The ClpB/Hsp104 molecular chaperone - A protein disaggregating machine

Journal of Structural Biology

Volumn 146, Issue 1-2, 2004, Pages 99-105

  Lee, Sukyeong ^a   Sowa, Mathew E ^a   Choi, Jae Mun ^a   Tsai, Francis T F ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

AAA+; ClpB; Hsp104; Molecular chaperone; Protein disaggregation

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 70; PROTEIN CLPB; PROTEIN DNAK;

ALPHA HELIX; CONFERENCE PAPER; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; PROTEIN CONFORMATION; PROTEIN RENATURATION;

EID: 1642361660     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2003.11.016     Document Type: Conference Paper

References (55)

1. Barnett M.E., Zolkiewska A., Zolkiewski M. Structure and activity of ClpB from Escherichia coli. Role of the amino- and carboxyl-terminal domains. J. Biol. Chem. 275:2000;37565-37571.
2. Beinker P., Schlee S., Groemping Y., Seidel R., 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. Beuron F., Maurizi M.R., Belnap D.M., Kocsis E., Booy F.P., Kessel M., Steven A.C. At sixes and sevens: characterization of the symmetry mismatch of the ClpAP chaperone-assisted protease. J. Struct. Biol. 123:1998;248-259.
4. Bochtler M., Hartmann C., Song H.K., Bourenkov G.P., Bartunik H.D., Huber R. The structures of HslU and the ATP-dependent protease HslU-HslV. Nature. 403:2000;800-805.
5. Cashikar A.G., Schirmer E.C., Hattendorf D.A., Glover J.R., Ramakrishnan M.S., Ware D.M., Lindquist S.L. Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol. Cell. 9:2002;751-760.
6. Clarke A.K., 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.
7. DeLaBarre B., Brünger A.T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat. Struct. Biol. 10:2003;856-863.
8. Diamant S., Ben-Zvi A.P., Bukau B., Goloubinoff P. Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery. J. Biol. Chem. 275:2000;21107-21113.
9. Dougan D.A., Mogk A., Bukau B. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell. Mol. Life Sci. 59:2002;1607-1616.
10. Dougan D.A., Mogk A., Zeth K., Turgay K., Bukau B. AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett. 529:2002;6-10.
11. Dougan D.A., Reid B.G., Horwich A.L., Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell. 9:2002;673-683.
12. Glover J.R., Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell. 94:1998;73-82.
13. 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. 96:1999;13732-13737.
14. Gottesman S., Wickner S., Maurizi M.R. Protein quality control: triage by chaperones and proteases. Genes Dev. 11:1997;815-823.
15. Grimaud R., Kessel M., Beuron F., Steven A.C., Maurizi M.R. Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem. 273:1998;12476-12481.
16. Guo F., Esser L., Singh S.K., Maurizi M.R., Xia D. Crystal structure of the heterodimeric complex of the adaptor, ClpS, with the N-domain of the AAA+ chaperone, ClpA. J. Biol. Chem. 277:2002;46753-46762.
17. Guo F., Maurizi M.R., Esser L., Xia D. Crystal structure of ClpA, an HSP100 chaperone and regulator of ClpAP protease. J. Biol. Chem. 277:2002;46743-46752.
18. Horwich A.L., Weber-Ban E.U., Finley D. Chaperone rings in protein folding and degradation. Proc. Natl. Acad. Sci. USA. 96:1999;11033-11040.
19. Ishikawa T., Beuron F., Kessel M., Wickner S., Maurizi M.R., Steven A.C. Translocation pathway of protein substrates in ClpAP protease. Proc. Natl. Acad. Sci. USA. 98:2001;4328-4333.
20. Kim, D.Y., Kim, K.K., 2003. Crystal structure of ClpX molecular chaperone from Helicobacter pylori. J. Biol. Chem. Sep 26 [Epub ahead of print].
21. Kim Y.-I., Levchenko I., Fraczkowska K., Woodruff R.V., Sauer R.T., Baker T.A. Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat. Struct. Biol. 8:2001;230-233.
22. Kim K.I., Cheong G.-W., Park S.-C., Ha J.-S., Woo K.M., Choi S.J., Chung C.H. Heptameric ring structure of the heat-shock protein ClpB, a protein-activated ATPase in Escherichia coli. J. Mol. Biol. 303:2000;655-666.
23. Lee S., Hisayoshi M., Makio H., Yoshida M., Tsai F.T.F. Crystallization and preliminary X-ray crystallographic analysis of the Hsp100 chaperone ClpB from Thermus thermophilus. Acta Crystallogr. D. 59:2003;2334-2336.
24. Lee S., Sowa M.E., Watanabe Y., Sigler P.B., Chiu W., Yoshida M., Tsai F.T.F. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell. 115:2003;229-240.
25. Lenzen C.U., Steinmann D., Whiteheart S.W., Weis W.I. Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein. Cell. 94:1998;525-536.
26. Li J., Sha B. Crystal structure of E. coli Hsp100 ClpB nucleotide-binding domain 1 (NBD1) and mechanistic studies on ClpB ATPase activity. J. Mol. Biol. 318:2002;1127-1137.
27. Li J., Sha B. Crystal structure of the E. coli Hsp100 ClpB N-terminal domain. Structure. 11:2003;323-328.
28. Li D., Zhao R., Lilyestrom W., Gai D., Zhang R., DeCaprio J.A., Fanning E., Joachimiak A., Szakonyi G., Chen X.S. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature. 423:2003;512-518.
29. Matouschek A. Protein unfolding - an important process in vivo? Curr. Opin. Struct. Biol. 13:2003;98-109.
30. Mogk A., Schlieker C., Strub C., Rist W., Weibezahn J., 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;17615-17624.
31. Mogk A., Tomoyasu T., Goloubinoff P., Rüdiger S., Röder D., Langen H., Bukau B. Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18:1999;6934-6949.
32. 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. 96:1999;7184-7189.
33. Neuwald A.F., Aravind L., Spouge J.L., 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.
34. Ortega J., Singh S.K., Ishikawa T., Maurizi M.R., Steven A.C. Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell. 6:2000;1515-1521.
35. Park S.-K., Kim K.I., Woo K.M., Seol J.H., Tanaka K., Ichihara A., Ha D.B., Chung C.H. Site-directed mutagenesis of the dual translational initiation sites of the clpB gene of Escherichia coli and characterization of its gene products. J. Biol. Chem. 268:1993;20170-20174.
36. Parsell D.A., Kowal A.S., Lindquist S. Saccharomyces cerevisiae Hsp104 protein. J. Biol. Chem. 269:1994;4480-4487.
37. Parsell D.A., Kowal A.S., Singer M.A., Lindquist S. Protein disaggregation mediated by heat-shock protein Hsp104. Nature. 372:1994;475-478.
38. Queitsch C., Hong S.W., Vierling E., Lindquist S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell. 12:2000;479-492.
39. Sanchez Y., Lindquist S. Hsp104 required for induced thermotolerance. Science. 248:1990;1112-1115.
40. Sanchez Y., Taulien J., Borkovich K.A., Lindquist S. Hsp104 is required for tolerance to many forms of stress. EMBO J. 11:1992;2357-2364.
41. Schirmer E.C., Glover J.R., Singer M.A., Lindquist S. Hsp100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21:1996;289-296.
42. Schlee S., Groemping Y., Herde P., Seidel R., 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.
43. Schlothauer T., Mogk A., Dougan D.A., Bukau B., Turgay K. MecA, an adaptor protein necessary for ClpC chaperone activity. Proc. Natl. Acad. Sci. USA. 100:2003;2306-2311.
44. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D.B. Crystal and solution structure of an HslUV protease-chaperone complex. Cell. 103:2000;633-643.
45. Squires C.L., Pedersen S., Ross B.M., Squires C. ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 173:1991;4254-4262.
46. Wang J., Song J.J., Franklin M.C., Kamtekar S., Im Y.J., Rho S.H., Seong I.S., Lee C.S., Chung C.H., Eom S.H. Crystal structure of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure. 9:2001;177-184.
47. Watanabe Y.-H., Motohashi K., Yoshida M. Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J. Biol. Chem. 277:2002;5804-5809.
48. Weber-Ban E.U., Reid B.G., Miranker A.D., Horwich A.L. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature. 401:1999;90-93.
49. Wickner S., Maurizi M.R., Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science. 286:1999;1888-1893.
50. Woo K.M., Kim K.I., Goldberg A., Ha D.B., Chung C.H. The heat-shock protein ClpB in Escherichia coli is a protein-activated ATPase. J. Biol. Chem. 267:1992;20429-20434.
51. Yu R.C., Hanson P.I., Jahn R., Brünger A.T. Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP. Nat. Struct. Biol. 5:1998;803-811.
52. Zeth K., Ravelli R.B., Paal K., Cusack S., Bukau B., Dougan D.A. Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat. Struct. Biol. 9:2002;906-911.
53. Zhang X., Shaw A., Bates P.A., Newman R.H., Gowen B., Orlova E., Gorman M.A., Kondo H., Dokurno P., Lally J., Leonard G., Meyer H., van Heel M., Freemont P.S. Structure of the AAA ATPase p97. Mol. Cell. 6:2000;1473-1484.
54. Zolkiewski M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. J. Biol. Chem. 274:1999;28083-28086.
55. Zolkiewski M., Kessel M., Ginsburg A., Maurizi M.R. Nucleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci. 8:1999;1899-1903.