Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces

Nature Structural and Molecular Biology

Volumn 19, Issue 12, 2012, Pages 1347-1355

  Seyffer, Fabian ^a,b   Kummer, Eva ^a,b   Oguchi, Yuki ^a,b   Winkler, Juliane ^a   Kumar, Mohit ^a,b   Zahn, Regina ^a,b   Sourjik, Victor ^a   Bukau, Bernd ^a,b   Mogk, Axel ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 70; PROTEIN CLPB;

ARTICLE; CHIMERA; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE;

HSP70 HEAT-SHOCK PROTEINS; PROTEIN BINDING;

ESCHERICHIA COLI; FUNGI;

EID: 84870792675     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2442     Document Type: Article

References (45)

1. Hartl, F.U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
2. Doyle, S.M. & Wickner, S. Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 34, 40-48 (2009).
3. Liberek, K., Lewandowska, A. & Zietkiewicz, S. Chaperones in control of protein disaggregation. EMBO J. 27, 328-335 (2008).
4. Sanchez, Y. & Lindquist, S.L. HSP104 required for induced thermotolerance. Science 248, 1112-1115 (1990).
5. Squires, C.L., Pedersen, S., Ross, B.M. & Squires, C. ClpB is the Escherichia coli heat shock protein F84. J. Bacteriol. 173, 4254-4262 (1991).
6. Queitsch, C., Hong, S.W., Vierling, E. & Lindquist, S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12, 479-492 (2000).
7. Hong, S.W. & Vierling, E. Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc. Natl. Acad. Sci. USA 97, 4392-4397 (2000).
8. Parsell, D.A., Kowal, A.S., Singer, M.A. & Lindquist, S. Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478 (1994).
9. Glover, J.R. & Lindquist, S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82 (1998).
10. Goloubinoff, P., Mogk, A., Peres Ben Zvi, A., 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).
11. Zolkiewski, M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 274, 28083-28086 (1999).
12. Motohashi, K., Watanabe, Y., Yohda, M. & Yoshida, M. Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. USA 96, 7184-7189 (1999).
13. Krzewska, J., Langer, T. & Liberek, K. Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 489, 92-96 (2001).
14. Weibezahn, J. et al. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119, 653-665 (2004).
15. Zietkiewicz, S., Krzewska, J. & Liberek, K. Successive and synergistic action of the Hsp70 and Hsp100 chaperones in protein disaggregation. J. Biol. Chem. 279, 44376-44383 (2004).
16. Winkler, J., Tyedmers, J., Bukau, B. & Mogk, A. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J. Cell Biol. 198, 387-404 (2012).
17. Acebrón, S.P., Martin, I., del Castillo, U., Moro, F. & Muga, A. DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett. 583, 2991-2996 (2009).
18. Lum, R., Tkach, J.M., Vierling, E. & Glover, J.R. Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J. Biol. Chem. 279, 29139-29146 (2004).
19. Schlieker, C. et al. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11, 607-615 (2004).
20. Lee, S. et al. The structure of ClpB. A molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240 (2003).
21. Mogk, A. et al. Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP-hydrolysis and chaperone activity. J. Biol. Chem. 278, 17615-17624 (2003).
22. Kedzierska, S., Akoev, V., Barnett, M.E. & Zolkiewski, M. Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry 42, 14242-14248 (2003).
23. Haslberger, T. et al. M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol. Cell 25, 247-260 (2007).
24. Schirmer, E.C., Homann, O.R., Kowal, A.S. & Lindquist, S. Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol. Biol. Cell 15, 2061-2072 (2004).
25. Miot, M. et al. Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc. Natl. Acad. Sci. USA 108, 6915-6920 (2011).
26. Sielaff, B. & Tsai, F.T. The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner. J. Mol. Biol. 402, 30-37 (2010).
27. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H. & Mogk, A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28, 315-325 (2009).
28. Pietrosiuk, A. et al. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 30010-30021 (2011).
29. Oguchi, Y. et al. A tightly regulated molecular toggle controls AAA+ disaggregase. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.2441 (18 November 2012).
30. Franzmann, T.M., Czekalla, A. & Walter, S.G. Regulatory circuits of the AAA+ disaggregase Hsp104. J. Biol. Chem. 286, 17992-18001 (2011).
31. Haslberger, T. et al. Protein disaggregation by the AAA+ chaperone ClpB involves partial threading of looped polypeptide segments. Nat. Struct. Mol. Biol. 15, 641-650 (2008).
32. Werbeck, N.D., Schlee, S. & Reinstein, J. Coupling and dynamics of subunits in the hexameric AAA+ chaperone ClpB. J. Mol. Biol. 378, 178-190 (2008).
33. del Castillo, U., Fernandez-Higuero, J.A., Perez-Acebron, S., Moro, F. & Muga, A. Nucleotide utilization requirements that render ClpB active as a chaperone. FEBS Lett. 584, 929-934 (2010).
34. Hoskins, J.R., Doyle, S.M. & Wickner, S. Coupling ATP utilization to protein remodeling by ClpB, a hexameric AAA+ protein. Proc. Natl. Acad. Sci. USA 22233-22238 (2009).
35. Laufen, T. et al. Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. USA 96, 5452-5457 (1999).
36. Winkler, J. et al. Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 29, 910-923 (2010).
37. Kumar, M. & Sourjik, V. Physical map and dynamics of the chaperone network in Escherichia coli. Mol. Microbiol. 84, 736-747 (2012).
38. Lee, S., Sielaff, B., Lee, J. & Tsai, F.T. CryoEM structure of Hsp104 and its mechanistic implication for protein disaggregation. Proc. Natl. Acad. Sci. USA 107, 8135-8140 (2010).
39. Sharma, S.K., De los Rios, P., Christen, P., Lustig, A. & Goloubinoff, P. The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat. Chem. Biol. 6, 914-920 (2010).
40. Konieczny, I. & Liberek, K. Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. J. Biol. Chem. 277, 18483-18488 (2002).
41. Doyle, S.M., Hoskins, J.R. & Wickner, S. Collaboration between the ClpB AAA+ remodeling protein and the DnaK chaperone system. Proc. Natl. Acad. Sci. USA 104, 11138-11144 (2007).
42. Tessarz, P., Mogk, A. & Bukau, B. Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol. Microbiol. 68, 87-97 (2008).
43. Andréasson, C., Fiaux, J., Rampelt, H., Druffel-Augustin, S. & Bukau, B. Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc. Natl. Acad. Sci. USA 105, 16519-16524 (2008).
44. Block, S.M., Segall, J.E. & Berg, H.C. Adaptation kinetics in bacterial chemotaxis. J. Bacteriol. 154, 312-323 (1983).
45. Kentner, D. & Sourjik, V. Dynamic map of protein interactions in the Escherichia coli chemotaxis pathway. Mol. Syst. Biol. 5, 238 (2009).