Mechanical deformation mechanisms and properties of amyloid fibrils

Physical Chemistry Chemical Physics

Volumn 17, Issue 2, 2015, Pages 1379-1389

  Choi, Bumjoon ^a   Yoon, Gwonchan ^b,c   Lee, Sang Woo ^a   Eom, Kilho ^d  

^a Yonsei University Wonju   (South Korea)

^b Boston University   (United States)

^c Korea University   (South Korea)

^d Sungkyunkwan University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID;

BIOMECHANICS; CHEMISTRY; ELASTICITY; MECHANICS; MOLECULAR DYNAMICS; PROTEIN SECONDARY STRUCTURE;

AMYLOID; BIOMECHANICAL PHENOMENA; ELASTICITY; MECHANICAL PROCESSES; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84916631559     PISSN: 14639076     EISSN: None     Source Type: Journal    
DOI: 10.1039/c4cp03804e     Document Type: Article

References (63)

1. I. Cherny and E. Gazit, Amyloids: Not Only Pathological Agents but Also Ordered Nanomaterials, Angew. Chem., Int. Ed., 2008, 47, 4062.
2. R. Mezzenga and P. Fischer, The self-assembly, aggregation and phase transitions of food protein systems in one, two and three dimensions, Rep. Prog. Phys., 2013, 76, 046601.
3. G. Merlini and V. Bellotti, Molecular Mechanisms of Amyloidosis, N. Engl. J. Med., 2003, 349, 583.
4. M. B. Pepys, Amyloidosis, Annu. Rev. Med., 2006, 57, 223.
5. J. W. M. Hoppener, B. Ahren and C. J. M. Lips, Islet Amyloid and Type 2 Diabetes Mellitus, N. Engl. J. Med., 2000, 343, 411.
6. A. Clark and J. Moffitt, Pancreatic Islet Amyloid and Diabetes, in Protein Misfolding, Aggregation, and Conformational Diseases, ed. V. N. Uversky and A. Fink, Springer, New York, 2007.
7. G. J. S. Cooper, A. C. Willis, A. Clark, R. C. Turner, R. B. Sim and K. B. M. Reid, Purification and characterization of a peptide from amyloid-rich pancreas of type 2 diabetic patients, Proc. Natl. Acad. Sci. U. S. A., 1987, 84, 8628.
8. P. Westermark, C. Wernstedt, E. Wilander, D. W. Hayden, T. D. O'Brien and K. H. Johnson, Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells, Proc. Natl. Acad. Sci. U. S. A., 1987, 84, 3881.
9. J. T. Nielsen, M. Bjerring, M. D. Jeppesen, R. O. Pedersen, J. M. Pedersen, K. L. Hein, T. Vosegaard, T. Skrydstrup, D. E. Otzen and N. C. Nielsen, Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy, Angew. Chem., Int. Ed., 2009, 48, 2118.
10. T. P. J. Knowles and M. J. Buehler, Nanomechanics of functional and pathological amyloid materials, Nat. Nanotechnol., 2011, 6, 469.
11. T. P. Knowles, A. W. Fitzpatrick, S. Meehan, H. R. Mott, M. Vendruscolo, C. M. Dobson and M. E. Welland, Role of Intermolecular Forces in Defining Material Properties of Protein Nanofibrils, Science, 2007, 318, 1900.
12. M. Sotomayor and K. Schulten, Single-Molecule Experiments in Vitro and in Silico, Science, 2007, 316, 1144.
13. K. Eom, Mechanical Characterization of Protein Materials, in Simulations in Nanobiotechnology, ed. K. Eom, CRC Press, Boca Raton, FL, 2013, ch. 7, p. 221.
14. K. Eom, P. C. Li, D. E. Makarov and G. J. Rodin, Relationship between the Mechanical Properties and Topology of Cross-Linked Polymer Molecules: Parallel Strands Maximize the Strength of Model Polymers and Protein Domains, J. Phys. Chem. B, 2003, 107, 8730.
15. S. Keten, Z. Xu, B. Ihle and M. J. Buehler, Nanoconfinement controls stiffness, strength and mechanical toughness of b-sheet crystals in silk, Nat. Mater., 2010, 9, 359.
16. M. Solar and M. J. Buehler, Tensile deformation and failure of amyloid and amyloid-like protein fibrils, Nanotechnology, 2014, 25, 105703.
17. M. Solar and M. J. Buehler, Comparative analysis of nanomechanics of protein filaments under lateral loading, Nanoscale, 2012, 4, 1177.
18. G. Yoon, M. Lee, J. I. Kim, S. Na and K. Eom, Role of Sequence and Structural Polymorphism on the Mechanical Properties of Amyloid Fibrils, PLoS One, 2014, 9, e88502.
19. M. F. M. Engel, L. Khemtemourian, C. C. Kleijer, H. J. D. Meeldijk, J. Jacobs, A. J. Verkleij, B. de Kruijff, J. A. Killian and J. W. M. Hoppener, Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 6033.
20. A. W. P. Fitzpatrick, S. T. Park and A. H. Zewail, Exceptional rigidity and biomechanics of amyloid revealed by 4D electron microscopy, Proc. Natl. Acad. Sci. U. S. A., 2013, 110, 10976.
21. M. Tanaka, S. R. Collins, B. H. Toyama and J. S. Weissman, The physical basis of how prion conformations determine strain phenotypes, Nature, 2006, 442, 585.
22. J. R. Silveira, G. J. Raymond, A. G. Hughson, R. E. Race, V. L. Sim, S. F. Hayes and B. Caughey, The most infectious prion protein particles, Nature, 2005, 437, 257.
23. G. Yoon, Y. K. Kim, K. Eom and S. Na, Relationship between disease-specific structures of amyloid fibrils and their mechanical properties, Appl. Phys. Lett., 2013, 102, 011914.
24. M. I. Solar and M. J. Buehler, Composite materials: Taking a leaf from nature's book, Nat. Nanotechnol., 2012, 7, 417.
25. T. P. J. Knowles, T. W. Oppenheim, A. K. Buell, D. Y. Chirgadze and M. E. Welland, Nanostructured films from hierarchical self-assembly of amyloidogenic proteins, Nat. Nanotechnol., 2010, 5, 204.
26. C. Li, J. Adamcik and R. Mezzenga, Biodegradable nanocomposites of amyloid fibrils and graphene with shapememory and enzyme-sensing properties, Nat. Nanotechnol., 2012, 7, 421.
27. M. Carrion-Vazquez, A. F. Oberhauser, T. E. Fisher, P. E. Marszalek, H. Li and J. M. Fernandez, Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering, Prog. Biophys. Mol. Biol., 2000, 74, 63.
28. A. Engel and H. E. Gaub, Structure and Mechanics of Membrane Proteins, Annu. Rev. Biochem., 2008, 77, 127.
29. C. Bustamante, Z. Bryant and S. B. Smith, Ten years of tension: single-molecule DNA mechanics, Nature, 2003, 421, 423.
30. C. Joo, H. Balci, Y. Ishitsuka, C. Buranachai and T. Ha, Advances in Single-Molecule Fluorescence Methods for Molecular Biology, Annu. Rev. Biochem., 2008, 77, 51.
31. K. Eom, J. Yang, J. Park, G. Yoon, Y. Sohn, S. Park, D. Yoon, S. Na and T. Kwon, Experimental and Computational Characterization of Biological Liquid Crystals: A Review of Single-Molecule Bioassays, Int. J. Mol. Sci., 2009, 10, 4009.
32. K. C. Neuman, T. Lionnet and J. F. Allemand, Single-Molecule Micromanipulation Techniques, Annu. Rev. Mater. Res., 2007, 37, 33.
33. S. Kumar and M. S. Li, Biomolecules under mechanical force, Phys. Rep., 2010, 486, 1.
34. M. J. Buehler, S. Keten and T. Ackbarow, Theoretical and computational hierarchical nanomechanics of protein materials: Deformation and fracture, Prog. Mater. Sci., 2008, 53, 1101.
35. H. Lu, B. Isralewitz, A. Krammer, V. Vogel and K. Schulten, Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation, Biophys. J., 1998, 75, 662.
36. M. Gao, M. Wilmanns and K. Schulten, Steered molecular dynamics studies of titin I1 domain unfolding, Biophys. J., 2002, 83, 3435.
37. M. Gao, D. Craig, V. Vogel and K. Schulten, Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics, J. Mol. Biol., 2002, 323, 939.
38. T. Ackbarow, X. Chen, S. Keten and M. J. Buehler, Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of α-helical and b-sheet protein domains, Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 16410.
39. H. Ndlovu, A. E. Ashcroft, S. E. Radford and S. A. Harris, Effect of Sequence Variation on the Mechanical Response of Amyloid Fibrils Probed by Steered Molecular Dynamics Simulation, Biophys. J., 2012, 102, 587.
40. H. Ndlovu, A. E. Ashcroft, S. E. Radford and S. A. Harris, Molecular dynamics simulations of mechanical failure in polymorphic arrangements of amyloid fibrils containing structural defects, Beilstein J. Nanotechnol., 2013, 4, 429.
41. M. Lee, I. Baek, H. J. Jang, G. Yoon and S. Na, The bond survival time variation of polymorphic amyloid fibrils in the mechanical insight, Chem. Phys. Lett., 2014, 600, 68.
42. G. Yoon, J. Kwak, J. I. Kim, S. Na and K. Eom, Mechanical Characterization of Amyloid Fibrils Using Coarse-Grained Normal Mode Analysis, Adv. Funct. Mater., 2011, 21, 3454.
43. Z. P. Xu, R. Paparcone and M. J. Buehler, Alzheimer's Ab(1-40) Amyloid Fibrils Feature Size-Dependent Mechanical Properties, Biophys. J., 2010, 98, 2053.
44. E. Evans and K. Ritchie, Dynamic strength of molecular adhesion bonds, Biophys. J., 1997, 72, 1541.
45. K. Eom, D. E. Makarov and G. J. Rodin, Theoretical studies of the kinetics of mechanical unfolding of cross-linked polymer chains and their implications for single-molecule pulling experiments, Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys., 2005, 71, 021904.
46. K. Eom, G. Yoon, J.-I. Kim and S. Na, Coarse-Grained Elastic Models of Protein Structures for Understanding Their Mechanics and Dynamics, J. Comput. Theor. Nanosci., 2010, 7, 1210.
47. M. Zink and H. Grubmuller, Mechanical Properties of the Icosahedral Shell of Southern Bean Mosaic Virus: A Molecular Dynamics Study, Biophys. J., 2009, 96, 1350.
48. C. Kappel, N. Dölker, R. Kumar, M. Zink, U. Zachariae and H. Grubmüller, Universal Relaxation Governs the Nonequilibrium Elasticity of Biomolecules, Phys. Rev. Lett., 2012, 109, 118304.
49. D. Alsteens, C. B. Ramsook, P. N. Lipke and Y. F. Dufrêne, Unzipping a Functional Microbial Amyloid, ACS Nano, 2012, 6, 7703.
50. F. Pampaloni, G. Lattanzi, A. Jonas, T. Surrey, E. Frey and E.-L. Florin, Thermal fluctuations of grafted microtubules provide evidence of a length-dependent persistence length, Proc. Natl. Acad. Sci. U. S. A., 2006, 103, 10248.
51. J. F. Smith, T. P. Knowles, C. M. Dobson, C. E. MacPhee and M. E. Welland, Characterization of the nanoscale properties of individual amyloid fibrils, Proc. Natl. Acad. Sci. U. S. A., 2006, 103, 15806.
52. C. Sachse, N. Grigorieff and M. Fändrich, Nanoscale Flexibility Parameters of Alzheimer Amyloid Fibrils Determined by Electron Cryo-Microscopy, Angew. Chem., Int. Ed., 2010, 49, 1321.
53. G. I. Bell, Models for the specific adhesion of cells to cell, Science, 1978, 200, 618.
54. S. Keten and M. J. Buehler, Geometric Confinement Governs the Rupture Strength of H-bond Assemblies at a Critical Length Scale, Nano Lett., 2008, 8, 743.
55. J. M. Gere, Mechanics of Materials, Thomson Learning, 6th edn, 2003.
56. J. Gosline, P. Guerette, C. Ortlepp and K. Savage, The mechanical design of spider silks: from fibroin sequence to mechanical function, J. Exp. Biol., 1999, 202, 3295.
57. M. J. Buehler and T. Ackbarow, Fracture mechanics of protein materials, Mater. Today, 2007, 10, 46.
58. Z. Shao and F. Vollrath, Surprising strength of of silkworm silk, Nature, 2002, 418, 741.
59. R. Merkel, P. Nassoy, A. Leung, K. Ritchie and E. Evans, Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy, Nature, 1999, 397, 50.
60. G. Yoon, S. Na and K. Eom, Loading device effect on protein unfolding mechanics, J. Chem. Phys., 2012, 137, 025102.
61. O. K. Dudko, J. Mathe, A. Szabo, A. Meller and G. Hummer, Extracting Kinetics from Single-Molecule Force Spectroscopy: Nanopore Unzipping of DNA Hairpins, Biophys. J., 2007, 92, 4188.
62. J. C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kalé and K. Schulten, Scalable molecular dynamics with NAMD, J. Comput. Chem., 2005, 26, 1781.
63. A. D. MacKerell, D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher, B. Roux, M. Schlenkrich, J. C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiórkiewicz-Kuczera, D. Yin and M. Karplus, All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins, J. Phys. Chem. B, 1998, 102, 3586.