A generic crystallization-like model that describes the kinetics of amyloid fibril formation

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30585-30594

  Crespo, Rosa ^a   Rocha, Fernando A ^a   Damas, Ana M ^a,b   Martins, Pedro M ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER; AMYLOID DISEASE; AMYLOID FIBRIL; AMYLOID FIBRIL FORMATION; COMPLEX ASSEMBLY; CURVE SHAPE; FIBRILLIZATION; FITTING RESULTS; FUNCTION OF TIME; IN-VITRO; LITERATURE SURVEY; NEURODEGENERATIVE DISORDERS; NUCLEATION AND GROWTH; PRION DISEASE; PROTEIN AGGREGATION; SOLUBLE PROTEINS; TWO PARAMETER; UNDERLYING PRINCIPLES; VISUAL INSPECTION;

GLYCOPROTEINS; HYPERBOLIC FUNCTIONS; KINETICS; NEURODEGENERATIVE DISEASES;

PROTEINS;

AMYLOID;

ARTICLE; CRYSTALLIZATION; KINETICS; MATHEMATICAL MODEL; MATHEMATICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN AGGREGATION; SOLUBILITY; THEORY; THERMODYNAMICS;

AMYLOID; HUMANS; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; NEURODEGENERATIVE DISEASES;

EID: 84865710194     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.375345     Document Type: Article

References (69)

1. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. (1997) Common core structure of amyloid fibrils by synchrotron x-ray diffraction. J. Mol. Biol. 273, 729-739
2. Kelly, J. W. (1997) Amyloid fibril formation and protein misassembly: a structural quest for insights into amyloid and prion diseases. Structure 5, 595-600
3. Greenwald, J., and Riek, R. (2010) Biology of amyloid: structure, function, and regulation. Structure 18, 1244-1260
4. Morris, A. M., Watzky, M. A., and Finke, R. G. (2009) Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature. Biochim. Biophys. Acta 1794, 375-397
5. Roychaudhuri, R., Yang, M., Hoshi, M. M., and Teplow, D. B. (2009) Amyloid β-protein assembly and Alzheimer disease. J. Biol. Chem. 284, 4749-4753
6. Bhak, G., Choe, Y. J., and Paik, S. R. (2009) Mechanism of amyloidogenesis: nucleation-dependent fibrillation versus double-concerted fibrillation. BMB Rep. 42, 541-551
7. Knowles, T. P., Waudby, C. A., Devlin, G. L., Cohen, S. I., Aguzzi, A., Vendruscolo, M., Terentjev, E. M., Welland, M. E., and Dobson, C. M. (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326, 1533-1537
8. Nilsson, M. R. (2004) Techniques to study amyloid fibril formation in vitro. Methods 34, 151-160
9. Bondos, S. E. (2006) Methods for measuring protein aggregation. Curr. Anal. Chem. 2, 157-170
10. Harper, J. D., and Lansbury, P. T. (1997) Models of amyloid seeding in Alzheimer disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu. Rev. Biochem. 66, 385-407
11. Frieden, C. (2007) Protein aggregation processes: in search of the mechanism. Protein Sci. 16, 2334-2344
12. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal. Biochem. 177, 244-249
13. Jarrett, J. T., and Lansbury, P. T., Jr. (1992) Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31, 12345-12352
14. Knowles, T. P., Shu, W., Devlin, G. L., Meehan, S., Auer, S., Dobson, C. M., and Welland, M. E. (2007) Kinetics and thermodynamics of amyloid formation from direct measurements of fluctuations in fibril mass. Proc. Natl. Acad. Sci. U.S.A. 104, 10016-10021
15. Xue, W. F., Homans, S. W., and Radford, S. E. (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc. Natl. Acad. Sci. U.S.A. 105, 8926-8931
16. Naiki, H., Hasegawa, K., Yamaguchi, I., Nakamura, H., Gejyo, F., and Nakakuki, K. (1998) Apolipoprotein E and antioxidants have different mechanisms of inhibiting Alzheimer β-amyloid fibril formation in vitro. Biochemistry 37, 17882-17889
17. Jarrett, J. T., and Lansbury, P. T., Jr. (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer disease and scrapie? Cell 73, 1055-1058
18. Hurshman, A. R., White, J. T., Powers, E. T., and Kelly, J. W. (2004) Transthyretin aggregation under partially denaturing conditions is a downhill polymerization. Biochemistry 43, 7365-7381
19. Naiki, H., Gejyo, F., and Nakakuki, K. (1997) Concentration-dependent inhibitory effects of apolipoprotein E on Alzheimer β-amyloid fibril formation in vitro. Biochemistry 36, 6243-6250
20. Morris, A. M., Watzky, M. A., Agar, J. N., and Finke, R. G. (2008) Fitting neurological protein aggregation kinetic data via a two-step, minimal/"Ockham's razor" model: the Finke-Watzky mechanism of nucleation followed by autocatalytic surface growth. Biochemistry 47, 2413-2427
21. Schmidt, H., Madsen, M. F., Danø, S., and Cedersund, G. (2008) Complexity reduction of biochemical rate expressions. Bioinformatics 24, 848-854
22. Bernacki, J. P., and Murphy, R. M. (2009) Model discrimination and mechanistic interpretation of kinetic data in protein aggregation studies. Biophys. J. 96, 2871-2887
23. Watzky, M. A., and Finke, R. G. (1997) Transition metal nanocluster formation kinetic and mechanistic studies: a new mechanism when hydrogen is the reductant: slow, continuous nucleation and fast autocatalytic surface growth. J. Am. Chem. Soc. 119, 10382-10400
24. 13C NMR. Protein Sci. 9, 867-877
25. Fernández, C. O., Hoyer, W., Zweckstetter, M., Jares-Erijman, E. A., Subramaniam, V., Griesinger, C., and Jovin, T. M. (2004) NMR of α-synuclein- polyamine complexes elucidates the mechanism and kinetics of induced aggregation. EMBO J. 23, 2039-2046
26. Ferrone, F. (1999) Analysis of protein aggregation kinetics. Methods Enzymol. 309, 256-274
27. Watzky, M. A., Morris, A. M., Ross, E. D., and Finke, R. G. (2008) Fitting yeast and mammalian prion aggregation kinetic data with the Finke- Watzky two-step model of nucleation and autocatalytic growth. Biochemistry 47, 10790-10800
28. Sluzky, V., Tamada, J. A., Klibanov, A. M., and Langer, R. (1991) Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces. Proc. Natl. Acad. Sci. U.S.A. 88, 9377-9381
29. O'Nuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of Aβ(1-40) amyloid fibril elongation. Biochemistry 44, 12709-12718
30. Hasegawa, K., Ono, K., Yamada, M., and Naiki, H. (2002) Kinetic modeling and determination of reaction constants of Alzheimer β-amyloid fibril extension and dissociation using surface plasmon resonance. Biochemistry 41, 13489-13498
31. Auer, S., and Kashchiev, D. (2010) Insight into the correlation between lag time and aggregation rate in the kinetics of protein aggregation. Proteins 78, 2412-2416
32. Markov, I. V. (2003) Crystal Growth for Begginers, 2nd Ed., World Scientific Publishing, Singapore
33. Minton, A. P. (2000) Implications of macromolecular crowding for protein assembly. Curr. Opin. Struct. Biol. 10, 34-39
34. Chiti, F., and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22
35. Stöhr, J., Weinmann, N., Wille, H., Kaimann, T., Nagel-Steger, L., Birkmann, E., Panza, G., Prusiner, S. B., Eigen, M., and Riesner, D. (2008) Mechanisms of prion protein assembly into amyloid. Proc. Natl. Acad. Sci. U.S.A. 105, 2409-2414
36. Bhak, G., Lee, J. H., Hahn, J. S., and Paik, S. R. (2009) Granular assembly of α-synuclein leading to the accelerated amyloid fibril formation with shear stress. PLoS ONE 4, e4177
37. Kashchiev, D. (2000) Nucleation: Basic Theory with Applications, Butterworth-Heinemann, Oxford
38. Kashchiev, D., and Auer, S. (2010) Nucleation of amyloid fibrils. J. Chem. Phys. 132, 215101
39. Zhang, T. H., and Liu, X. Y. (2009) Nucleation: what happens at the initial stage? Angew. Chem. Int. Ed. Engl. 48, 1308-1312
40. Padrick, S. B., and Miranker, A. D. (2002) Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis. Biochemistry 41, 4694-4703
41. Heldt, C. L., Zhang, S., and Belfort, G. (2011) Asymmetric amyloid fibril elongation: a new perspective on a symmetric world. Proteins 79, 92-98
42. Ban, T., and Goto, Y. (2006) Direct observation of amyloid growth monitored by total internal reflection fluorescence microscopy. Methods Enzymol. 413, 91-102
43. Collins, S. R., Douglass, A., Vale, R. D., and Weissman, J. S. (2004) Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2, e321
44. Patil, S. M., Mehta, A., Jha, S., and Alexandrescu, A. T. (2011) Heterogeneous amylin fibril growth mechanisms imaged by total internal reflection fluorescence microscopy. Biochemistry 50, 2808-2819
45. Scheibel, T., Kowal, A. S., Bloom, J. D., and Lindquist, S. L. (2001) Bidirectional amyloid fiber growth for a yeast prion determinant. Curr. Biol. 11, 366-369
46. Goldsbury, C., Kistler, J., Aebi, U., Arvinte, T., and Cooper, G. J. (1999) Watching amyloid fibrils grow by time-lapse atomic force microscopy. J. Mol. Biol. 285, 33-39
47. Ionescu-Zanetti, C., Khurana, R., Gillespie, J. R., Petrick, J. S., Trabachino, L. C., Minert, L. J., Carter, S. A., and Fink, A. L. (1999) Monitoring the assembly of Ig light-chain amyloid fibrils by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 13175-13179
48. Ruschak, A. M., and Miranker, A. D. (2007) Fiber-dependent amyloid formation as catalysis of an existing reaction pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 12341-12346
49. Martins, P. M., and Rocha, F. (2007) Characterization of crystal growth using a spiral nucleation model. Surf. Sci. 601, 3400-3408
50. Martins, P. M., and Rocha, F. (2007) New developments on size-dependent growth applied to the crystallization of sucrose. Surf. Sci. 601, 5466-5472
51. Martins, P. M., and Rocha, F. A. (2008) Kinetic studies on the influence of temperature and growth rate history on crystal growth. Cryst. Res. Technol. 43, 1258-1267
52. 2-microglobulin with tryptophan mutagenesis. J. Mol. Biol. 400, 1057-1066
53. 2-microglobulin fibril elongation probed by pulse-labeling H/D exchange combined with NMR analysis. J. Mol. Biol. 405, 851-862
54. Jiménez, J. L., Nettleton, E. J., Bouchard, M., Robinson, C. V., Dobson, C. M., and Saibil, H. R. (2002) The protofilament structure of insulin amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 99, 9196-9201
55. Santoso, A., Chien, P., Osherovich, L. Z., and Weissman, J. S. (2000) Molecular basis of a yeast prion species barrier. Cell 100, 277-288
56. Smith, J. F., Knowles, T. P., Dobson, C. M., Macphee, C. E., and Welland, M. E. (2006) Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 103, 15806-15811
57. Xue, W. F., Hellewell, A. L., Gosal, W. S., Homans, S. W., Hewitt, E. W., and Radford, S. E. (2009) Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272-34282
58. 2- microglobulin. J. Biol. Chem. 280, 32843-32848
59. Kim, H. J., Chatani, E., Goto, Y., and Paik, S. R. (2007) Seed-dependent accelerated fibrillation of α-synuclein induced by periodic ultrasonication treatment. J. Microbiol. Biotechnol. 17, 2027-2032
60. Giehm, L., and Otzen, D. E. (2010) Strategies to increase the reproducibility of protein fibrillization in plate reader assays. Anal. Biochem. 400, 270-281
61. Fändrich, M. (2007) Absolute correlation between lag time and growth rate in the spontaneous formation of several amyloid-like aggregates and fibrils. J. Mol. Biol. 365, 1266-1270
62. 2-microglobulin under acidic and neutral pH conditions. Biochemistry 47, 2650-2660
63. Rochet, J. C., and Lansbury, P. T., Jr. (2000) Amyloid fibrillogenesis: themes and variations. Curr. Opin. Struct. Biol. 10, 60-68
64. 2- microglobulin amyloid formation in vitro. Biochim. Biophys. Acta 1753, 51-63
65. Tanaka, M., Collins, S. R., Toyama, B. H., and Weissman, J. S. (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589
66. White, D. A., Buell, A. K., Knowles, T. P., Welland, M. E., and Dobson, C. M. (2010) Protein aggregation in crowded environments. J. Am. Chem. Soc. 132, 5170-5175
67. Baskakov, I. V., and Bocharova, O. V. (2005) In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry 44, 2339-2348
68. Pronchik, J., He, X., Giurleo, J. T., and Talaga, D. S. (2010) In vitro formation of amyloid from α-synuclein is dominated by reactions at hydrophobic interfaces. J. Am. Chem. Soc. 132, 9797-9803
69. Toyama, B. H., Kelly, M. J., Gross, J. D., and Weissman, J. S. (2007) The structural basis of yeast prion strain variants. Nature 449, 233-237