Atomic force microscopy under controlled conditions reveals structure of c-terminal region of α-synuclein in amyloid fibrils

ACS Nano

Volumn 6, Issue 7, 2012, Pages 5952-5960

  Sweers, Kim K M ^a   Van Der Werf, Kees O ^a   Bennink, Martin L ^a   Subramaniam, Vinod ^a,b  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

amyloid fibrils; atomic force microscopy; PeakForce QNM; peptide truncation; R synuclein

Indexed keywords

AFM; AMYLOID FIBRIL; C-TERMINAL REGIONS; C-TERMINAL TAIL; CHARGE SCREENING; COMPACT STRUCTURES; CONTROLLED CONDITIONS; ENVIRONMENTAL CONDITIONS; ION CONCENTRATIONS; MORPHOLOGICAL PARAMETERS; NANO SCALE; PEAKFORCE QNM; PROTEIN MONOMERS; R-SYNUCLEIN; SYNUCLEIN;

BIOLOGICAL MATERIALS; GLYCOPROTEINS; MECHANICAL PROPERTIES;

ATOMIC FORCE MICROSCOPY;

ALPHA SYNUCLEIN; AMYLOID; MUTANT PROTEIN; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; METHODOLOGY; NANOTECHNOLOGY; PARKINSON DISEASE; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE;

ALPHA-SYNUCLEIN; AMINO ACID SUBSTITUTION; AMYLOID; HUMANS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MUTANT PROTEINS; NANOTECHNOLOGY; PARKINSON DISEASE; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS;

EID: 84864198987     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn300863n     Document Type: Article

References (50)

1. Gosal, W. S.; Myers, S. L.; Radford, S. E.; Thomson, N. H. Amyloid under the Atomic Force Microscope Protein Pept. Lett. 2006, 13, 261-270
2. Knowles, T. P. J.; Buehler, M. J. Nanomechanics of Functional and Pathological Amyloid Materials Nat. Nanotechnol. 2011, 6, 469-479
3. Dobson, C. M. Protein Folding and Misfolding Nature 2003, 426, 884-890 (Pubitemid 38056880)
4. Shults, C. W. Lewy Bodies Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 1661-1668 (Pubitemid 43228751)
5. Segers-Nolten, I.; van der Werf, K.; van Raaij, M.; Subramaniam, V. Quantitative Characterization of Protein Nanostructures Using Atomic Force Microscopy Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 6609-6612
6. Khurana, R.; Ionescu-Zanetti, C.; Pope, M.; Li, J.; Nielson, L.; Ramirez-Alvarado, M.; Regan, L.; Fink, A. L.; Carter, S. A. A General Model for Amyloid Fibril Assembly Based on Morphological Studies Using Atomic Force Microscopy Biophys. J. 2003, 85, 1135-1144 (Pubitemid 36909675)
7. van Raaij, M. E.; Segers-Nolten, I. M. J.; Subramaniam, V. Quantitative Morphological Analysis Reveals Ultrastructural Diversity of Amyloid Fibrils from α-Synuclein Mutants Biophys. J. 2006, 91, L96-L98
8. Apetri, M. M.; Maiti, N. C.; Zagorski, M. G.; Carey, P. R.; Anderson, V. E. Secondary Structure of α-Synuclein Oligomers: Characterization by Raman and Atomic Force Microscopy J. Mol. Biol. 2006, 355, 63-71 (Pubitemid 41774139)
9. Barkhordarian, H.; Emadi, S.; Schulz, P.; Sierks, M. R. Isolating Recombinant Antibodies against Specific Protein Morphologies Using Atomic Force Microscopy and Phage Display Technologies Protein Eng. Des. Sel. 2006, 19, 497-502 (Pubitemid 44627322)
10. Bhak, G.; Lee, S.; Park, J. W.; Cho, S.; Paik, S. R. Amyloid Hydrogel Derived from Curly Protein Fibrils of α-Synuclein Biomaterials 2010, 31, 5986-5995
11. Conway, K. A.; Harper, J. D.; Lansbury, P. T., Jr. Fibrils Formed in Vitro from α-Synuclein and Two Mutant Forms Linked to Parkinson's Disease Are Typical Amyloid Biochemistry 2000, 39, 2552-2563 (Pubitemid 30148907)
12. Crowther, R. A.; Jakes, R.; Spillantini, M. G.; Goedert, M. Synthetic Filaments Assembled from C-Terminally Truncated α-Synuclein FEBS Lett. 1998, 436, 309-312 (Pubitemid 28482951)
13. De Franceschi, G.; Frare, E.; Pivato, M.; Relini, A.; Penco, A.; Greggio, E.; Bubacco, L.; Fontana, A.; De Laureto, P. P. Structural and Morphological Characterization of Aggregated Species of α-Synuclein Induced by Docosahexaenoic Acid J. Biol. Chem. 2011, 286, 22262-22274
14. Gai, W. P.; Pountney, D. L.; Power, J. H.; Li, Q. X.; Culvenor, J. G.; McLean, C. A.; Jensen, P. H.; Blumbergs, P. C. α-Synuclein Fibrils Constitute the Central Core of Oligodendroglial Inclusion Filaments in Multiple System Atrophy Exp. Neurol. 2003, 181, 68-78 (Pubitemid 36438677)
15. Kim, H. J.; Chatani, E.; Goto, Y.; Paik, S. R. Seed-Dependent Accelerated Fibrillation of α-Synuclein Induced by Periodic Ultrasonication Treatment J. Microbiol. Biotechnol. 2007, 17, 2027-2032
16. Murray, I. V. J.; Giasson, B. I.; Quinn, S. M.; Koppaka, V.; Axelsen, P. H.; Ischiropoulos, H.; Trojanowski, J. Q.; Lee, V. M.-Y. Role of α-Synuclein Carboxy-Terminus on Fibril Formation in Vitro Biochemistry 2003, 42, 8530-8540 (Pubitemid 36875420)
17. Qin, Z.; Hu, D.; Han, S.; Hong, D. P.; Fink, A. L. Role of Different Regions of α-Synuclein in the Assembly of Fibrils Biochemistry 2007, 46, 13322-13330 (Pubitemid 350136372)
18. Volkova, K. D.; Kovalska, V. B.; Yu Losytskyy, M. Y.; Veldhuis, G.; Segers-Nolten, G. M. J.; Tolmachev, O. I.; Subramaniam, V.; Yarmoluk, S. M. Studies of Interaction Between Cyanine Dye T-284 and Fibrillar Alpha-Synuclein J. Fluoresc. 2010, 20, 1267-1274
19. Zhang, F.; Lin, X.; Ji, L. N.; Du, H. N.; Tang, L.; He, J. H.; Hu, J.; Hu, H. Y. Assembly of α-Synuclein Fibrils in Nanoscale Studied by Peptide Truncation and AFM Biochem. Biophys. Res. Commun. 2008, 368, 388-394
20. 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
21. Sweers, K. K. M.; van der Werf, K. O.; Bennink, M. L.; Subramaniam, V. Nanomechanical Properties of α-Synuclein Amyloid Fibrils: A Comparative Study by Nanoindentation, Harmonic Force Microscopy, and PeakForce QNM Nanoscale Res. Lett. 2011, 6, 270
22. Keller, A.; Fritzsche, M.; Yu, Y. P.; Liu, Q.; Li, Y. H.; Dong, M.; Besenbacher, F. Influence of Hydrophobicity on the Surface-Catalyzed Assembly of the Islet Amyloid Polypeptide ACS Nano 2011, 5, 2770-2778
23. Moreno-Herrero, F.; Pérez, M.; Baró, A. M.; Avila, J. Characterization by Atomic Force Microscopy of Alzheimer Paired Helical Filaments under Physiological Conditions Biophys. J. 2004, 86, 517-525 (Pubitemid 38067481)
24. Chamberlain, A. K.; Macphee, C. E.; Zurdo, J.; Morozova-Roche, L. A.; Hill, H. A.; Dobson, C. M.; Davis, J. J. Ultrastructural Organization of Amyloid Fibrils by Atomic Force Microscopy Biophys. J. 2000, 79, 3282-3293
25. Nikiforov, M. P.; Thompson, G. L.; Reukov, V. V.; Jesse, S.; Guo, S.; Rodriguez, B. J.; Seal, K.; Vertegel, A. A.; Kalinin, S. V. Double-Layer Mediated Electromechnical Response of Amyloid Fibrils in Liquid Environment ACS Nano 2010, 4, 689-698
26. Song, Y.; Bhushan, B. Finite-Element Vibration Analysis of Tapping-Mode Atomic Force Microscopy in Liquid Ultramicroscopy 2007, 107, 1095-1104 (Pubitemid 47095121)
27. Goedert, M. Alpha-Synuclein and Neurodegenerative Diseases Nat. Rev. Neurosci. 2001, 2, 492-501 (Pubitemid 33676584)
28. Zarranz, J. J.; Alegre, J.; Gómez-Esteban, J. C.; Lezcano, E.; Ros, R.; Ampuero, I.; Vidal, L.; Hoenicka, J.; Rodriguez, O.; Atarés, B. et al. The New Mutation, E46K, of α-Synuclein Causes Parkinson and Lewy Body Dementia Ann. Neurol. 2004, 55, 164-173 (Pubitemid 38166992)
29. Pittenger, B.; Erina, N.; Su, C. Quantitative Mechanical Property Mapping at the Nanoscale with PeakForce QNM. Application Note, Veeco Instruments Inc., 2010
30. Derjaguin, B. V.; Muller, V. M.; Toporov, Yu. P. Effect of Contact Deformations on Adhesion of Particles J. Colloid Interface Sci. 1975, 53, 314-326
31. Young, T. J.; Monclus, M. A.; Burnett, T. L.; Broughton, W. R.; Ogin, S. L.; Smith, P. A. The Use of the PeakForce Quantitative Nanomechanical Mapping AFM-Based Method for High-Resolution Young's Modulus Measurement of Polymers Meas. Sci. Technol. 2011, 22, 125703
32. Tan, J. C.; Saines, P. J.; Bithell, E. G.; Cheetham, A. K. Hybrid Nanosheets of an Inorganic-Organic Framework Material: Facile Synthesis, Structure and Elastic Properties ACS Nano 2012, 6, 615-621
33. Adamcik, J.; Berquand, A.; Mezzenga, R. Single-Step Direct Measurement of Amyloid Fibrils Stiffness by Peak Force Quantitative Nanomechanical Atomic Force Microscopy Appl. Phys. Lett. 2011, 98, 193701
34. Ban, T.; Hamada, D.; Hasegawa, K.; Naiki, H.; Goto, Y. Direct Observation of Amyloid Fibril Growth Monitored by Thioflavin T Fluorescence J. Biol. Chem. 2003, 278, 16462-16465 (Pubitemid 36799502)
35. Hoyer, W.; Cherny, D.; Subramaniam, V.; Jovin, T. M. Impact of the Acidic C-Terminal Region Comprising Amino Acids 109-140 on α-Synuclein Aggregation in Vitro Biochemistry 2004, 43, 16233-16242 (Pubitemid 40041036)
36. Goldsbury, C.; Goldie, K.; Pellaud, J.; Seelig, J.; Frey, P.; Müller, S. A.; Kistler, J.; Cooper, G. J. S.; Aebi, U. Amyloid Fibril Formation from Full-Length and Fragments of Amylin J. Struct. Biol. 2000, 130, 352-362
37. van Noort, S. J. T.; van der Werf, K. O.; de Grooth, B. G.; van Hulst, N. F.; Greve, J. Height Anomalies in Tapping Mode Atomic Force Microscopy in Air Caused by Adhesion Ultramicroscopy 1997, 69, 117-127 (Pubitemid 27418144)
38. Santos, S.; Barcons, V.; Christenson, H. K.; Font, J.; Thomson, N. H. The Intrinsic Resolution Limit in the Atomic Force Microscope: Implications for Heights of Nano-Scale Features PloS One 2011, 6, e23821
39. Weisenhorn, A. L.; Hansma, P. K.; Albrecht, T. R.; Quate, C. F. Forces in Atomic Force Microscopy in Air and Water Appl. Phys. Lett. 1989, 54, 2651-2653
40. Farshchi-Tabrizi, M.; Kappl, M.; Butt, H. J. Influence of Humidity on Adhesion: An Atomic Force Microscopy Study J. Adhes. Sci. Technol. 2008, 22, 181-203 (Pubitemid 351535777)
41. Goodman, F. O.; Garcia, N. Roles of Attractive and Repulsive Forces in Atomic-Force Microscopy Phys. Rev. B 1991, 43, 4728-4731
42. Butt, H. J.; Capella, B.; Kappl, M. Force Measurements with the Atomic Force Microscope: Technique, Interpretation and Applications Surf. Sci. Rep. 2005, 59, 1-152 (Pubitemid 41594664)
43. Vilar, M.; Chou, H.; Lührs, T.; Maji, S. K.; Riek-Loher, D.; Verel, R.; Manning, G.; Stahlberg, H.; Riek, R. The Fold of α-Synuclein Fibrils Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 8637-8642
44. Sunde, M.; Serpell, L. C.; Bartlam, M.; Fraser, P. E.; Pepys, M. B.; Blake, C. C. F. Common Core Structure of Amyloid Fibrils by Synchrotron X-Ray Diffraction J. Mol. Biol. 1997, 273, 729-739 (Pubitemid 27488813)
45. Ghosh, K.; Dill, K. A. Computing Protein Stabilities from their Chain Lengths Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 10649-10654
46. Fitzkee, N. C.; Rose, G. D. Reassessing Random Coil Statistics in Unfolded Proteins Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 12497-12502 (Pubitemid 39122052)
47. Hoh, J. H.; Revel, J.; Hansma, P. K. Tip-Sample Interactions in Atomic Force Microscopy: I. Modulating Adhesion between Silicon Nitride and Glass Nanotechnology 1991, 2, 119-122
48. Senden, T. J.; Drummond, C. J. Surface Chemistry and Tip-Sample Interactions in Atomic Force Microscopy Colloid Surf. A 1995, 94, 29-51
49. Ebeling, D.; van den Ende, D.; Mugele, F. Electrostatic Interaction Forces in Aqueous Salt Solutions of Variable Concentration and Valency Nanotechnology 2011, 22, 305706
50. van der Werf, K. O.; Putman, C. A. J.; de Grooth, B. G.; Segerink, F. B.; Schipper, E. H.; van Hulst, N. F.; Greve, J. Compact Stand-Alone Atomic Force Microscope Rev. Sci. Instrum. 1993, 64, 2892-2897