Human Hsp70 Disaggregase Reverses Parkinson's-Linked α-Synuclein Amyloid Fibrils

Molecular Cell

Volumn 59, Issue 5, 2015, Pages 781-793

  Gao, Xuechao ^a,b   Carroni, Marta ^c   Nussbaum Krammer, Carmen ^a,b   Mogk, Axel ^a,b   Nillegoda, Nadinath B ^a,b   Szlachcic, Anna ^a,b   Guilbride, D Lys ^b   Saibil, Helen R ^c   Mayer, Matthias P ^b   Bukau, Bernd ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA SYNUCLEIN; AMYLOID; CHAPERONE; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; PROTEIN DNAJ; PROTEIN DNAJB1; UNCLASSIFIED DRUG; DNAJB1 PROTEIN, HUMAN; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 40; HSPA8 PROTEIN, HUMAN; PROTEIN AGGREGATE;

ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; ELECTRON MICROSCOPY; FLUORESCENCE; HUMAN; PARKINSON DISEASE; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN INTERACTION; CHEMISTRY; ELECTRON TOMOGRAPHY; IN VITRO STUDY; KINETICS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEINOSIS; SOLUBILITY; ULTRASTRUCTURE;

ALPHA-SYNUCLEIN; AMYLOID; ELECTRON MICROSCOPE TOMOGRAPHY; HSC70 HEAT-SHOCK PROTEINS; HSP110 HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IN VITRO TECHNIQUES; KINETICS; MOLECULAR CHAPERONES; PARKINSON DISEASE; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN MULTIMERIZATION; SOLUBILITY;

EID: 84940897433     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.07.012     Document Type: Article

References (30)

1. Bieschke J., Cohen E., Murray A., Dillin A., Kelly J.W. A kinetic assessment of the C. elegans amyloid disaggregation activity enables uncoupling of disassembly and proteolysis. Protein Sci. 2009, 18:2231-2241.
2. Bieschke J., Russ J., Friedrich R.P., Ehrnhoefer D.E., Wobst H., Neugebauer K., Wanker E.E. EGCG remodels mature alpha-synuclein and amyloid-beta fibrils and reduces cellular toxicity. Proc. Natl. Acad. Sci. USA 2010, 107:7710-7715.
3. Bukau B., Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell 1998, 92:351-366.
4. Caughey B., Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 2003, 26:267-298.
5. Chen B., Retzlaff M., Roos T., Frydman J. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 2011, 3:a004374.
6. Duennwald M.L., Echeverria A., Shorter J. Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans. PLoS Biol. 2012, 10:e1001346.
7. Evans C.G., Wisén S., Gestwicki J.E. Heat shock proteins 70 and 90 inhibit early stages of amyloid beta-(1-42) aggregation in vitro. J. Biol. Chem. 2006, 281:33182-33191.
8. Finka A., Goloubinoff P. Proteomic data from human cell cultures refine mechanisms of chaperone-mediated protein homeostasis. Cell Stress Chaperones 2013, 18:591-605.
9. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007, 8:101-112.
10. Inoue Y., Yoshida M. In vitro assay for fragmentation of amyloid fibers of yeast prion protein. Methods 2006, 39:56-60.
11. Jarrett J.T., Lansbury P.T. Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie?. Cell 1993, 73:1055-1058.
12. Khurana R., Ionescu-Zanetti C., Pope M., Li J., Nielson L., Ramírez-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.
13. Kim Y.E., Hipp M.S., Bracher A., Hayer-Hartl M., Hartl F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 2013, 82:323-355.
14. Kityk R., Kopp J., Sinning I., Mayer M.P. Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol. Cell 2012, 48:863-874.
15. Knowles T.P., Vendruscolo M., Dobson C.M. The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 2014, 15:384-396.
16. Mattoo R.U., Sharma S.K., Priya S., Finka A., Goloubinoff P. Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates. J. Biol. Chem. 2013, 288:21399-21411.
17. Mayer M.P. Hsp70 chaperone dynamics and molecular mechanism. Trends Biochem. Sci. 2013, 38:507-514.
18. Murray A.N., Solomon J.P., Wang Y.J., Balch W.E., Kelly J.W. Discovery and characterization of a mammalian amyloid disaggregation activity. Protein Sci. 2010, 19:836-846.
19. Murray A.N., Palhano F.L., Bieschke J., Kelly J.W. Surface adsorption considerations when working with amyloid fibrils in multiwell plates and Eppendorf tubes. Protein Sci. 2013, 22:1531-1541.
20. Nillegoda N.B., Kirstein J., Szlachcic A., Berynskyy M., Stank A., Stengel F., Arnsburg K., Gao X., Scior A., Aebersold R., et al. Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation. Nature 2015, Published online August 5, 2015. 10.1038/nature14884.
21. Nollen E.A., Brunsting J.F., Song J., Kampinga H.H., Morimoto R.I. Bag1 functions in vivo as a negative regulator of Hsp70 chaperone activity. Mol. Cell. Biol. 2000, 20:1083-1088.
22. Pieri L., Madiona K., Bousset L., Melki R. Fibrillar α-synuclein and huntingtin exon 1 assemblies are toxic to the cells. Biophys. J. 2012, 102:2894-2905.
23. Pierpaoli E.V., Gisler S.M., Christen P. Sequence-specific rates of interaction of target peptides with the molecular chaperones DnaK and DnaJ. Biochemistry 1998, 37:16741-16748.
24. Rampelt H., Kirstein-Miles J., Nillegoda N.B., Chi K., Scholz S.R., Morimoto R.I., Bukau B. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J. 2012, 31:4221-4235.
25. Shorter J. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS ONE 2011, 6:e26319.
26. Shorter J., Lindquist S. Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 2004, 304:1793-1797.
27. Tsai J., Douglas M.G. A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J. Biol. Chem. 1996, 271:9347-9354.
28. van Ham T.J., Thijssen K.L., Breitling R., Hofstra R.M., Plasterk R.H., Nollen E.A. C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. PLoS Genet. 2008, 4:e1000027.
29. Vilar M., Chou H.T., Lührs T., Maji S.K., Riek-Loher D., Verel R., Manning G., Stahlberg H., Riek R. The fold of alpha-synuclein fibrils. Proc. Natl. Acad. Sci. USA 2008, 105:8637-8642.
30. Winkler J., Tyedmers J., Bukau B., Mogk A. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J. Cell Biol. 2012, 198:387-404.