Minimal model for self-catalysis in the formation of amyloid-like elongated fibrils

Journal of Physical Chemistry Letters

Volumn 4, Issue 18, 2013, Pages 3158-3164

  Di Michele, Lorenzo ^a   Eiser, Erika ^a   Foderà, Vito ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

amyloid like fibrils; conformational changes; Monte Carlo simulations; secondary nucleation; self catalysis

Indexed keywords

AMYLOID-LIKE FIBRIL; COMPUTATIONAL APPROACH; CONFORMATIONAL CHANGE; CONFORMATIONAL EQUILIBRIUM; METROPOLIS MONTE CARLO; PROTEIN CONCENTRATIONS; SECONDARY NUCLEATION; SELF-CATALYSIS;

AGGLOMERATION; CATALYSIS; CONFORMATIONS; GLYCOPROTEINS; MONTE CARLO METHODS;

PROTEINS;

EID: 84884560406     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz401600g     Document Type: Article

References (46)

1. 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
2. Vendruscolo, M.; Zurdo, J.; MacPhee, C. E.; Dobson, C. M. Protein Folding ad Misfolding: a Paradigm of Self-Assembly and Regulation in Complex Biological System Phil. Trans. R. Soc. London, Ser. A 2003, 361, 1205-1222
3. Griffin, M. D. W.; Mok, M. L. Y.; Wilson, L. M.; Pham, C. L. L.; Waddington, L. J.; Perugini, M. A.; Howlett, G. J. Phospholipid Interaction Induces Molecular-Level Polymorphism in Apolipoprotein C-II Amyloid Fibrils via Alternative Assembly Pathways J. Mol. Biol. 2008, 375, 240-256
4. Pellarin, R.; Caflisch, A. Interpreting the Aggregation Kinetics of Amyloid Peptides J. Mol. Biol. 2006, 360, 882-892
5. Friedman, R.; Pellarin, R.; Caflisch, A. Amyloid Aggregation on Lipid Bilayers and Its Impact on Membrane Permeability J. Mol. Biol. 2009, 387, 407-415
6. Friedman, R.; Pellarin, R.; Caflisch, A. Soluble Protofibrils as Metastable Intermediates in Simulations of Amyloid Fibril Degradation Induced by Lipid Vesicles J. Phys. Chem. Lett. 2009, 1, 471-474
7. Gaspari, R.; Gliozzi, A.; Ferrando, R. Aggregation Phenomena in a System of Molecules with Two Internal States Phys. Rev. E 2007, 76, 041604
8. Strodel, B.; Wales, D. J. Implicit Solvent Models and the Energy Landscape for Aggregation of the Amyloidogenic KFFE Peptide J. Chem. Theory Comput. 2008, 4, 657-672
9. Vacha, R.; Frenkel, D. Relation between Molecular Shape and the Morphology of Self-Assembling Aggregates: A Simulation Study Biophys. J. 2011, 101, 1432-1439
10. Irbäck, A.; Jónsson, S. Æ.; Linnemann, N.; Linse, B.; Wallin, S. Aggregate Geometry in Amyloid Fibril Nucleation Phys. Rev. Lett. 2013, 110, 058101
11. Bieler, N. S.; Knowles, T. P. J.; Frenkel, D.; Vacha, R. Connecting Macroscopic Observables and Microscopic Assembly Events in Amyloid Formation Using Coarse Grained Simulations PLoS Comput. Biol. 2012, 8, e1002692
12. Whitelam, S.; Rogers, C.; Pasqua, A.; Paavola, C.; Trent, J.; Geissler, P. L. The Impact of Conformational Fluctuations on Self-Assembly: Cooperative Aggregation of Archaeal Chaperonin Proteins Nano Lett. 2009, 9, 292-297
13. 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
14. Baiesi, M.; Seno, F.; Trovato, A. Fibril Elongation Mechanisms of HET-s Prion-Forming Domain: Topological Evidence for Growth Polarity Proteins: Struct., Funct., Bioinf. 2011, 79, 3067-3081
15. Buell, A. K.; Blundell, J. R.; Dobson, C. M.; Welland, M. E.; Terentjev, E. M.; Knowles, T. P. J. Frequency Factors in a Landscape Model of Filamentous Protein Aggregation Phys. Rev. Lett. 2010, 104, 228101
16. Wu, C.; Shea, J.-E. Coarse-Grained Models for Protein Aggregation Curr. Opin. Struct. Biol. 2011, 21, 209-220
17. Yong, W.; Lomakin, A.; Kirkitadze, M. D.; Teplow, D. B.; Chen, S.-H.; Benedek, G. B. Structure Determination of Micelle-Like Intermediates in Amyloid β-Protein Fibril Assembly by Using Small Angle Neutron Scattering Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 150-154
18. Lomakin, A.; Chung, D. S.; Benedek, G. B.; Kirschner, D. A.; Teplow, D. B. On the Nucleation and Growth of Amyloid β-Protein Fibrils: Detection of Nuclei and Quantitation of Rate Constants Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 1125-1129
19. Li, M. S.; Klimov, D. K.; Straub, J. E.; Thirumalai, D. Probing the Mechanisms of Fibril Formation Using Lattice Models J. Chem. Phys. 2008, 129, 175101/1-175101/10
20. Li, M. S.; Co, N. T.; Reddy, G.; Hu, C.-K.; Straub, J. E.; Thirumalai, D. Factors Governing Fibrillogenesis of Polypeptide Chains Revealed by Lattice Models Phys. Rev. Lett. 2010, 105, 218101
21. Massi, F.; Klimov, D.; Thirumalai, D.; Straub, J. E. Charge States Rather than Propensity for β-Structure Determine Enhanced Fibrillogenesis in Wild-Type Alzheimer's-Amyloid Peptide Compared to E22Q Dutch Mutant Protein Sci. 2002, 11, 1639-1647
22. Vetri, V.; Militello, V. Thermal Induced Conformational Changes Involved in the Aggregation Pathways of β-Lactoglobulin Biophys. Chem. 2005, 113, 83-91
23. Vetri, V.; Canale, C.; Relini, A.; Librizzi, F.; Militello, V.; Gliozzi, A.; Leone, M. Amyloid Fibrils Formation and Amorphous Aggregation in Concanavalin A Biophys. Chem. 2007, 125, 184-190
24. Vetri, V.; D'Amico, M.; Foderà, V.; Leone, M.; Ponzoni, A.; Sberveglieri, G.; Militello, V. Bovine Serum Albumin Protofibril-Like Aggregates Formation: Solo but Not Simple Mechanism Arch. Biochem. Biophys. 2011, 508, 13-24
25. Librizzi, F.; Foderà, V.; Vetri, V.; Lo Presti, C.; Leone, M. Effects of Confinement on Insulin Amyloid Fibrils Formation Eur. Biophys. J. 2007, 36, 711-715
26. Foderà, V.; Librizzi, F.; Groenning, M.; van de Weert, M.; Leone, M. Secondary Nucleation and Accessible Surface in Insulin Amyloid Fibril Formation J. Phys. Chem. B 2008, 112, 3853-3858
27. Foderà, V.; van de Weert, M.; Vestergaard, B. Large-Scale Polymorphism and Auto-Catalytic Effect in Insulin Fibrillogenesis Soft Matter 2010, 6, 4413-4419
28. Knowles, T. P. J.; Waudby, C. A.; Devlin, G. L.; Cohen, S. I. A.; Aguzzi, A.; Vendruscolo, M.; Terentjev, E. M.; Welland, M. E.; Dobson, C. M. An Analytical Solution to the Kinetics of Breakable Filament Assembly Science 2009, 326, 1533-1537
29. Cohen, S. I. A.; Linse, S.; Luheshi, L. M.; Hellstrand, E.; White, D. A.; Rajah, L.; Otzen, D. E.; Vendruscolo, M.; Dobson, C. M.; Knowles, T. P. J. Proliferation of Amyloid-β42 Aggregates Occurs through a Secondary Nucleation Mechanism Proc. Natl. Acad. Sci. U.S.A. 2013, 10.1073/pnas.1218402110
30. Wood, S. J.; Maleeff, B.; Hart, T.; Wetzel, R. Physical, Morphological and Functional Differences between pH 5.8 and 7.4 Aggregates of the Alzheimer's Amyloid Peptide Aβ J. Mol. Biol. 1996, 256, 870-877
31. Schmittschmitt, J. P.; Scholtz, J. M. The Role of Protein Stability, Solubility, and Net Charge in Amyloid Fibril Formation Protein Sci. 2003, 12, 2374-2378
32. Hoyer, W.; Antony, T.; Cherny, D.; Heim, G.; Jovin, T. M.; Subramaniam, V. Dependence of α-Synuclein Aggregate Morphology on Solution Conditions J. Mol. Biol. 2002, 322, 383-393
33. Haas, J.; Vöhringer-Martinez, E.; Bögehold, A.; Matthes, D.; Hensen, U.; Pelah, A.; Abel, B.; Grubmüller, H. Primary Steps of pH-Dependent Insulin Aggregation Kinetics Are Governed by Conformational Flexibility ChemBioChem 2009, 10, 1742-1742
34. Smith, M. I.; Foderà, V.; Sharp, J. S.; Roberts, C. J.; Donald, A. M. Factors Affecting the Formation of Insulin Amyloid Spherulites Colloids Surf., B 2012, 89, 216-222
35. Fändrich, M. Absolute Correlation between Lag Time and Growth Rate in the Spontaneous Formation of Several Amyloid-Like Aggregates and Fibrils J. Mol. Biol. 2007, 365, 1266-1270
36. Jansen, R.; Dzwolak, W.; Winter, R. Amyloidogenic Self-Assembly of Insulin Aggregates Probed by High Resolution Atomic Force Microscopy Biophys. J. 2005, 88, 1344-1353
37. Ferrone, F. A.; Hofrichter, J.; Eaton, W. A. Kinetics of Sickle Hemoglobin Polymerization: I. Studies Using Temperature-Jump and Laser Photolysis Techniques J. Mol. Biol. 1985, 183, 591-610
38. Ferrone, F. A.; Hofrichter, J.; Eaton, W. A. Kinetics of Sickle Hemoglobin Polymerization: II. A Double Nucleation Mechanism J. Mol. Biol. 1985, 183, 611-631
39. Foderà, V.; Cataldo, S.; Librizzi, F.; Pignataro, B.; Spiccia, P.; Leone, M. Self-Organization Pathways and Spatial Heterogeneity in Insulin Amyloid Fibril Formation J. Phys. Chem. B 2009, 113, 10830-10837
40. O'Brien, E. P.; Okamoto, Y.; Straub, J. E.; Brooks, B. R.; Thirumalai, D. Thermodynamic Perspective on the Dock-Lock Growth Mechanism of Amyloid Fibrils J. Phys. Chem. B 2009, 113, 14421-14430
41. Foderà, V.; Zaccone, A.; Lattuada, M.; Donald, A. M. Electrostatics Controls the Formation of Amyloid Superstructures in Protein Aggregation Phys. Rev. Lett. 2013, 111, 108105
42. Kikuchi, K.; Yoshida, M.; Maekawa, T.; Watanabe, H. Metropolis Monte Carlo Method as a Numerical Technique to Solve the Fokker-Planck Equation Chem. Phys. Lett. 1991, 185, 335-338
43. Fichthorn, K. A.; Weinberg, W. H. Theoretical Foundations of Dynamical Monte Carlo Simulations J. Chem. Phys. 1991, 95, 1090-1096
44. Whitelam, S.; Geissler, P. L. Avoiding Unphysical Kinetic Traps in Monte Carlo Simulations of Strongly Attractive Particles J. Chem. Phys. 2007, 127, 154101
45. Sanz, E.; Marenduzzo, D. Dynamic Monte Carlo versus Brownian Dynamics: A Comparison for Self-Diffusion and Crystallization in Colloidal Fluids J. Chem. Phys. 2010, 132, 194102-7
46. Bora, R. P.; Prabhakar, R. Translational, Rotational and Internal Dynamics of Amyloid β-Peptides (Aβ40 and Aβ42) from Molecular Dynamics Simulations J. Chem. Phys. 2009, 131, 155103/1-133103/11