Nanomechanics of functional and pathological amyloid materials

Nature Nanotechnology

Volumn 6, Issue 8, 2011, Pages 469-479

  Knowles, Tuomas P J ^a   Buehler, Markus J ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEINS; MAMMALS; NANOMECHANICS; NANOSTRUCTURED MATERIALS; NEURODEGENERATIVE DISEASES;

AMYLOID-LIKE FIBRIL; FUNCTIONAL PROTEINS; GENERAL CLASS; MATERIAL SELECTION; MULTISCALE MATERIAL DESIGNS; NANO SCALE; NEURODEGENERATIVE DISORDERS;

PROTEINS;

AMYLOID; NANOMATERIAL; PEPTIDE DERIVATIVE;

BACTERIUM; BIOMECHANICS; MAMMAL; MOLECULAR MECHANICS; NANOTECHNOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; REVIEW; SIMULATION;

EID: 79961211353     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2011.102     Document Type: Review

References (106)

1. Dobson, C. M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24, 329-32 (1999). (Pubitemid 29421804)
2. Jaroniec, C. P. et al. High-resolution molecular structure of a peptide in an amyloid fbril determined by magic angle spinning NMR spectroscopy. Proc. Natl Acad. Sci.USA 101, 711-716 (2004). (Pubitemid 38121022)
3. Luhrs, T. et al. 3D structure of Alzheimer's amyloid-beta(1-42) fbrils. Proc. Natl Acad. Sci.USA 102, 17342-17347 (2005).
4. Sawaya, M. R. et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447, 453-457 (2007). (Pubitemid 46816731)
5. Wasmer, C. et al. Amyloid fbrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319, 1523-1526 (2008). (Pubitemid 351398180)
6. Sipe, J. D. & Cohen, A. S. Review: History of the amyloid fbril. J. Struct. Biol. 130, 88-98 (2000).
7. Tan, S. Y. & Pepys, M. B. Amyloidosis. Histopathology 25, 403-414 (1994). (Pubitemid 24356782)
8. Selkoe, D. J. Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev. 81, 741-766 (2001). (Pubitemid 32267077)
9. Antzutkin, O. N. et al. Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of beta-sheets in Alzheimer's beta-amyloid fbrils. Proc. Natl Acad. Sci.USA 97, 13045-13050 (2000).
10. Bucciantini, M. et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511 (2002). (Pubitemid 34288846)
11. Tsai, H. H. et al. Energy landscape of amyloidogenic peptide oligomerization by parallel-tempering molecular dynamics simulation: signifcant role of Asn ladder. Proc. Natl Acad. Sci. USA 102, 8174-8179 (2005)
12. Pepys, M. B. Amyloidosis. Ann. Rev. Med. 57, 223-241 (2006). (Pubitemid 43261989)
13. Zanuy, D., Gunasekaran, K., Lesk, A. M. & Nussinov, R. Computational study of the fbril organization of polyglutamine repeats reveals a common motif identifed in beta-helices. J. Mol. Biol. 358, 330-45 (2006).
14. Paravastu, A. K., Leapman, R. D., Yau, W. M. & Tycko, R. Molecular structural basis for polymorphism in Alzheimer's beta-amyloid fbrils. Proc. Natl Acad. Sci.USA 105, 18349-18354 (2008).
15. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-66 (2006). (Pubitemid 44118036)
16. Fowler, D. M. et al. Functional amyloid formation within mammalian tissue. PLoS Biol. 4, e6 (2006).
17. Fowler, D. M., Koulov, A. V., Balch, W. E. & Kelly, J. W. Functional amyloid-from bacteria to humans. Trends Biochem. Sci. 32, 217-24 (2007).
18. Kelly, J. W. & Balch, W. E. Amyloid as a natural product. J. Cell Biol. 161, 461-462 (2003). (Pubitemid 36578568)
19. Mostaert, A. S., Higgins, M. J., Fukuma, T., Rindi, F. & Jarvis, S. P. Nanoscale mechanical characterisation of amyloid fbrils discovered in a natural adhesive. J. Biol. Phys. 32, 393-401 (2006). (Pubitemid 46175640)
20. Watt, B. et al. N-terminal domains elicit formation of functional Pmel17 amyloid fbrils. J. Biol. Chem. 284, 35543-35555 (2009).
21. Spillantini, M. G. et al. α-Synuclein in Lewy bodies. Nature 388, 839-840 (1997).
22. Fandrich, M., Fletcher, M. A. & Dobson, C. M. Amyloid fbrils from muscle myoglobin. Nature 410, 165-166 (2001).
23. Dobson, C. M. Protein folding and misfolding. Nature 426, 884-90 (2003). (Pubitemid 38056880)
24. Keten, S., Xu, Z., Ihle, B. & Buehler, M. J. Nanoconfnement controls stifness, strength and mechanical toughness of beta-sheet crystals in silk. Nature Mater. 9, 359-367 (2010).
25. Kol, N. et al. Self-assembled peptide nanotubes are uniquely rigid bioinspired supramolecular structures. Nano Lett. 5, 1343-1346 (2005).
26. Salvetat, J. P. et al. Elastic and shear moduli of single-walled carbon nanotube ropes. Phys. Rev. Lett. 82, 944-947 (1999).
27. Kis, A. et al. Nanomechanics of microtubules. Phys. Rev. Lett. 89, 248101 (2002).
28. Smith, J. F., Knowles, T. P. J., Dobson, C. M., MacPhee, C. E. & Welland, M. E. Characterization of the nanoscale properties of individual amyloid fbrils. Proc. Natl Acad. Sci.USA 103, 15806-15811 (2006). (Pubitemid 44657548)
29. Gittes, F., Mickey, B., Nettleton, J. & Howard, J. Flexural rigidity of microtubules and actin-flaments measured from thermal fuctuations in shape. J. Cell Biol. 120, 923-934 (1993). (Pubitemid 23056298)
30. Wang, J. C. et al. Micromechanics of isolated sickle cell hemoglobin fbers: Bending moduli and persistence lengths. J. Mol. Biol. 315, 601-612 (2002). (Pubitemid 34729312)
31. Adamcik, J. et al. Understanding amyloid aggregation by statistical analysis of atomic force microscopy images. Nature Nanotech. 5, 423-428 (2010).
32. Knowles, T. P. et al. An analytical solution to the kinetics of breakable flament assembly. Science 326, 1533-1537 (2009).
33. Meersman, F., Cabrera, R. Q., McMillan, P. F. & Dmitriev, V. Compressibility of insulin amyloid fbrils determined by X-ray difraction in a diamond anvil cell. High Pressure Res. 29, 665-670 (2009).
34. Sachse, C., Grigorief, N. & Fandrich, M. Nanoscale fexibility parameters of Alzheimer amyloid fbrils determined by electron cryo-microscopy. Angew. Chem. Int. Ed. 49, 1321-1323 (2010).
35. Knowles, T. P. et al. Role of intermolecular forces in defning material properties of protein nanofbrils. Science 318, 1900-1903 (2007).
36. Park, J., Kahng, B., Kamm, R. D. & Hwang, W. Atomistic simulation approach to a continuum description of self-assembled beta-sheet flaments. Biophys. J. 90, 2510-2524 (2006).
37. Paparcone, R., Keten, S. & Buehler, M. J. Atomistic simulation of nanomechanical properties of Alzheimer's A beta(1-40) amyloid fbrils under compressive and tensile loading. J. Biomechanics 43, 1196-1201 (2010).
38. Relini, A. et al. Detection of populations of amyloid-like protofbrils with diferent physical properties. Biophys. J. 98, 1277-1284 (2010).
39. Guo, S. & Akhremitchev, B. B. Packing density and structural heterogeneity of insulin amyloid fbrils measured by AFM nanoindentation. Biomacromolecules 7, 1630-1636 (2006). (Pubitemid 43811222)
40. Petkova, A. T. et al. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fbrils. Science 307, 262-265 (2005). (Pubitemid 40116242)
41. Tanaka, M., Collins, S. R., Toyama, B. H. & Weissman, J. S. Te physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589 (2006). (Pubitemid 44167919)
42. Dzwolak, W., Smirnovas, V., Jansen, R. & Winter, R. Insulin forms amyloid in a strain-dependent manner: An FT-IR spectroscopic study. Protein Sci. 13, 1927-1932 (2004). (Pubitemid 38822132)
43. Sigurdson, C. J. et al. Prion strain discrimination using luminescent conjugated polymers. Nature Meth. 4, 1023-1030 (2007). (Pubitemid 350201774)
44. Paparcone, R., Cranford, S. W. & Buehler, M. J. Self-folding and aggregation of amyloid fbrils Nanoscale 3, 1748-1755 (2011).
45. Huang, Y. Y., Knowles, T. P. J. & Terentjev, E. M. Strength of nanotubes, flaments, and nanowires from sonication-induced scission. Adv. Mater. 21, 3945-3948 (2009).
46. Streltsov, V. X-ray absorption and difraction studies of the metal binding sites in amyloid beta-peptide. Eur. Biophys. J. 37, 257-263 (2008).
47. Ackbarow, T., Chen, X., Keten, S. & Buehler, M. J. Hierarchies, multiple energy barriers and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proc. Natl Acad. Sci. USA 104, 16410-16415 (2007). (Pubitemid 350211030)
48. Ma, B. & Nussinov, R. Stabilities and conformations of Alzheimer's beta-amyloid peptide oligomers (Abeta 16-22, Abeta 16-35, and Abeta 10-35): Sequence efects. Proc. Natl Acad. Sci. USA 99, 14126-14131 (2002). (Pubitemid 35257636)
49. Periole, X., Rampioni, A., Vendruscolo, M. & Mark, A. E. Factors that afect the degree of twist in beta-sheet structures: a molecular dynamics simulation study of a cross-beta flament of the GNNQQNY peptide. J. Phys. Chem. B 113, 1728-1737 (2009).
50. Lee, C. F., Loken, J., Jean, L. & Vaux, D. J. Elongation dynamics of amyloid fbrils: A rugged energy landscape picture. Phys. Rev. E 80, 041906 (2009).
51. Wei, G. H., Mousseau, N. & Derreumaux, P. Computational simulations of the early steps of protein aggregation. Prion 1, 3-8 (2007).
52. Xu, Z., Paparcone, R. & Buehler, M. J. Alzheimer's abeta(1-40) amyloid fbrils feature size-dependent mechanical properties. Biophys. J. 98, 2053-2062 (2010).
53. Auer, S. et al. Importance of metastable states in the free energy landscapes of polypeptide chains. Phys. Rev. Lett. 99, 178104 (2007).
54. Xu, Z. & Buehler, M. J. Mechanical energy transfer and dissipation in fbrous beta-sheet-rich proteins. Phys. Rev. E 81, 061910 (2010).
55. Fratzl, P. & Weinkamer, R. Nature's hierarchical materials. Prog. Mater. Sci. 52, 1263-1334 (2007). (Pubitemid 47374755)
56. Ashby, M. F., Gibson, L. J., Wegst, U. & Olive, R. Te mechanical properties of natural materials. I. Material property charts. Proc. R. Soc. Lond. A 450, 123-140 (1995).
57. Wegst, U. G. K. & Ashby, M. F. Te mechanical efciency of natural materials. Phil. Mag. 84, 2167-2181 (2004).
58. Kreplak, L., Bar, H., Leterrier, J. F., Herrmann, H. & Aebi, U. Exploring the mechanical behavior of single intermediate flaments. J. Mol. Biol. 354, 569-577 (2005). (Pubitemid 41628276)
59. Yang, L. et al. Micromechanical bending of single collagen fbrils using atomic force microscopy. J. Biomed. Mater. Res. A 82, 160-168 (2007). (Pubitemid 46906502)
60. Shen, Z. L., Dodge, M. R., Kahn, H., Ballarini, R. & Eppell, S. J. Stress-strain experiments on individual collagen fbrils. Biophys. J. 95, 3956-3963 (2008).
61. Slotta, U. et al. Spider silk and amyloid fbrils: A structural comparison. Macromol. Biosci. 7, 183-188 (2007). (Pubitemid 47264213)
62. Vollrath, F. & Knight, D. P. Liquid crystalline spinning of spider silk. Nature 410, 541-548 (2001). (Pubitemid 32267190)
63. Collins, S. R., Douglass, A., Vale, R. D. & Weissman, J. S. Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2, e321 (2004).
64. Shorter, J. & Lindquist, S. Destruction or potentiation of diferent prions catalyzed by similar Hsp104 remodeling activities. Mol. Cell 23, 425-438 (2006). (Pubitemid 44128844)
65. Paparcone, R. & Buehler, M. J. Failure of A-beta-(1-40) amyloid fbrils under tensile loading. Biomaterials 32, 3367-3374 (2011).
66. Aguzzi, A. Cell biology: Beyond the prion principle. Nature 459, 924-925 (2009).
67. Prusiner, S. B. Molecular biology of prion diseases. Science 252, 1515-1522 (1991). (Pubitemid 21917065)
68. Riek, R. Cell biology: infectious Alzheimer's disease? Nature 444, 429-431 (2006). (Pubitemid 44809046)
69. Eisele, Y. S. et al. Peripherally applied A beta-containing inoculates induce cerebral beta-amyloidosis. Science 330, 980-982 (2010).
70. Aguzzi, A. & Rajendran, L. Te transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64, 783-790 (2009).
71. Kofe, R. M. et al. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl Acad. Sci. USA 106, 4012-4017 (2009).
72. Haass, C. & Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nature Rev. Mol. Cell Biol. 8, 101-112 (2007). (Pubitemid 46432529)
73. Gebbink, M. F. B. G., Claessen, D., Bouma, B., Dijkhuizen, L. & Wosten, H. A. B. Amyloids-A functional coat for microorganisms. Nature Rev. Microbiol. 3, 333-341 (2005).
74. Maji, S. K. et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325, 328-332 (2009).
75. Chapman, M. R. et al. Role of Escherichia coli curli operons in directing amyloid fber formation. Science 295, 851-855 (2002). (Pubitemid 34118365)
76. Shorter, J. & Lindquist, S. Prions as adaptive conduits of memory and inheritance. Nature Rev. Genet. 6, 435-450 (2005). (Pubitemid 40733889)
77. Meyer-Luehmann, M. et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451, 720-724 (2008). (Pubitemid 351220570)
78. Barnhart, M. M. & Chapman, M. R. Curli biogenesis and function. Annu. Rev. Microbiol. 60, 131-147 (2006). (Pubitemid 44627943)
79. Hammer, N. D., Schmidt, J. C. & Chapman, M. R. Te curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc. Natl Acad. Sci. USA 104, 12494-12499 (2007). (Pubitemid 47206166)
80. Zhang, S. G., Holmes, T., Lockshin, C. & Rich, A. Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc. Natl Acad. Sci. USA 90, 3334-3338 (1993). (Pubitemid 23111360)
81. Zhang, S. G. Fabrication of novel biomaterials through molecular self-assembly. Nature Biotechnol. 21, 1171-1178 (2003).
82. Lovett, M. et al. Silk fbroin microtubes for blood vessel engineering. Biomaterials 28, 5271-5279 (2007). (Pubitemid 47542340)
83. Keten, S. & Buehler, M. J. Geometric confnement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Lett. 8, 743-748 (2008).
84. MacPhee, C. E. & Dobson, C. M. Formation of mixed fbrils demonstrates the generic nature and potential utility of amyloid nanostructures. J. Am. Chem. Soc. 122, 12707-12713 (2000). (Pubitemid 32052199)
85. Reches, M. & Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625-627 (2003). (Pubitemid 36520583)
86. Carny, O., Shalev, D. E. & Gazit, E. Fabrication of coaxial metal nanocables using a self-assembled peptide nanotube scafold. Nano Lett. 6, 1594-1597 (2006).
87. Lu, W. & Lieber, C. M. Nanoelectronics from the bottom up. Nature Mater. 6, 841-850 (2007). (Pubitemid 350050579)
88. Scheibel, T. et al. Conducting nanowires built by controlled self-assembly of amyloid fbers and selective metal deposition. Proc. Natl Acad. Sci. USA 100, 4527-4532 (2003). (Pubitemid 36457764)
89. Niu, L. J., Chen, X. Y., Allen, S. & Tendler, S. J. B. Using the bending beam model to estimate the elasticity of diphenylalanine nanotubes. Langmuir 23, 7443-7446 (2007). (Pubitemid 47116397)
90. Reches, M. & Gazit, E. Controlled patterning of aligned self-assembled peptide nanotubes. Nature Nanotech. 1, 195-200 (2006).
91. Adler-Abramovich, L. et al. Self-assembled arrays of peptide nanotubes by vapour deposition. Nature Nanotech. 4, 849-854 (2009).
92. Hamley, I. W. et al. Alignment of a model amyloid peptide fragment in bulk and at a solid surface. J. Phys. Chem. B 114, 8244-8254 (2010).
93. Knowles, T. P. J., Oppenheim, T., Buell, A. K., Chirgadze, D. Y. & Welland, M. E. Nanostructured bioflms from hierarchical self-assembly of amyloidogenic proteins. Nature Nanotech. 5, 204-207 (2010).
94. Barrau, S. et al. Integration of amyloid nanowires in organic solar cells. Appl. Phys. Lett. 93, 023307 (2008).
95. Channon, K. J., Devlin, G. L. & MacPhee, C. E. Efcient energy transfer within self-assembling peptide fbers: A route to light-harvesting nanomaterials. J. Am. Chem. Soc. 131, 12520-12521 (2009).
96. Liang, Y. et al. Light harvesting antenna on an amyloid scafold. Chem. Commun. 6522-6524 (2008).
97. Maji, S. K. et al. Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol. 6, e17 (2008).
98. Holmes, T. C. et al. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scafolds. Proc. Natl Acad. Sci. USA 97, 6728-6733 (2000). (Pubitemid 30412782)
99. Ellis-Behnke, R. G. et al. Nano neuro knitting: Peptide nanofber scafold for brain repair and axon regeneration with functional return of vision. Proc. Natl Acad. Sci. USA 103, 5054-5059 (2006).
100. Gras, S. L. et al. Functionalised amyloid fbrils for roles in cell adhesion. Biomaterials 29, 1553-1562 (2008).
101. Gimona, M. Protein linguistics-a grammar for modular protein assembly? Nature Rev. Mol. Cell Biol. 7, 68-73 (2006). (Pubitemid 43361574)
102. Diaz-Avalos, R. et al. Cross-beta order and diversity in nanocrystals of an amyloid-forming peptide. J. Mol. Biol. 330, 1165-1175 (2003) (Pubitemid 36818911)
103. Hemingway, E. Te Old Man and the Sea (Vintage Books, 2007).
104. Nelson, R. et al. Structure of the cross-β spine of amyloid-like fbrils. Nature 435, 773-778 (2005). (Pubitemid 40839722)
105. Galkin, V. E., Orlova, A., Cherepanova, O., Lebart, M-C. & Ebelman, E. H. High-resolution cryo-EM structure of the F-actin-fmbrin/plastin ABD2 complex. Proc. Natl Acad. Sci. USA 105, 1494-1498 (2008). (Pubitemid 351346542)
106. Li, H., DeRosier, D. J., Nicholson, W. V., Nogales, E. & Downing, K. H. Microtubule structure at 8 A resolution. Structure 10, 1317-1328 (2002).