Solution conditions determine the relative importance of nucleation and growth processes in α-synuclein aggregation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 21, 2014, Pages 7671-7676

  Buell, Alexander K ^a   Galvagnion, Céline ^a   Gaspar, Ricardo ^b   Sparr, Emma ^b   Vendruscolo, Michele ^a   Knowles, Tuomas P J ^a   Linse, Sara ^b   Dobson, Christopher M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Electrostatic interactions; Kinetic analysis; Neurodegenerative disease; Prion like behavior; Seeding

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID;

ACIDITY; ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CRYSTALLIZATION; ENDOSOME; HYDROPHOBICITY; IN VITRO STUDY; LIPID BILAYER; LYSOSOME; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY;

ELECTROSTATIC INTERACTIONS; KINETIC ANALYSIS; NEURODEGENERATIVE DISEASE; PRION-LIKE BEHAVIOR; SEEDING;

ALPHA-SYNUCLEIN; AMYLOID; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MICROSCOPY, ATOMIC FORCE; PARKINSON DISEASE; STATIC ELECTRICITY;

EID: 84901660540     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315346111     Document Type: Article

References (44)

1. Otzen DE, ed (2013) Amyloid Fibrils and Prefibrillar Aggregates: Molecular and Biological Properties (Wiley-VCH, Weinheim, Germany).
2. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366. (Pubitemid 44118036)
3. Cohen SIA, Vendruscolo M, Dobson CM, Knowles TPJ (2012) From macroscopic measurements to microscopic mechanisms of protein aggregation. J Mol Biol421(2-3):160-171.
4. Cohen SIA, et al. (2013) Proliferation of amyloid-ß42 aggregates occurs through a secondary nucleation mechanism. Proc Natl Acad Sci USA 110(24):9758-9763.
5. Ferrone FA, Hofrichter J, Eaton WA (1985) Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism. J Mol Biol 183(4):611-631. (Pubitemid 15036851)
6. Ruschak AM, Miranker AD (2007) Fiber-dependent amyloid formation as catalysis of an existing reaction pathway. Proc Natl Acad Sci USA 104(30):12341-12346. (Pubitemid 47206139)
7. Knowles TPJ, et al. (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326(5959):1533-1537.
8. Cohen SIA, et al. (2011) Nucleated polymerization with secondary pathways. I. Time evolution of the principal moments. J Chem Phys 135(6):065105.
9. Conway KA, Harper JD, Lansbury PT (1998) Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat Med 4(11):1318-1320. (Pubitemid 28512115)
10. Fink A (2007) Factors affecting the fibrillation of a-synuclein, a natively unfolded protein. Misbehaving Proteins: Protein (Mis)folding, Aggregation, and Stability, eds Murphy R, Tsai A (Springer, Berlin), pp 265-285.
11. Giehm L, Otzen DE (2010) Strategies to increase the reproducibility of protein fi-brillization in plate reader assays. Anal Biochem 400(2):270-281.
12. Grey M, Linse S, Nilsson H, Brundin P, Sparr E (2011) Membrane interaction of a-synuclein in different aggregation states. J Parkinsons Dis 1(4):359-371.
13. Jarrett JT, Lansbury PT, Jr. (1993) Seeding "one-dimensional crystallization" of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73(6):1055-1058. (Pubitemid 23180480)
14. Cohen SIA, Vendruscolo M, Dobson CM, Knowles TPJ (2011) Nucleated polymerisation in the presence of pre-formed seed filaments. Int J Mol Sci 12(9):5844-5852.
15. Ostwald W (1897) Studien über die Bildung und Umwandlung fester Körper. 1. Übersättigung und Überkaltung. Z Phys Chem 22:290-330.
16. Lomakin A, Chung DS, Benedek GB, Kirschner DA, Teplow DB (1996) On the nucleation and growth of amyloid beta-protein fibrils: Detection of nuclei and quantitation of rate constants. Proc Natl Acad Sci USA 93(3):1125-1129. (Pubitemid 26054370)
17. Kashchiev D, Auer S (2010) Nucleation of amyloid fibrils. J Chem Phys 132(21):215101.
18. Huang YY, Knowles TPJ, Terentjev EM (2009) Strength of nanotubes, filaments, and nanowires from sonication-induced scission. Adv Mater 21(38-39):39453948.
19. Sweers KKM, van der Werf KO, Bennink ML, Subramaniam V (2012) Atomic force microscopy under controlled conditions reveals structure of C-terminal region of a-synuclein in amyloid fibrils. ACS Nano 6(7):5952-5960.
20. Collins SR, Douglass A, Vale RD, Weissman JS (2004) Mechanism of prion propagation: Amyloid growth occurs by monomer addition. PLoS Biol 2(10):e321.
21. Lorenzen N, et al. (2012) Role of elongation and secondary pathways in S6 amyloid fibril growth. Biophys J 102(9):2167-2175.
22. Buell AK, et al. (2010) Frequency factors in a landscape model of filamentous protein aggregation. Phys Rev Lett 104(22):228101.
23. Serio TR, et al. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289(5483):1317-1321. (Pubitemid 30656041)
24. Giehm L, Svergun DI, Otzen DE, Vestergaard B (2011) Low-resolution structure of a vesicle disrupting α-synuclein oligomer that accumulates during fibrillation. Proc Natl Acad Sci USA 108(8):3246-3251.
25. Xue W-F, Homans SW, Radford SE (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc Natl Acad Sci USA 105(26):8926-8931.
26. Wang C, Shah N, Thakur G, Zhou F, Leblanc RM (2010) Alpha-synuclein in alpha-helical conformation at air-water interface: Implication of conformation and orientation changes during its accumulation/aggregation. Chem Commun (Camb) 46(36):6702-6704.
27. Campioni S, et al. (2014) The presence of an air-water interface affects formation and elongation of α-Synuclein fibrils. J Am Chem Soc 136(7):2866-2875.
28. Zhu M, Li J, Fink AL (2003) The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. J Biol Chem 278(41):40186-40197. (Pubitemid 37248587)
29. Necula M, Chirita CN, Kuret J (2003) Rapid anionic micelle-mediated alpha-synuclein fibrillization in vitro. J Biol Chem 278(47):46674-46680. (Pubitemid 37452245)
30. Ahmad MF, Ramakrishna T, Raman B, Rao ChM (2006) Fibrillogenic and non-fibrillogenic ensembles of SDS-bound human alpha-synuclein. J Mol Biol 364(5):1061-1072. (Pubitemid 44765047)
31. Pronchik J, He X, Giurleo JT, Talaga DS (2010) In vitro formation of amyloid from alpha-synuclein is dominated by reactions at hydrophobic interfaces. J Am Chem Soc 132(28):9797-9803.
32. Cremades N, et al. (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell 149(5):1048-1059.
33. Sasahara K, Yagi H, Sakai M, Naiki H, Goto Y (2008) Amyloid nucleation triggered by agitation of beta2-microglobulin under acidic and neutral pH conditions. Biochemistry 47(8):2650-2660. (Pubitemid 351304570)
34. Giehm L, Oliveira CLP, Christiansen G, Pedersen JS, Otzen DE (2010) SDS-induced fibrillation of alpha-synuclein: An alternative fibrillation pathway. J Mol Biol 401(1): 115-133.
35. Eisenthal R, Cornish-Bowden A (1974) The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters. Biochem J 139(3):715-720.
36. Kar K, Jayaraman M, Sahoo B, Kodali R, Wetzel R (2011) Critical nucleus size for disease-related polyglutamine aggregation is repeat-length dependent. Nat Struct Mol Biol 18(3):328-336.
37. Buell AK, et al. (2012) Detailed analysis of the energy barriers for amyloid fibril growth. Angew Chem Int Ed Engl 51(21):5247-5251.
38. Xue W-F, Radford SE (2013) An imaging and systems modeling approach to fibril breakage enables prediction of amyloid behavior. Biophys J 105(12):2811-2819.
39. Croke RL, Patil SM, Quevreaux J, Kendall DA, Alexandrescu AT (2011) NMR determination of pKa values in α-synuclein. Protein Sci 20(2):256-269.
40. Kesvatera T, Jönsson B, Thulin E, Linse S (1996) Measurement and modelling of sequence-specific pKa values of lysine residues in calbindin D9k. J Mol Biol 259(4):828-839. (Pubitemid 26226020)
41. Hu X, et al. (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci USA 106(48):20324-20329.
42. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14(5):504-506. (Pubitemid 351655212)
43. Desplats P, et al. (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 106(31):13010-13015.
44. Hoyer W, et al. (2002) Dependence of alpha-synuclein aggregate morphology on solution conditions. J Mol Biol 322(2):383-393.