Zhao, M.; Pensalfini, A.; Soriaga, A. B.; Landau, M.; Teng, P. K. Atomic View of a Toxic Amyloid Small Oligomer Science 2012, 335, 1228-1231
48. Liu, C.; Zhao, M.; Jiang, L.; Cheng, P.-N.; Park, J.; Sawaya, M. R.; Pensalfini, A.; Gou, D.; Berk, A. J.; Glabe, C. G. Out-of-Register β -Sheets Suggest a Pathway to Toxic Amyloid Aggregates Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 20913-20918
49. Berhanu, W. M.; Hansmann, U. H. E. The Stability of Cylindrin β -Barrel Amyloid Oligomer Models-A Molecular Dynamics Study Proteins 2013, 81, 1542-1555
50. Xie, L.; Luo, Y.; Wei, G. A β (16-22) Peptides Can Assemble into Ordered β -Barrels and Bilayer β -Sheets, while Substitution of Phenylalanine 19 by Tryptophan Increases the Population of Disordered Aggregates J. Phys. Chem. B 2013, 117, 10149-10160
51. Mehta, A. K.; Lu, K.; Childers, W. S.; Liang, Y.; Dublin, S. N.; Dong, J.; Snyder, J. P.; Pingali, S. V.; Thiyagarajan, P.; Lynn, D. G. Facial Symmetry in Protein Self-Assembly J. Am. Chem. Soc. 2008, 130, 9829-9835
52. Reddy, A. S.; Chopra, M.; de Pablo, J. J. GNNQQNY-Investigation of Early Steps during Amyloid Formation Biophys. J. 2010, 98, 1038-1045
53. Hwang, W.; Zhang, S.; Kamm, R. D.; Karplus, M. Kinetic Control of Dimer Structure Formation in Amyloid Fibrillogenesis Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 12916-12921
54. Meli, M.; Morra, G.; Colombo, G. Investigating the Mechanism of Peptide Aggregation: Insights from Mixed Monte Carlo-Molecular Dynamics Simulations Biophys. J. 2008, 94, 4414-4426
55. Zhang, Z.; Chen, H.; Bai, H.; Lai, L. Molecular Dynamics Simulations on the Oligomer-Formation Process of the GNNQQNY Peptide from Yeast Prion Protein Sup35 Biophys. J. 2007, 93, 1484-1492
56. Berryman, J. T.; Radford, S. E.; Harris, S. A. Thermodynamic Description of Polymorphism in Q- and N-Rich Peptide Aggregates Revealed by Atomistic Simulation Biophys. J. 2009, 97, 1-11
57. Park, J.; Kahng, B.; Hwang, W. Thermodynamic Selection of Steric Zipper Patterns in the Amyloid Cross- β Spine. PLoS Comput. Biol. 2009, 5.
58. Collins, S. R.; Douglass, A.; Vale, R. D.; Weissman, J. S. Mechanism of Prion Propagation: Amyloid Growth Occurs by Monomer Addition PLoS Biol. 2004, 2, e321
59. Narayanan, S.; Walter, S.; Reif, B. Yeast Prion-Protein, Sup35, Fibril Formation Proceeds by Addition and Substraction of Oligomers ChemBioChem 2006, 7, 757-765
60. Petkova, A. T.; Leapman, R. D.; Guo, Z.; Yau, W.-M.; Mattson, M. P.; Tycko, R. Self-Propagating, Molecular-Level Polymorphism in Alzheimer's β-Amyloid Fibrils Science 2005, 307, 262-265
61. 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 Aetiology of Alzheimer's Disease Nat. Chem. 2009, 1, 326-331
62. 1-42 Oligomers to Fibrils Nat. Struct. Mol. Biol. 2010, 17, 561-567