M Domains Couple the ClpB Threading Motor with the DnaK Chaperone Activity

Molecular Cell

Volumn 25, Issue 2, 2007, Pages 247-260

  Haslberger, Tobias ^a   Weibezahn, Jimena ^a   Zahn, Regina ^a   Lee, Sukyeong ^b   Tsai, Francis T F ^b   Bukau, Bernd ^a   Mogk, Axel ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

PROTEINS

Indexed keywords

CHAPERONE; MOLECULAR MOTOR; PROTEIN CLPB; PROTEIN DNAK;

ARTICLE; ENZYME DENATURATION; ENZYME SUBSTRATE; MOLECULAR INTERACTION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; THERMUS THERMOPHILUS;

EID: 33846231395     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.11.008     Document Type: Article

References (35)

1. Barnett M.E., Nagy M., Kedzierska S., and Zolkiewski M. The amino-terminal domain of ClpB supports binding to strongly aggregated proteins. J. Biol. Chem. 280 (2005) 34940-34945
2. Beinker P., Schlee S., Groemping Y., Seidel R., and Reinstein J. The N terminus of ClpB from Thermus thermophilus is not essential for the chaperone activity. J. Biol. Chem. 277 (2002) 47160-47166
3. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
4. Burton R.E., Baker T.A., and Sauer R.T. Nucleotide-dependent substrate recognition by the AAA+ HslUV protease. Nat. Struct. Mol. Biol. 12 (2005) 245-251
5. Chin J.W., Martin A.B., King D.S., Wang L., and Schultz P.G. Addition of a photocrosslinking amino acid to the genetic code of Escherichiacoli. Proc. Natl. Acad. Sci. USA 99 (2002) 11020-11024
6. Chow I.T., Barnett M.E., Zolkiewski M., and Baneyx F. The N-terminal domain of Escherichia coli ClpB enhances chaperone function. FEBS Lett. 579 (2005) 4242-4248
7. Clarke A.K., and Eriksson M.J. The truncated form of the bacterial heat shock protein ClpB/HSP100 contributes to development of thermotolerance in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 182 (2000) 7092-7096
8. Creighton T.E. Protein Function: A Practical Approach (1997), IRL Press, Oxford
9. Dougan D.A., Mogk A., Zeth K., Turgay K., and Bukau B. AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett. 529 (2002) 6-10
10. Dougan D.A., Reid B.G., Horwich A.L., and Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 9 (2002) 673-683
11. Glover J.R., and Lindquist S. Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins. Cell 94 (1998) 73-82
12. Hattendorf D.A., and Lindquist S.L. Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J. 21 (2002) 12-21
13. Kedzierska S., Akoev V., Barnett M.E., and Zolkiewski M. Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry 42 (2003) 14242-14248
14. Krzewska J., Langer T., and Liberek K. Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 489 (2001) 92-96
15. Lee S., Sowa M.E., Watanabe Y., Sigler P.B., Chiu W., Yoshida M., and Tsai F.T. The structure of ClpB. A molecular chaperone that rescues proteins from an aggregated state. Cell 115 (2003) 229-240
16. Lee U., Wie C., Escobar M., Williams B., Hong S.W., and Vierling E. Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell 17 (2005) 559-571
17. Lee S., Choi J.-M., and Tsai F.T.F. Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding. Mol. Cell 25 (2007) 261-271 this issue
18. Lum R., Tkach J.M., Vierling E., and Glover J.R. Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J. Biol. Chem. 279 (2004) 29139-29146
19. Maurizi M.R., and Xia D. Protein binding and disruption by Clp/Hsp100 chaperones. Structure 12 (2004) 175-183
20. Mogk A., Schlieker C., Friedrich K.L., Schönfeld H.-J., Vierling E., and Bukau B. Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J. Biol. Chem. 278 (2003) 31033-31042
21. Mogk A., Schlieker C., Strub C., Rist W., Weibezahn J., and Bukau B. Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP-hydrolysis and chaperone activity. J. Biol. Chem. 278 (2003) 15-24
22. Neuwald A.F., Aravind L., Spouge J.L., and Koonin E.V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9 (1999) 27-43
23. Sanchez Y., and Lindquist S.L. HSP104 required for induced thermotolerance. Science 248 (1990) 1112-1115
24. Sauer R.T., Bolon D.N., Burton B.M., Burton R.E., Flynn J.M., Grant R.A., Hersch G.L., Joshi S.A., Kenniston J.A., Levchenko I., et al. Sculpting the proteome with AAA+ proteases and disassembly machines. Cell 119 (2004) 9-18
25. Schirmer E.C., Homann O.R., Kowal A.S., and Lindquist S. Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol. Biol. Cell 15 (2004) 2061-2072
26. Schlee S., Groemping Y., Herde P., Seidel R., and Reinstein J. The chaperone function of ClpB from Thermus thermophilus depends on allosteric interactions of its two ATP-binding sites. J. Mol. Biol. 306 (2001) 889-899
27. Schlieker C., Weibezahn J., Patzelt H., Tessarz P., Strub C., Zeth K., Erbse A., Schneider-Mergener J., Chin J.W., Schultz P.G., et al. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11 (2004) 607-615
28. Shrake A., Fisher M.T., McFarland P.J., and Ginsburg A. Partial unfolding of dodecameric glutamine synthetase from Escherichia coli: temperature-induced, reversible transitions of two domains. Biochemistry 28 (1989) 6281-6294
29. Tomoyasu T., Mogk A., Langen H., Goloubinoff P., and Bukau B. Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol. Microbiol. 40 (2001) 397-413
30. Watanabe Y.H., Takano M., and Yoshida M. ATP binding to nucleotide binding domain (NBD)1 of the ClpB chaperone induces motion of the long coiled-coil, stabilizes the hexamer, and activates NBD2. J. Biol. Chem. 280 (2005) 24562-24567
31. Weibezahn J., Schlieker C., Bukau B., and Mogk A. Characterization of a trap mutant of the AAA+ chaperone ClpB. J. Biol. Chem. 278 (2003) 32608-32617
32. Weibezahn J., Tessarz P., Schlieker C., Zahn R., Maglica Z., Lee S., Zentgraf H., Weber-Ban E.U., Dougan D.A., Tsai F.T., et al. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119 (2004) 653-665
33. Weibezahn J., Schlieker C., Tessarz P., Mogk A., and Bukau B. Novel insights into the mechanism of chaperone-assisted protein disaggregation. Biol. Chem. 386 (2005) 739-744
34. Wojtyra U.A., Thibault G., Tuite A., and Houry W.A. The N-terminal zinc binding domain of ClpX is a dimerization domain that modulates the chaperone function. J. Biol. Chem. 278 (2003) 48981-48990
35. Zietkiewicz S., Lewandowska A., Stocki P., and Liberek K. Hsp70 chaperone machine remodels protein aggregates at the initial step of Hsp70-Hsp100-dependent disaggregation. J. Biol. Chem. 281 (2006) 7022-7029