Analysis of the cooperative ATPase cycle of the AAA+ chaperone ClpB from thermus thermophilus by using ordered heterohexamers with an alternating subunit arrangement

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9789-9800

  Yamasaki, Takashi ^a   Oohata, Yukiko ^a   Nakamura, Toshiki ^a   Watanabe, Yo Hei ^a  

^a KONAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

ATP HYDROLYSIS; ATPASE-ACTIVE FORMS; DISAGGREGATION; MECHANICAL POWER; NUCLEOTIDE BINDING; PROTEIN AGGREGATES; PROTEIN DISAGGREGATION; THERMUS THERMOPHILUS;

HYDROLYSIS;

ADENOSINE TRIPHOSPHATASE; CHAPERONE; CHAPERONE CLPB; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DISULFIDE; HEAT SHOCK PROTEIN; PROTEIN AGGREGATE; PROTEIN BINDING; PROTEIN SUBUNIT;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; HYDROLYSIS; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; OLIGOMERIZATION; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; THERMUS THERMOPHILUS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEAT; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE;

THERMUS THERMOPHILUS;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BINDING SITES; DISULFIDES; HEAT-SHOCK PROTEINS; HOT TEMPERATURE; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTATION; PROTEIN AGGREGATES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; THERMUS THERMOPHILUS;

EID: 84927144987     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.617696     Document Type: Article

References (45)

1. Thomas, J. G., and Baneyx, F. (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J. Bacteriol. 180, 5165-5172
2. Sanchez, Y., and Lindquist, S. L. (1990) HSP104 required for induced thermotolerance. Science 248, 1112-1115
3. Parsell, D. A., Kowal, A. S., Singer, M. A., and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478
4. Glover, J. R., and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82
5. Motohashi, K., Watanabe, Y., Yohda, M., and Yoshida, M. (1999) Heatinactivated proteins are rescued by the DnaK: J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. U.S.A. 96, 7184-7189
6. Goloubinoff, P., Mogk, A., Zvi, A. P., Tomoyasu, T., and Bukau, B. (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. U.S.A. 96, 13732-13737
7. Zolkiewski, M. (1999) 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
8. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rüdiger, S., Röder, D., Langen, H., and Bukau, B. (1999) Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18, 6934-6949
9. Krzewska, J., Langer, T., and Liberek, K. (2001) Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 489, 92-96
10. Schirmer, E. C., Glover, J. R., Singer, M. A., and Lindquist, S. (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21, 289-296
11. Neuwald, A. F., Aravind, L., Spouge, J. L., and Koonin, E. V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43
12. Ogura, T., and Wilkinson, A. J. (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6, 575-597
13. Snider, J., and Houry, W. A. (2008) AAA+ proteins: diversity in function, similarity in structure. Biochem. Soc. Trans. 36, 72-77
14. Lee, S., Sowa, M. E., Watanabe, Y. H., Sigler, P. B., Chiu, W., Yoshida, M., and Tsai, F. T. (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115, 229-240
15. Mogk, A., Schlieker, C., Strub, C., Rist, W., Weibezahn, J., and Bukau, B. (2003) 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
16. Parsell, D. A., Kowal, A. S., and Lindquist, S. (1994) Saccharomyces cerevisiae Hsp104 protein: purification and characterization of ATP-induced structural changes. J. Biol. Chem. 269, 4480-4487
17. Zolkiewski, M., Kessel, M., Ginsburg, A., and Maurizi, M. R. (1999) Nu-cleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci. 8, 1899-1903
18. Schlee, S., Groemping, Y., Herde, P., Seidel, R., and Reinstein, J. (2001) The chaperone function of ClpB from Thermus thermophilus depends on allosteric interactions of its two ATP-binding sites. J. Mol. Biol. 306, 889-899
19. Krzewska, J., Konopa, G., and Liberek, K. (2001) Importance of two ATPbinding sites for oligomerization, ATPase activity and chaperone function of mitochondrial Hsp78 protein. J. Mol. Biol. 314, 901-910
20. Watanabe, Y. H., Motohashi, K., and Yoshida, M. (2002) Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J. Biol. Chem. 277, 5804-5809
21. Akoev, V., Gogol, E. P., Barnett, M. E., and Zolkiewski, M. (2004) Nucle-otide-induced switch in oligomerization of the AAA+ ATPase ClpB. Protein Sci. 13, 567-574
22. Hattendorf, D. A., and Lindquist, S. L. (2002) Analysis of theAAAsensor-2 motif in the C-terminal ATPase domain of Hsp104 with a site-specific fluorescent probe of nucleotide binding. Proc. Natl. Acad. Sci. U.S.A. 99, 2732-2737
23. Hattendorf, D. A., and Lindquist, S. L. (2002) Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J. 21, 12-21
24. Werbeck, N. D., Schlee, S., and Reinstein, J. (2008) Coupling and dynamics of subunits in the hexameric AAA+ chaperone ClpB. J. Mol. Biol. 378, 178-190
25. Hoskins, J. R., Doyle, S. M., and Wickner, S. (2009) Coupling ATP utilization to protein remodeling by ClpB, a hexameric AAA+ protein. Proc. Natl. Acad. Sci. U.S.A. 106, 22233-22238
26. del Castillo, U., Fernández-Higuero, J. A., Pérez-Acebrón, S., Moro, F., and Muga, A. (2010) Nucleotide utilization requirements that render ClpB active as a chaperone. FEBS Lett. 584, 929-934
27. Fernández-Higuero, J. A., Acebrón, S. P., Taneva, S. G., Del Castillo, U., Moro, F., and Muga, A. (2011) Allosteric communication between the nucleotide binding domains of caseinolytic peptidase B. J. Biol. Chem. 286, 25547-25555
28. Franzmann, T. M., Czekalla, A., and Walter, S. G. (2011) Regulatory circuits of the AAA+ disaggregase Hsp104. J. Biol. Chem. 286, 17992-18001
29. DeSantis, M. E., Leung, E. H., Sweeny, E. A., Jackrel, M. E., Cushman-Nick, M., Neuhaus-Follini, A., Vashist, S., Sochor, M. A., Knight, M. N., and Shorter, J. (2012) Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151, 778-793
30. Higuchi, R., Krummel, B., and Saiki, R. K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367
31. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77, 51-59
32. Mizuno, S., Nakazaki, Y., Yoshida, M., and Watanabe, Y. H. (2012) Orientation of the amino-terminal domain of ClpB affects the disaggregation of the protein. FEBS J. 279, 1474-1484
33. Watanabe, Y. H., Takano, M., and Yoshida, M. (2005) 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, 24562-24567
34. Motohashi, K., Yohda, M., Endo, I., and Yoshida, M. (1996) A novel factor required for the assembly of the DnaK and DnaJ chaperones of Thermus thermophilus. J. Biol. Chem. 271, 17343-17348
35. + is an indispensable cofactor for GrpE stimulation of ATPase activity of DnaK x DnaJ complex from Thermus thermophilus. FEBS Lett. 412, 633-636
36. Watanabe, Y. H., and Yoshida, M. (2004) Trigonal DnaK-DnaJ complex versus free DnaK and DnaJ: heat stress converts the former to the latter, and only the latter can do disaggregation in cooperation with ClpB. J. Biol. Chem. 279, 15723-15727
37. Mizutani, T., Nemoto, S., Yoshida, M., and Watanabe, Y. H. (2009) Tem-perature-dependent regulation of Thermus thermophilus DnaK/DnaJ chaperones by DafA protein. Genes Cells 14, 1405-1413
38. Watanabe, Y. H., Nakazaki, Y., Suno, R., and Yoshida, M. (2009) Stability of the two wings of the coiled-coil domain of ClpB chaperone is critical for its disaggregation activity. Biochem. J. 421, 71-77
39. Bochtler, M., Hartmann, C., Song, H. K., Bourenkov, G. P., Bartunik, H. D., and Huber, R. (2000) The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 403, 800-805
40. Wang, F., Mei, Z., Qi, Y., Yan, C., Hu, Q., Wang, J., and Shi, Y. (2011) chine. Nature 471, 331-335
41. Glynn, S. E., Nager, A. R., Baker, T. A., and Sauer, R. T. (2012) Dynamic and static components power unfolding in topologically closed rings of a AAA+ proteolytic machine. Nat. Struct. Mol. Biol. 19, 616-622
42. Yamasaki, T., Nakazaki, Y., Yoshida, M., and Watanabe, Y. H. (2011) Roles of conserved arginines in ATP-binding domains of AAA+ chaperone ClpB from Thermus thermophilus. FEBS J. 278, 2395-2403
43. Biter, A. B., Lee, S., Sung, N., and Tsai, F. T. (2012) Structural basis for intersubunit signaling in a protein disaggregating machine. Proc. Natl. Acad. Sci. U.S.A. 109, 12515-12520
44. Ogura, T., Whiteheart, S. W., and Wilkinson, A. J. (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and intersubunit interactions in AAA and AAA+ ATPases. J. Struct. Biol. 146, 106-112
45. Carroni, M., Kummer, E., Oguchi, Y., Wendler, P., Clare, D. K., Sinning, I., Kopp, J., Mogk, A., Bukau, B., and Saibil, H. R. (2014) Head-to-tail interactions of the coiled-coil domains regulate ClpB activity and cooperation with Hsp70 in protein disaggregation. eLife 3, e02481