Structural model for α-synuclein fibrils derived from high resolution imaging and nanomechanical studies using atomic force microscopy

Soft Matter

Volumn 8, Issue 27, 2012, Pages 7215-7222

  Sweers, Kim K M ^a   Segers Nolten, Ine M J ^a   Bennink, Martin L ^a   Subramaniam, Vinod ^a,b  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AFM IMAGE; AMYLOID FIBRIL; BENDING RIGIDITY; HIGH RESOLUTION; HIGH-RESOLUTION IMAGING; MEASURED DATA; MECHANICAL CHARACTERISTICS; MORPHOLOGICAL FEATURES; NANOMECHANICAL STUDIES; PACKING CONFIGURATION; PARKINSON'S DISEASE; PROTEIN AGGREGATES; SELF-ASSEMBLE; STRUCTURAL MODELS; SYNUCLEIN; SYNUCLEIN PROTEINS;

ATOMIC FORCE MICROSCOPY; MODEL STRUCTURES;

PROTEINS;

EID: 84869595605     PISSN: 1744683X     EISSN: 17446848     Source Type: Journal    
DOI: 10.1039/c2sm25426c     Document Type: Article

References (57)

1. C. M. Dobson Protein folding and misfolding Nature 2003 426 884 890 (Pubitemid 38056880)
2. J. D. Sipe A. S. Cohen History of the amyloid fibril J. Struct. Biol. 2000 130 88 98
3. F. Chiti C. M. Dobson Protein misfolding, functional amyloid and human disease Annu. Rev. Biochem. 2006 75 333 366 (Pubitemid 44118036)
4. C. W. Shults Lewy bodies Proc. Natl. Acad. Sci. U. S. A. 2006 103 1661 1668 (Pubitemid 43228751)
5. M. Goedert Alpha-synuclein and neurodegenerative diseases Nat. Rev. Neurosci. 2001 2 492 501 (Pubitemid 33676584)
6. V. N. Uversky and A. L. Fink, Folding and Misfolding of α-Synuclein, in Molecular Mechanisms in Parkinson's Disease, ed., P. Kahle, and, C. Haass, Landes Bioscience, Austin, 2007 82 98
7. L. C. Serpell J. Berriman R. Jakes M. Goedert R. A. Crowther Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation Proc. Natl. Acad. Sci. U. S. A. 2000 97 4897 4902 (Pubitemid 30238654)
8. M. Vilar H. T. Chou T. Luhrs S. K. Maji D. Riek-Loher R. Verel G. Manning H. Stahlberg R. Riek The fold of α-synuclein fibrils Proc. Natl. Acad. Sci. U. S. A. 2008 105 8637 8642
9. L. P. Li T. A. Darden L. Bartolotti D. Kominos L. G. Pedersen An atomic model for the pleated β-sheet structure of Aβ amyloid protofilaments Biophys. J. 1999 76 2871 2878 (Pubitemid 29269437)
10. O. S. Makin L. C. Serpell Structures for amyloid fibrils FEBS J. 2005 272 5950 5961 (Pubitemid 41713687)
11. M. Fändrich J. Meinhardt N. Grigorieff Structural polymorphism of Alzheimer Aβ and other amyloid fibrils Prion 2009 3 89 93
12. R. Kodali R. Wetzel Polymorphism in the intermediates and products of amyloid assembly Curr. Opin. Struct. Biol. 2007 17 48 57 (Pubitemid 46242190)
13. S. Kumar J. B. Udgaonkar Mechanisms of amyloid fibril formation by proteins Curr. Sci. 2010 98 639 656
14. J. Adamcik J. Jung J. M. Flakowski P. De Los Rios G. Dietler R. Mezzenga Understanding amyloid aggregation by statistical analysis of atomic force microscopy images Nat. Nanotech. 2010 5 423 428
15. R. Jansen W. Dzwolak R. Winter Amyloidenic self-assembly of insulin aggregates probed by high resolution atomic force microscopy Biophys. J. 2005 88 1344 1353 (Pubitemid 40975961)
16. K. L. de Jong B. Incledon C. M. Yip M. R. DeFelippis Amyloid fibrils of glucagon characterized by high-resolution atomic force microscopy Biophys. J. 2006 91 1905 1914 (Pubitemid 44352452)
17. M. Dong M. B. Hovgaard S. L. Xu D. E. Otzen F. Besenbacher AFM study of glucagon fibrillation via oligomeric structures resulting in interwoven fibrils Nanotechnology 2006 17 4003 4009 (Pubitemid 44424339)
18. N. M. Kad S. L. Myers D. P. Smith D. A. M. Smith S. E. Radford N. H. Thomson Hierarchical assembly of β2-microglobulin amyloid in vitro revealed by atomic force microscopy J. Mol. Biol. 2003 88 785 797
19. M. Anderson O. V. Bocharova N. Makarava L. Breydo V. V. Salnikov I. V. Baskakov Polymorphism and ultrastructural organization of prion protein amyloid fibrils: an insight from high resolution atomic force microscopy J. Mol. Biol. 2006 358 580 596
20. R. Khurana C. Ionescu-Zanetti M. Pope J. Li L. Nielson M. Ramirez-Alvarado L. Regan A. L. Fink S. A. Carter A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy Biophys. J. 2003 85 1135 1144 (Pubitemid 36909675)
21. M. E. Raaij van I. M. J. Segers-Nolten V. Subramaniam Quantitative morphological analysis reveals ultrastructural diversity of amyloid fibrils from α-synuclein mutants Biophys. J. 2006 L96 L98
22. I. M. J. Segers-Nolten, K. van der Werf M. van Raaij, and V. Subramaniam, Quantitative characterization of protein nanostructures using atomic force microscopy, Proc. Annu. Int. Conf. IEEE Eng. Med. Biol. Sci, 2007, pp. 6608-6611
23. W. Hoyer T. Antony D. Cherny G. Heim T. M. Jovin V. Subramaniam Dependence of α-synuclein aggregate morphology on solutions conditions J. Mol. Biol. 2002 322 383 393
24. H. Heise W. Hoyer S. Becker O. C. Andronesi D. Riedel M. Baldus Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR Proc. Natl. Acad. Sci. U. S. A. 2005 102 15871 15876 (Pubitemid 41552835)
25. G. Comellas J. J. Lopez A. J. Nieuwkoop L. R. Lemkau C. M. Rienstra Straightforward, effective calibration of SPINAL-64 decoupling results in the enhancement of sensitivity and resolution of biomolecular solid-state NMR J. Magn. Reson. 2011 209 131 135
26. G. Comellas L. R. Lemkau A. J. Nieuwkoop K. D. Kloepper D. T. Ladror R. Ebisu W. S. Woods A. S. Lipton J. M. George C. M. Rienstra Structured regions of α-synuclein fibrils include the early-onset Parkinson's disease mutation sites J. Mol. Biol. 2011 411 881 895
27. L. R. Lemkau G. Comellas K. D. Kloepper W. S. Woods J. M. George C. M. Rienstra Mutant A30P α-synuclein adopts wild-type fibril structure, despite slower fibrillation kinetics J. Biol. Chem. 2012 287 11526 22532
28. L. Yang K. O. van der Werf B. F. J. M. Koopman V. Subramaniam M. L. Bennink P. J. Dijkstra J. Feijen Micromechanical bending of single collagen fibrils using atomic force microscopy J. Biomed. Mater. Res. 2007 82 160 168 (Pubitemid 46906502)
29. J. Kjelstrup-Hansen O. Hansen H. G. Rubahn O. Boggild Mechanical properties of organic nanofibers Small 2006 5 660 666
30. Y. Isono, T. Namazu and T. Taneka, AFM Bending AFM bending testing of nanometric single crystal silicon wire at intermediate temperatures for MEMS, Proc. 14th IEEE Int. Conf. MEMS, 2001, 135 138 (Pubitemid 32470771)
31. T. P. J. Knowles A. W. Fitzpatrick S. Meehan H. R. Mott M. Vendruscolo C. M. Dobson M. E. Welland Role of intermolecular forces defining material properties of protein nanofibrils Science 2007 318 1900 1903
32. N. Mücke L. Kreplak R. Kirmse T. Wedig H. Herrmann U. Aebi J. Langowski Assessing the flexibility of intermediate filaments by atomic force microscopy J. Mol. Biol. 2004 335 1241 1250 (Pubitemid 38077243)
33. B. Mickey J. Howard Rigidity of microtubules is increased by stabilizing agents J. Cell Biol. 1995 130 909 917
34. J. C. Wang M. S. Turner G. Agarwal S. Kwong R. Josephs F. A. Ferrone R. W. Briehl Micromechanics of isolated sickle cell hemoglobin fibers: bending moduli and persistence lengths J. Mol. Biol. 2002 315 601 612 (Pubitemid 34729312)
35. T. P. J. Knowles J. F. Smith A. Craig C. M. Dobson M. E. Welland Spatial persistence of angular correlations in amyloid fibrils Phys. Rev. Lett. 2006 96 238301
36. J. F. Smith T. P. J. Knowles C. M. Dobson C. M. MacPhee M. E. Welland Characterization of the nanoscale properties of individual amyloid fibrils Proc. Natl. Acad. Sci. U. S. A. 2006 103 15806 15811 (Pubitemid 44657548)
37. C. Rivetti M. Guthold C. Bustamante Scanning force microscopy of DNA deposited onto mica: equilibration versus kinetic trapping studied by statistical polymer chain analysis J. Mol. Biol. 1996 264 919 932 (Pubitemid 27019483)
38. V. VanBuren L. Cassimeris D. J. Odde Mechanochemical model of microtubule structure and self-assembly kinetics Biophys. J. 2005 89 2911 2926 (Pubitemid 41636049)
39. F. Moreno-Herrero M. Perez A. M. Baro J. Avila Characterization by atomic force microscopy of Alzheimer paired helical filaments under physiological conditions Biophys. J. 2004 86 517 525 (Pubitemid 38067481)
40. Z. G. Liu Z. Li H. L. Zhou G. Wei Y. H. Song L. Wang Imaging DNA molecules on mica surface by atomic force microscopy in air and in liquid Microsc. Res. Tech. 2005 66 179 185 (Pubitemid 40840394)
41. J. Adamcik R. Mezzenga Adjustable twisting periodic pitch of amyloid fibrils Soft Matter 2011 7 5437 5443
42. J. M. Gosline P. A. Guerette C. S. Ortlepp K. N. Savage The mechanical design of spider silks: from fibroin sequence to mechanical function J. Exp. Biol. 1999 202 3295 3303 (Pubitemid 30018435)
43. F. Vollrath D. P. Knight Liquid crystalline spinning of spider silk Nature 2001 410 541 548 (Pubitemid 32267190)
44. J. M. Gere and S. P. Timoshenko, in Mechanics of Materials, Stanley Thornes (Publishers) Ltd, Cheltenham, 4th SI edn, 1999
45. R. Nelson M. R. Sawaya M. Balbirnie A. O. Madsen C. Riekel R. Grothe D. Eisenberg Structure of the cross-beta spine of amyloid-like fibrils Nature 2005 435 773 778 (Pubitemid 40839722)
46. D. Eisenberg R. Nelson M. R. Sawaya M. Balbirnie M. R. Sambashivan M. I. Ivanova A. O. Madsen C. Riekel The structural biology of protein aggregation diseases: fundamental questions and some answers Accounts Chem. Res. 2006 39 568 575
47. F. Meersman R. Q. Cabrera P. F. McMillian V. Dmitriev Structural and mechanical properties of TTR105-115 amyloid fibrils from compression experiments Biophys. J. 2011 100 193 197
48. I. Karyagina S. Becker K. Giller D. Riedel T. M. Jovin C. Griesinger M. Bennati Electron paramagnetic resonance spectroscopy measures the distance between the external β-strands of folded α-synuclein in amyloid fibrils Biophys. J. 2011 101 L1 L3
49. M. Chen M. Margittai J. Chen R. Langen Investigation of alpha-synuclein fibril structure by site-directed spin labeling J. Biol. Chem. 2007 282 24970 24979 (Pubitemid 47347515)
50. M. H. Shabestari I. M. J. Segers-Nolten M. M. A. E. Claessens B. D. van Rooijen V. Subramaniam M. Huber Elucidating the α-synuclein fibril fold by pulsed EPR Biophys. J. 2012 102 454a
51. A. Esposito C. P. Dohm P. Kermer M. Bahr F. S. Wouters α-synuclein and its disease-related mutants interact differentially with the microtubule protein tau and associate with the actin cytoskeleton Neurobiol. Dis. 2007 26 521 531 (Pubitemid 46756322)
52. M. A. Alim Q. L. Ma K. Takeda T. Aizawa M. Matsubara M. Nakamura A. Asada T. Saito H. Kaji M. Yoshii S. Hisanaga K. Ueda Demonstration of a role for α-synuclein as a functional microtubule-associated protein J. Alzheimers Dis. 2004 6 435 442 (Pubitemid 39287257)
53. C. Wersinger A. Sidhu Disruption of the interaction of α-synuclein with the microtubules enhances cell surface recruitment of the dopamine transporter Biochemistry 2007 44 13612 13624
54. H. Kojima A. Ishijima T. Yanagida Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation Proc. Natl. Acad. Sci. U. S. A. 1994 91 12962 12966
55. M. M. A. E. Claessens M. Bathe E. Frey A. R. Bausch Actin-binding proteins sensitively mediate F-actin bundle stiffness Nat. Mater. 2006 5 748 753 (Pubitemid 44320328)
56. I. A. T. Schaap C. Carrasco P. J. de Pablo F. C. MacKintosh C. F. Schmidt Elastic response, buckling, and instability of microtubules under radial indentation Biophys. J. 2006 91 1521 1531 (Pubitemid 44174269)
57. D. S. Fudge K. H. Gardner V. T. Forsyth C. Riekel J. M. Gosline The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads Biophys. J. 2003 85 2015 2027 (Pubitemid 37052281)