Kinetic analysis reveals the diversity of microscopic mechanisms through which molecular chaperones suppress amyloid formation

Nature Communications

Volumn 7, Issue , 2016, Pages

  Arosio, Paolo ^a   Michaels, Thomas C T ^a   Linse, Sara ^b   Månsson, Cecilia ^b   Emanuelsson, Cecilia ^b   Presto, Jenny ^c   Johansson, Jan ^c   Vendruscolo, Michele ^a   Dobson, Christopher M ^a   Knowles, Tuomas P J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; CHAPERONE; AMYLOID BETA PROTEIN;

COMPLEXITY; CONNECTIVITY; MICROSCOPY; NUMERICAL MODEL; PROTEIN; REACTION KINETICS; TOPOLOGY;

ARTICLE; CHEMICAL REACTION KINETICS; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; HUMAN; KINETICS; METABOLISM; MOLECULAR MODEL;

AMYLOID; AMYLOID BETA-PEPTIDES; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR CHAPERONES;

EID: 84961620982     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10948     Document Type: Article

References (50)

1. Chiti, F., Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006).
2. Knowles, T. P. J., Vendruscolo, M., Dobson, C. M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396 (2014).
3. Eisenberg, D., Jucker, M. The amyloid state of proteins in human diseases. Cell 148, 1188-1203 (2012).
4. Hardy, J., Selkoe, D. J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 (2002).
5. Lansbury, P. T., Lashuel, H. A. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443, 774-779 (2006).
6. Hartl, F. U., Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858 (2002).
7. Hartl, F. U., Bracher, A., Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
8. Balch, W. E., Morimoto, R. I., Dillin, A., Kelly, J. W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008).
9. Muchowski, P. J. et al. Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl Acad. Sci. USA 97, 7841-7846 (2000).
10. Muchowski, P. J., Wacker, J. L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11-22 (2005).
11. Jones, G. W., Tuite, M. F. Chaperoning prions: the cellular machinery for propagating an infectious protein? Bioessays 27, 823-832 (2005).
12. Perrett, S., Jones, G. W. Insights into the mechanism of prion propagation. Curr. Opin. Struct. Biol. 18, 52-59 (2008).
13. Zhang, H., Xu, L. Q., Perrett, S. Studying the effects of chaperones on amyloid fibril formation. Methods 53, 285-294 (2011).
14. Mannini, B. et al. Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc. Natl Acad. Sci. USA 109, 12479-12484 (2012).
15. Månsson, C. et al. DNAJB6 is a peptide-binding chaperone which can suppress amyloid fibrillation of polyglutamine peptides at substoichiometric molar ratios. Cell Stress Chaperones 19, 227-239 (2014).
16. Shammas, S. L. et al. Binding of the molecular chaperone aB-crystallin to Ab amyloid fibrils inhibits fibril elongation. Biophys. J. 101, 1681-1689 (2011).
17. Knowles, T. P. J. et al. Kinetics and thermodynamics of amyloid formation from direct measurements of fluctuations in fibril mass. Proc. Natl Acad. Sci. USA 104, 10016-10021 (2007).
18. Dedmon, M. M., Christodoulou, J., Wilson, M. R., Dobson, C. M. Heat shock protein 70 inhibits alpha-synuclein fibril formation via preferential binding to prefibrillar species. J. Biol. Chem. 280, 14733-14740 (2005).
19. Ferrone, F. A., Hofrichter, J., Eaton, W. A. Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism. J. Mol. Biol. 183, 611-631 (1985).
20. Ferrone, F. Analysis of protein aggregation kinetics. Methods Enzymol. 309, 256-274 (1999).
21. Knowles, T. P. J. et al. An analytical solution to the kinetics of breakable filament assembly. Science 326, 1533-1537 (2009).
22. Tanaka, M., Collins, S. R., Toyama, B. H., Weissman, J. S. The physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589 (2006).
23. Ruschak, A. M., Miranker, A. D. Fiber-dependent amyloid formation as catalysis of an existing reaction pathway. Proc. Natl. Acad. Sci. USA 104, 12341-12346 (2007).
24. Foderà, V., Librizzi, F., Groenning, M., van de Weert, M., Leone, M. Secondary nucleation and accessible surface in insulin amyloid fibril formation. J. Phys. Chem. B 112, 3853-3858 (2008).
25. Cohen, S. I. A. et al. Proliferation of amyloid beta42 aggregates occurs through a secondary nucleation mechanism. Proc. Natl. Acad. Sci. USA 110, 9758-9763 (2013).
26. Cohen, S. I. A., Vendruscolo, M., Dobson, C. M., Knowles, T. P. J. From macroscopic measurements to microscopic mechanisms of protein aggregation. J. Mol. Biol. 421, 160-171 (2012).
27. Arosio, P., Cukalevski, R., Birgitta, F., Knowles, T. P. J., Linse, S. A quantitative amyloid chain reaction assay reveals the presence of Ab42 fibrils during the lag-phase. J. Am. Chem. Soc. 136, 219-225 (2014).
28. Arosio, P., Knowles, T. P. J., Linse, S. On the lag phase in amyloid fibril formation. Phys. Chem. Chem. Phys. 17, 7606-7618 (2015).
29. Cohen, S. I. A. et al. Nucleated polymerization with secondary pathways. I. Time evolution of the principal moments. J. Chem. Phys. 135, 065105 (2011).
30. Cohen, S. I. A., Vendruscolo, M., Dobson, C. M., Knowles, T. P. J. Nucleated polymerization with secondary pathways. II. Determination of self-consistent solutions to growth processes described by non-linear master equations. J. Chem. Phys. 135, 065106 (2011).
31. Månsson, C. et al. Interaction of the molecular chaperone DNAJB6 with growing amyloid-beta 42 (A42) aggregates leads to sub-stoichiometric inhibition of amyloid formation. J. Biol. Chem. 289, 31066-31076 (2014).
32. Xu, L. et al. Influence of specific Hsp70 domains on fibril formation of the yeast prion protein Ure2. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20110410 (2013).
33. Cohen, S. I. A. et al. A molecular chaperone breaks the catalytic cycle that generates toxic Ab2 oligomers. Nat. Struct. Mol. Biol. 22, 207-2013 (2015).
34. Arosio, P., Vendruscolo, M., Dobson, C. M., Knowles, T. P. J. Chemical kinetics for drug discovery to combat protein aggregation diseases. Trends Pharmacol. Sci. 35, 127-135 (2014).
35. Michaels, T. C. T., Knowles, T. P. J. Kinetic theory of protein filament growth: Self-consistent methods and perturbative techniques. Int. J. Mod. Phys. B 29, 1530002 (2015).
36. Segel, I. H. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems (Wiley Classis Library, 1993).
37. Hamley, I. W. The amyloid beta peptide: a chemist's perspective. Role in Alzheimer's and fibrillization. Chem. Rev. 112, 5147-5192 (2012).
38. Bartolini, M., Andrisano, V. Strategies for the inhibition of protein aggregation in human diseases. Chembiochem 11, 1018-1035 (2010).
39. Porat, Y., Abramowitz, A., Gazit, E. Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug Des. 67, 27-37 (2006).
40. Ehrnhoefer, D. E. et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566 (2008).
41. Abelein, A., Bolognesi, B., Dobson, C. M., Graslund, A., Lendel, C. Hydrophobicity and conformational change as mechanistic determinants for nonspecific modulators of amyloid b self-assembly. Biochemistry 51, 126-137 (2012).
42. Sievers, S. A. et al. Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation. Nature 475, 96-100 (2011).
43. Cohen, F. E., Kelly, J. W. Therapeutic approaches to protein-misfolding diseases. Nature 426, 905-909 (2003).
44. Cabaleiro-Lago, C. et al. Inhibition of amyloid beta protein fibrillation by polymeric nanoparticles. J. Am. Chem. Soc. 130, 15437-15443 (2008).
45. Cabaleiro-Lago, C., Quinlan-Pluck, F., Lynch, I., Dawson, K. A., Linse, S. Dual effect of amino modified polystyrene nanoparticles on amyloid beta protein fibrillation. ACS Chem. Neurosci. 1, 279-287 (2010).
46. Vacha, R., Linse, S., Lund, M. Surface effects on aggregation kinetics of amyloidogenic peptides. J. Am. Chem. Soc. 136, 11776-11782 (2014).
47. Walsh, D. M. et al. A facile method for expression and purification of the Alzheimer's disease-associated amyloid beta-peptide. FEBS J. 276, 1266-1281 (2009).
48. Boelens, W. C., Croes, Y., de Jong, W. W. Interaction between alpha B-crystallin and the human 20S proteasomal subunit C8/alpha 7. Biochim. Biophys. Acta 1544, 311-319 (2001).
49. Peng, S. et al. The extracellular domain of Bri2 (ITM2B) binds the ABri peptide (1-23) and amyloid beta-peptide (Abeta 1-40): Implications for Bri2 effects on processing of amyloid precursor protein and A beta aggregation. Biochem. Biophys. Res. Commun. 393, 356-361 (2010).
50. Hellstrand, E., Boland, B., Walsh, D. M., Linse, S. Amyloid beta-protein aggregation produces highly reproducible kinetic data and occurs by a two-phase process. ACS Chem. Neurosci. 1, 13-18 (2010).