Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation

Nature

Volumn 524, Issue 7564, 2015, Pages 247-251

  Nillegoda, Nadinath B ^a   Kirstein, Janine ^b   Szlachcic, Anna ^a   Berynskyy, Mykhaylo ^c   Stank, Antonia ^c,d   Stengel, Florian ^e   Arnsburg, Kristin ^b   Gao, Xuechao ^a   Scior, Annika ^b   Aebersold, Ruedi ^e,f   Guilbride, D Lys ^a   Wade, Rebecca C ^a,c,d   Morimoto, Richard I ^g   Mayer, Matthias P ^a   Bukau, Bernd ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e ETH ZURICH   (Switzerland)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHAPERONE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; J PROTEIN; MALATE DEHYDROGENASE; MULTIPROTEIN COMPLEX; UNCLASSIFIED DRUG; PROTEIN AGGREGATE; PROTEIN BINDING;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; GENE EXPRESSION; METAZOAN; PROTEIN; QUALITY CONTROL;

ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CROSS LINKING; DIMERIZATION; ENERGY TRANSFER; HUMAN; HYDROLYSIS; IN VITRO STUDY; MOLECULAR DOCKING; NONHUMAN; PHOTINUS PYRALIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN DISAGGREGATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN QUALITY; PROTEIN REFOLDING; PROTEIN STRUCTURE; REACTION TIME; REGULATORY MECHANISM; SOLUBILIZATION; STOICHIOMETRY; SUBSTRATE CONCENTRATION; SURFACE PROPERTY; TEMPERATURE STRESS; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY;

METAZOA;

ANIMALS; CAENORHABDITIS ELEGANS; HSP110 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY;

EID: 84939559331     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14884     Document Type: Article

References (59)

1. Hipp, M. S., Park, S. H. & Hartl, F. U. Proteostasis impairment in protein-misfolding and -aggregation diseases. Trends Cell Biol. 24, 506-514 (2014
2. Morimoto, R. I. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438 (2008
3. Kirstein-Miles, J., Scior, A., Deuerling, E. & Morimoto, R. I. The nascent polypeptideassociated complex is a key regulator of proteostasis. EMBO J. 32, 1451-1468 (2013
4. Rampelt, H., et al. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J. 31, 4221-4235 (2012
5. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T. & Bukau, B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl Acad. Sci. USA 96, 13732-13737 (1999
6. Parsell, D. A., Kowal, A. S., Singer, M. A. & Lindquist, S. Protein disaggregation mediated by heat-shock protein HSP104. Nature 372, 475-478 (1994
7. Shorter, J. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 andHsp40to catalyze protein disaggregation and reactivation ina cell-free system. PLoS ONE 6, e26319 (2011
8. Mayer, M. P. & Bukau, B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684 (2005
9. Kampinga, H. H. & Craig, E. A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nature Rev. Mol. Cell Biol. 11, 579-592 (2010
10. Cyr, D. M. & Ramos, C. H. Specification of Hsp70 function by type I and type II HSP40. Subcell. Biochem. 78, 91-102 (2015
11. Sahi, C. & Craig, E. A. Network of general and specialty J protein chaperones of the yeast cytosol. Proc. Natl Acad. Sci. USA 104, 7163-7168 (2007
12. Tzankov, S., Wong, M. J., Shi, K., Nassif, C. & Young, J. C. Functional divergence between co-chaperones of Hsc70. J. Biol. Chem. 283, 27100-27109 (2008
13. Rauch, J. N. & Gestwicki, J. E. Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J. Biol. Chem. 289, 1402-1414 (2014
14. Lu, Z. & Cyr, D.M. Protein folding activity ofHSP70 ismodified differentially by the Hsp40 co-chaperones Sis1 and Ydj1. J. Biol. Chem. 273, 27824-27830 (1998
15. Weibezahn, J., et al. Thermotolerance requires refolding of aggregated proteins by substrate translocationthroughthe central pore ofClpB. Cell 119, 653-665 (2004
16. Ramos, C. H., Oliveira, C. L., Fan, C. Y., Torriani, I. L. & Cyr, D. M. Conserved central domains control the quaternary structure of type I and type II HSP40 molecular chaperones. J. Mol. Biol. 383, 155-166 (2008
17. Borges, J. C., Fischer, H., Craievich, A. F. & Ramos, C. H. Low resolution structural study of two human HSP40 chaperones in solution. DJA1 from subfamily A and DJB4 from subfamily B have different quaternary structures. J. Biol. Chem. 280, 13671-13681 (2005
18. 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. 271, 9347-9354 (1996
19. Suh,W. C., Lu, C. Z. & Gross, C. A. Structural features required for the interaction of the Hsp70 molecular chaperone DnaK with its cochaperone DnaJ. J. Biol. Chem. 274, 30534-30539 (1999
20. Genevaux, P., Schwager, F., Georgopoulos, C.&Kelley, W. L. Scanningmutagenesis identifies amino acid residues essential for the in vivo activity of the Escherichia coli DnaJ (Hsp40) J-domain. Genetics 162, 1045-1053 (2002
21. De Los Rios, P., Ben-Zvi, A., Slutsky, O., Azem, A. & Goloubinoff, P. Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling. Proc. Natl Acad. Sci. USA 103, 6166-6171 (2006
22. Caughey, B. & Lansbury, P. T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298 (2003
23. Cheetham, M. E. & Caplan, A. J. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3, 28-36 (1998
24. Li, J., Qian, X. & Sha, B. The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 11, 1475-1483 (2003
25. Lu, Z. & Cyr, D.M. The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J. Biol. Chem. 273, 5970-5978 (1998
26. Andréasson, C., Fiaux, J., Rampelt, H., Mayer, M. P. & Bukau, B. Hsp110 is a nucleotide-activated exchange factor for Hsp70. J. Biol. Chem. 283, 8877-8884 (2008
27. Cashikar, A. G., Duennwald, M. & Lindquist, S. L. A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J. Biol. Chem. 280, 23869-23875 (2005
28. Haslbeck, M., Miess, A., Stromer, T., Walter, S. & Buchner, J. Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J. Biol. Chem. 280, 23861-23868 (2005
29. Carra, S., et al. Different anti-aggregation and pro-degradative functions of the members of the mammalian sHSP family in neurological disorders. Phil. Trans. R. Soc. Lond. B 368, 20110409 (2013
30. Vos,M. J., et al. HSPB7 is themost potent polyQ aggregation suppressor within the HSPB family of molecular chaperones. Hum. Mol. Genet. 19, 4677-4693 (2010
31. Skouri-Panet, F., Michiel, M., Ferard, C., Duprat, E. & Finet, S. Structural and functional specificity of small heat shock protein HspB1 and HspB4, two cellular partners of HspB5: role of the in vitro hetero-complex formation in chaperone activity. Biochimie 94, 975-984 (2012
32. Peschek, J., et al. Regulated structural transitions unleash the chaperone activity of aB-crystallin. Proc. Natl Acad. Sci. USA 110, E3780-E3789 (2013
33. Leitner, A., et al. Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol. Cell. Proteomics 11, M111.014126 (2012
34. Rinner, O., et al. Identification of cross-linked peptides from large sequence databases. Nature Methods 5, 315-318 (2008
35. Walzthoeni, T., et al. False discovery rate estimation for cross-linked peptides identified by mass spectrometry. Nature Methods 9, 901-903 (2012
36. Adams, S. R., et al. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J.Am. Chem. Soc. 124, 6063-6076 (2002
37. Spagnuolo, C. C., Vermeij, R. J. & Jares-Erijman, E. A. Improved photostable FRETcompetent biarsenical-tetracysteine probes based on fluorinated fluoresceins. J. Am. Chem. Soc. 128, 12040-12041 (2006
38. Dixit, A., Ray, K., Lakowicz, J. R. & Black, L. W. Dynamics of the T4 bacteriophage DNA packasome motor: endonuclease VII resolvase release of arrested Y-DNA substrates. J. Biol. Chem. 286, 18878-18889 (2011
39. Guex, N., Peitsch, M. C. & Schwede, T. Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30 (suppl. 1), S162-S173 (2009
40. Kopp, J. & Schwede, T. The SWISS-MODEL Repository of annotated threedimensional protein structure homology models. Nucleic Acids Res. 32, D230-D234 (2004
41. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. & Schwede, T. The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-D392 (2009
42. Arnold, K.,Bordoli, L.,Kopp, J.&Schwede, T. TheSWISS-MODEL workspace: awebbased environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006
43. Suzuki, H., et al. Peptide-binding sites as revealed by the crystal structures of the human Hsp40 Hdj1 C-terminal domain in complex with the octapeptide from human Hsp70. Biochemistry 49, 8577-8584 (2010
44. Qian, Y. Q., Patel, D.,Hartl, F.U.&McColl, D. J.Nuclearmagnetic resonance solution structure of the human Hsp40 (HDJ-1) J-domain. J. Mol. Biol. 260, 224-235 (1996
45. Martinez, M., et al. SDA7: a modular and parallel implementation of the simulation of diffusional association software. J. Comput. Chem. 36, 1631-1645 (2015
46. Gabdoulline, R. R. & Wade, R. C. Simulation of the diffusional association of barnase and barstar. Biophys. J. 72, 1917-1929 (1997
47. Vriend, G.WHAT IF: amolecularmodeling and drug design program. J. Mol. Graph. 8, 52-56 (1990
48. Madura, J. D., et al. Electrostaticsand diffusionofmolecules insolution: simulations with the University of Houston Brownian Dynamics Program Comp. Phys. Comm. 91, 57-95 (1995
49. Jorgensen, W. L., Maxwell, D. S. & Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236 (1996
50. Gabdoulline, R. R. & Wade, R. C. Effective charges for macromolecules in solvent. J. Phys. Chem. 100, 3868-3878 (1996
51. Elcock, A. H., Gabdoulline, R. R., Wade, R. C. & McCammon, J. A. Computer simulation of protein-protein association kinetics: acetylcholinesterase-fasciculin. J. Mol. Biol. 291, 149-162 (1999
52. Gabdoulline, R. R. & Wade, R. C. On the contributions of diffusion and thermal activation to electron transfer between Phormidiumlaminosumplastocyanin and cytochrome f: Brownian dynamics simulations with explicitmodeling of nonpolar desolvation interactions and electron transfer events. J. Am. Chem. Soc. 131, 9230-9238 (2009
53. Barends, T. R., et al. Combining crystallography and EPR: crystal and solution structures of the multidomain cochaperone DnaJ. Acta Crystallogr. D 69, 1540-1552 (2013
54. Dragovic, Z., Broadley, S. A., Shomura, Y., Bracher, A. & Hartl, F. U. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25, 2519-2528 (2006
55. Raviol, H., Sadlish, H.,Rodriguez, F., Mayer, M. P.&Bukau,B. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 25, 2510-2518 (2006
56. Chen, J., Walter, S., Horwich, A. L. & Smith, D. L. Folding of malate dehydrogenase inside the GroEL-GroES cavity. Nature Struct. Biol. 8, 721-728 (2001
57. Linke, K., Wolfram, T., Bussemer, J. & Jakob, U. The roles of the two zinc binding sites in DnaJ. J. Biol. Chem. 278, 44457-44466 (2003
58. Garimella, R., et al. Hsc70 contacts helix III of the J domain from polyomavirus T antigens: addressing a dilemma in the chaperone hypothesis of how they release E2F from pRb. Biochemistry 45, 6917-6929 (2006
59. Greene, M. K., et al. Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc. Natl Acad. Sci. USA 95, 6108-6113 (1998