Interaction of the molecular chaperone DNAJB6 with growing amyloid-beta 42 (Aβ42) aggregates leads to sub-stoichiometric inhibition of amyloid formation

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31066-31076

  Månsson, Cecilia ^a   Arosio, Paolo ^b   Hussein, Rasha ^c,d   Kampinga, Harm H ^c   Hashem, Reem M ^d   Boelens, Wilbert C ^e   Dobson, Christopher M ^b   Knowles, Tuomas P J ^b   Linse, Sara ^a   Emanuelsson, Cecilia ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d Beni Suef University   (Egypt)

^e RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; BIOCHEMISTRY; CIRCULAR DICHROISM SPECTROSCOPY; DISSOCIATION; DYES; NEURODEGENERATIVE DISEASES; NUCLEATION; PEPTIDES;

AMYLOID-BETA PEPTIDES; INHIBITORY ACTIVITY; MOLECULAR CHAPERONE PROTEINS; MOLECULAR CHAPERONES; NEURODEGENERATIVE DISORDERS; PROTEIN AGGREGATION; QUANTITATIVE KINETICS; SECONDARY NUCLEATION;

GLYCOPROTEINS;

AMYLOID BETA 42 PROTEIN; AMYLOID BETA PROTEIN; PROTEIN DNAJ; PROTEIN DNAJB6; THIOFLAVINE; UNCLASSIFIED DRUG; ALPHA CRYSTALLIN; AMYLOID; AMYLOID BETA-PROTEIN (1-42); CHAPERONE; DNAJB6 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 40; NERVE PROTEIN; PEPTIDE FRAGMENT; PROTEIN BINDING; SERUM ALBUMIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; MOLECULAR INTERACTION; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN UNFOLDING; STOICHIOMETRY; ULTRAVIOLET SPECTROSCOPY; CELL PROLIFERATION; CIRCULAR DICHROISM; DEGENERATIVE DISEASE; HUMAN; KINETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ALPHA-CRYSTALLIN B CHAIN; AMYLOID; AMYLOID BETA-PEPTIDES; CELL PROLIFERATION; CIRCULAR DICHROISM; HSP40 HEAT-SHOCK PROTEINS; HUMANS; KINETICS; MOLECULAR CHAPERONES; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SERUM ALBUMIN;

EID: 84909951802     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.595124     Document Type: Article

References (54)

1. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
2. Cohen, A. S., and Calkins, E. (1959) Electron microscopic observations on a fibrous component in amyloid of diverse origins. Nature 183, 1202-1203
3. Dobson, C. M. (1999) Protein misfolding, evolution and disease. Trends Biochem. Sci 24, 329-332
4. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447, 453-457
5. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424, 805-808
6. Greenwald, J., and Riek, R. (2010) Biology of amyloid: structure, function, and regulation. Structure 18, 1244-1260
7. Selkoe, J. D. (2011) Alzheimer's disease. Cold Spring Harbor Perspectives in Biology, Vol. 3
8. Fändrich, M., Schmidt, M., and Grigorieff, N. (2011) Recent progress in understanding Alzheimer's β-amyloid structures. Trends Biochem. Sci. 36, 338-345
9. Walsh, D. M., and Teplow, D. B. (2012) Alzheimer's disease and the amyloid β-protein. Prog. Mol. Biol. Transl. Sci. 107, 101-124
10. Cohen, S. I., Linse, S., Luheshi, L. M., Hellstrand, E., White, D. A., Rajah, L., Otzen, D. E., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. (2013) Proliferation of amyloid-β42 aggregates occurs through a secondary nucleation mechanism. Proc. Natl. Acad. Sci. U.S.A. 110, 9758-9763
11. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539
12. Bucciantini, M., Giannoni, E., Chiti, F., Baroni, F., Formigli, L., Zurdo, J., Taddei, N., Ramponi, G., Dobson, C. M., and Stefani, M. (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511
13. Fändrich, M. (2012) Oligomeric intermediates in amyloid formation: structure determination and mechanisms of toxicity. J. Mol. Biol. 421, 427-440
14. Meisl, G., Yang, X., Hellstrand, E., Frohm, B., Kirkegaard, J. B., Cohen, S. I., Dobson, C. M., Linse, S., and Knowles, T. P. (2014) Differences in nucleation behavior underlie the contrasting aggregation kinetics of the Aβ40 and Aβ42 peptides. Proc. Natl. Acad. Sci. U.S.A. 111, 9384-9389
15. Arosio, P., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. (2014) Chemical kinetics for drug discovery to combat protein aggregation diseases. Trends Pharmacol. Sci. 35, 127-135
16. Cohen, S. I. A., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. J. (2012) From Macroscopic Measurements to Microscopic Mechanisms of Protein Aggregation. J. Mol. Biol. 421, 160-171
17. 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
18. Hellstrand, E., Boland, B., Walsh, D. M., and Linse, S. (2010) Amyloid β-protein aggregation produces highly reproducible kinetic data and occurs by a two-phase process. ACS Chemical Neuroscience 1, 13-18
19. Willander, H., Presto, J., Askarieh, G., Biversta˚l, H., Frohm, B., Knight, S. D., Johansson, J., and Linse, S. (2012) BRICHOS domains efficiently delay fibrillation of amyloid β-peptide. J. Biol. Chem. 287, 31608-31617
20. Ferrone, F. A., Hofrichter, J., and Eaton, W. A. (1985) Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism. J. Mol. Biol. 183, 611-631
21. Shammas, S. L., Waudby, C. A., Wang, S., Buell, A. K., Knowles, T. P., Ecroyd, H., Welland, M. E., Carver, J. A., Dobson, C. M., and Meehan, S. (2011) Binding of the molecular chaperone αB-crystallin to Aβ amyloid fibrils inhibits fibril elongation. Biophys. J. 101, 1681-1689
22. Ecroyd, H., and Carver, J. A. (2009) Crystallin proteins and amyloid fibrils. Cell. Mol. Life Sci. 66, 62-81
23. Härd, T., and Lendel, C. (2012) Inhibition of amyloid formation. J. Mol. Biol. 421, 441-465
24. Ellis, R. J. (2013) Assembly chaperones: a perspective. Phil. Trans. R. Soc. B 10.1098/rstb.2011.0398
25. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332
26. Kampinga, H. H. (1993) Thermotolerance in Mammalian-Cells - PROTEIN Denaturation and Aggregation, and Stress Proteins. J. Cell Sci. 104, 11-17
27. Morimoto, R. I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438
28. Tyedmers, J., Mogk, A., and Bukau, B. (2010) Cellular strategies for controlling protein aggregation. Nature Reviews Molecular Cell Biology 11, 777-788
29. Mannini, B., Cascella, R., Zampagni, M., van Waarde-Verhagen, M., Meehan, S., Roodveldt, C., Campioni, S., Boninsegna, M., Penco, A., Relini, A., Kampinga, H. H., Dobson, C. M., Wilson, M. R., Cecchi, C., and Chiti, F. (2012) Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc. Natl. Acad. Sci. U.S.A. 109, 12479-12484
30. Narayan, P., Meehan, S., Carver, J. A., Wilson, M. R., Dobson, C. M., and Klenerman, D. (2012) Amyloid-β oligomers are sequestered by both intracellular and extracellular chaperones. Biochemistry 51, 9270-9276
31. Goldstein, L. E., Muffat, J. A., Cherny, R. A., Moir, R. D., Ericsson, M. H., Huang, X., Mavros, C., Coccia, J. A., Faget, K. Y., Fitch, K. A., Masters, C. L., Tanzi, R. E., Chylack, L. T., Jr., and Bush, A. I. (2003) Cytosolic β-amyloid deposition and supranuclear cataracts in lenses from people with Alzheimer's disease. Lancet 361, 1258-1265
32. Yoo, B. C., Kim, S. H., Cairns, N., Fountoulakis, M., and Lubec, G. (2001) Deranged expression of molecular chaperones in brains of patients with Alzheimer's disease. Biochem. Biophys. Res. Commun. 280, 249-258
33. Hermansson, E., Schultz, S., Crowther, D., Linse, S., Winblad, B., Westermark, G., Johansson, J., and Presto, J. (2014) The chaperone domain BRICHOS prevents CNS toxicity of amyloid-β peptide in Drosophila melanogaster. Disease Models Mechanisms 7, 659-665
34. Ma˚nsson, C., Kakkar, V., Monsellier, E., Sourigues, Y., Härmark, J., Kampinga, H. H., Melki, R., and Emanuelsson, C. (2014) DNAJB6 is a peptidebinding chaperone which can suppress amyloid fibrillation of polyglutamine peptides at substoichiometric molar ratios. Cell Stress Chaperones 19, 227-239
35. Orr, H. T., and Zoghbi, H. Y. (2007) Trinucleotide Repeat Disorders. Annu. Rev. Neurosci. 30, 575-621
36. Wetzel, R. (2012) Physical Chemistry of Polyglutamine: Intriguing Tales of a Monotonous Sequence. J. Mol. Biol. 421, 466-490
37. Walsh, D. M., Thulin, E., Minogue, A. M., Gustavsson, N., Pang, E., Teplow, D. B., and Linse, S. (2009) A facile method for expression and purification of the Alzheimer's disease-associated amyloid β-peptide. FEBS J. 276, 1266-1281
38. Blennow, A., Surin, B. P., Ehring, H., McLennan, N. F., and Spangfort, M. D. (1995) Isolation and biochemical characterization of highly purified Escherichia coli molecular chaperone Cpn60 (GroEL) by affinity chromatography and urea-induced monomerization. Biochim. Biophys. Acta 1252, 69-78
39. Boelens, W. C., Croes, Y., and de Jong, W. W. (2001) Interaction between αB-crystallin and the human 20 S proteasomal subunit C8/α7. Biochim. Biophys. Acta 1544, 311-319
40. Cedervall, T., Lynch, I., Lindman, S., Bergga˚rd, T., Thulin, E., Nilsson, H., Dawson, K. A., and Linse, S. (2007) Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. U.S.A. 104, 2050-2055
41. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
42. Stoscheck, C. M. (1990) Quantitation of protein. Methods Enzymol. 182, 50-68
43. Sørensen, B. K., Højrup, P., Østerga˚rd, E., Jørgensen, C. S., Enghild, J., Ryder, L. R., and Houen, G. (2002) Silver staining of proteins on electroblotting membranes and intensification of silver staining of proteins separated by polyacrylamide gel electrophoresis. Anal. Biochem. 304, 33-41
44. Cohen, S. I., Vendruscolo, M., Welland, M. E., Dobson, C. M., Terentjev, E. M., and Knowles, T. P. (2011) Nucleated polymerization with secondary pathways. I. Time evolution of the principal moments. J. Chem. Phys. 135, 065105
45. Cohen, S. I., Vendruscolo, M., Dobson, C. M., and Knowles, T. P. (2011) 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
46. Ferrone, F. (1999) Analysis of protein aggregation kinetics. Methods Enzymol. 309, 256-274
47. Lorenzen, N., Cohen, S. I., Nielsen, S. B., Herling, T. W., Christiansen, G., Dobson, C. M., Knowles, T. P., and Otzen, D. (2012) Role of elongation and secondary pathways in S6 amyloid fibril growth. Biophys. J. 102, 2167-2175
48. Hageman, J., Rujano, M. A., van Waarde, M. A. W. H., Kakkar, V., Dirks, R. P., Govorukhina, N., Oosterveld-Hut, H. M. J., Lubsen, N. H., and Kampinga, H. H. (2010) A DNAJB Chaperone Subfamily with HDACDependent Activities Suppresses Toxic Protein Aggregation. Mol. Cell 37, 355-369
49. Gillis, J., Schipper-Krom, S., Juenemann, K., Gruber, A., Coolen, S., van den Nieuwendijk, R., van Veen, H., Overkleeft, H., Goedhart, J., Kampinga, H. H., and Reits, E. A. (2013) The DNAJB6 and DNAJB8 protein chaperones prevent intracellular aggregation of polyglutamine peptides. J. Biol. Chem. 288, 17225-17237
50. Evans, C. G., Wisén, S., and Gestwicki, J. E. (2006) Heat shock proteins 70 and 90 inhibit early stages of amyloid β-(1-42) aggregation in vitro. J. Biol. Chem. 281, 33182-33191
51. Kampinga, H. H., and Craig, E. A. (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nature Reviews Molecular Cell Biology 11, 579-592
52. Assarsson, A., Hellstrand, E., Cabaleiro-Lago, C., and Linse, S. (2014) Charge Dependent Retardation of Amyloid β Aggregation by Hydrophilic Proteins. ACS Chemical Neuroscience 5, 266-274
53. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
54. Ladiwala, A. R., Litt, J., Kane, R. S., Aucoin, D. S., Smith, S. O., Ranjan, S., Davis, J., Van Nostrand, W. E., and Tessier, P. M. (2012) Conformational differences between two amyloid beta oligomers of similar size and dissimilar toxicity. J. Biol. Chem. 287, 24765-24773