Protein Binding and Disruption by Clp/Hsp100 Chaperones

Structure

Volumn 12, Issue 2, 2004, Pages 175-183

  Maurizi, Michael R ^a   Xia, Di ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; ENDOPEPTIDASE CLP; HEAT SHOCK PROTEIN 100;

ANALYTIC METHOD; COMPLEX FORMATION; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE MUTATION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

EID: 1242283848     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2004.01.021     Document Type: Review

References (81)

1. Barnett M.E., Zolkiewski M. Site-directed mutagenesis of conserved charged amino acid residues in ClpB from Escherichia coli. Biochemistry. 41:2002;11277-11283.
2. Ben-Zvi A.P., Goloubinoff P. Review. mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones J. Struct. Biol. 135:2001;84-93.
3. Beuron F., Maurizi M.R., Belnap D.M., Kocsis E., Booy F.P., Kessel M. 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 HsIU and the ATP-dependent protease HsIU-HsIV. Nature. 403:2000;800-805.
5. + a domain of E. coli Lon protease at 1.9 Å resolution. J. Struct. Biol. 146:2004;. in press.
6. 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.
7. DeLaBarre B., Brunger A.T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat. Struct. Biol. 10:2003;856-863.
8. Donaldson L.W., Wojtyra U., Houry W.A. Solution structure of the dimeric zinc binding domain of the chaperone ClpX. J. Biol. Chem. 278:2003;48991-48996.
9. 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.
10. Flynn J.M., Levchenko I., Seidel M., Wickner S.H., Sauer R.T., Baker T.A. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc. Natl. Acad. Sci. USA. 98:2001;10584-10589.
11. Flynn J.M., Neher S.B., Kim Y.I., Sauer R.T., Baker T.A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell. 11:2003;671-683.
12. Gallie D.R., Fortner D., Peng J., Puthoff D. ATP-dependent hexameric assembly of the heat shock protein Hsp101 involves multiple interaction domains and a functional C-proximal nucleotide-binding domain. J. Biol. Chem. 277:2002;39617-39626.
13. Glover J.R., Lindquist S. Hsp104, Hsp70, and Hsp40. a novel chaperone system that rescues previously aggregated proteins Cell. 94:1998;73-82.
14. Glover J.R., Tkach J.M. Crowbars and ratchets. hsp100 chaperones as tools in reversing protein aggregation Biochem. Cell Biol. 79:2001;557-568.
15. Gonciarz-Swiatek M., Wawrzynow A., Um S.J., Learn B.A., McMacken R., Kelley W.L., Georgopoulos C., Sliekers O., Zylicz M. Recognition, targeting, and hydrolysis of the lambda O replication protein by the ClpP/ClpX protease. J. Biol. Chem. 274:1999;13999-14005.
16. Gottesman S. Proteolysis in bacterial regulatory circuits. Annu. Rev. Cell Dev. Biol. 19:2003;565-587.
17. Gottesman S., Wickner S., Maurizi M.R. Protein quality control. triage by chaperones and proteases Genes Dev. 11:1997;815-823.
18. 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.
19. Grishin N.V. Treble clef finger - a functionally diverse zinc-binding structural motif. Nucleic Acids Res. 29:2001;1703-1714.
20. + chaperone, ClpA. J. Biol. Chem. 277:2002;46753-46762. a.
21. 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. b.
22. Hattendorf D.A., 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.
23. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the sigma (S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:2002;373-395.
24. 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.
25. Hoskins J.R., Kim S.Y., Wickner S. Substrate recognition by the ClpA chaperone component of ClpAP protease. J. Biol. Chem. 275:2000;35361-35367.
26. Ishii Y., Sonezaki S., Iwasaki Y., Miyata Y., Akita K., Kato Y., Amano F. Regulatory role of C-terminal residues of SulA in its degradation by Lon protease in Escherichia coli. J. Biochem. (Tokyo). 127:2000;837-844.
27. Ishikawa T., Maurizi M.R., Steven A.C. The N-terminal substrate-binding domain of ClpA unfoldase is highly mobile and extends axially from the distal surface of ClpAP protease. J. Struct. Biol. 146:2004;. in press.
28. Jeruzalmi D., O'Donnell M., Kuriyan J. Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III. Cell. 106:2001;429-441.
29. Joshi S.A., Baker T.A., Sauer R.T. C-terminal domain mutations in ClpX uncouple substrate binding from an engagement step required for unfolding. Mol. Microbiol. 48:2003;67-76.
30. Kang S.G., Ortega J., Singh S.K., Wang N., Huang N.N., Steven A.C., Maurizi M.R. Functional proteolytic complexes of the human mitochondrial ATP-dependent protease, hClpXP. J. Biol. Chem. 277:2002;21095-21102.
31. Karzai A.W., Roche E.D., Sauer R.T. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat. Struct. Biol. 7:2000;449-455.
32. Kim D.Y., Kim K.K. Crystal structure of ClpX molecular chaperone from Helicobacter pylori. J. Biol. Chem. 278:2003;50664-50670.
33. 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. a.
34. Kim Y.I., Burton R.E., Burton B.M., Sauer R.T., Baker T.A. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell. 5:2000;639-648. b.
35. Kobiler O., Koby S., Teff D., Court D., Oppenheim A.B. The phage lambda CII transcriptional activator carries a C-terminal domain signaling for rapid proteolysis. Proc. Natl. Acad. Sci. USA. 99:2002;14964-14969.
36. Krzewska J., Konopa G., Liberek K. Importance of two ATP-binding sites for oligomerization, ATPase activity and chaperone function of mitochondrial Hsp78 protein. J. Mol. Biol. 314:2001;901-910. a.
37. 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. 489:2001;92-96. b.
38. Krzywda S., Brzozowski A.M., Verma C., Karata K., Ogura T., Wilkinson A.J. The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 Å resolution. Structure. 10:2002;1073-1083.
39. Kwon A.R., Trame C.B., McKay D.B. Kinetics of substrate degradation by HslUV. J. Struct. Biol. 146:2004;. in press.
40. Lee S., Sowa M.E., Watanabe Y.H., Sigler P.B., Chiu W., Yoshida M., Tsai F.T. The structure of ClpB. a molecular chaperone that rescues proteins from an aggregated state Cell. 115:2003;229-240.
41. 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.
42. + protease in complex with a peptide degradation tag. Mol. Cell. 12:2003;365-372.
43. Levchenko I., Smith C.K., Walsh N.P., Sauer R.T., Baker T.A. PDZ-like domains mediate binding specificity in the Clp/Hsp100 family of chaperones and protease regulatory subunits. Cell. 91:1997;939-947.
44. Li J., Sha B. Crystal structure of the E. coli Hsp100 ClpB N-terminal domain. Structure. 11:2003;323-328.
45. Little J.W. Autodigestion of LexA and phage lambda repressors. Proc. Natl. Acad. Sci. USA. 81:1984;1375-1379.
46. Lupas A.N., Martin J. AAA proteins. Curr. Opin. Struct. Biol. 12:2002;746-753.
47. + chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J. Biol. Chem. 278:2003;17615-17624.
48. Mogk A., Tomoyasu T., Goloubinoff P., Rudiger S., Roder 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.
49. Neher S.B., Flynn J.M., Sauer R.T., Baker T.A. Latent ClpX-recognition signals ensure LexA destruction after DNA damage. Genes Dev. 17:2003;1084-1089.
50. +. a class of chaperone-like atpases associated with the assembly, operation, and disassembly of protein complexes Genome Res. 9:1999;27-43.
51. Nieto-Sotelo J., Kannan K.B., Martinez L.M., Segal C. Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene. 230:1999;187-195.
52. Niwa H., Tsuchiya D., Makyio H., Yoshida M., Morikawa K. Hexameric ring structure of the ATPase domain of the membrane-integrated metalloprotease FtsH from Thermus thermophilus HB8. Structure. 10:2002;1415-1423.
53. + superfamily ATPases. common structure, diverse activities Genes Cells. 6:2001;575-597.
54. 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.
55. Pak M., Hoskins J.R., Singh S.K., Maurizi M.R., Wickner S. Concurrent chaperone and protease activities of ClpAP and the requirement for the N-terminal ClpA ATP binding site for chaperone activity. J. Biol. Chem. 274:1999;19316-19322.
56. 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.
57. Porankiewicz J., Wang J., Clarke A.K. New insights into the ATP-dependent Clp protease. Escherichia coli and beyond Mol. Microbiol. 32:1999;449-458.
58. Pratt L.A., Silhavy T.J. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. USA. 93:1996;2488-2492.
59. Rohrwild M., Pfeifer G., Santarius U., Muller S.A., Huang H.C., Engel A., Baumeister W., Goldberg A.L. The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome. Nat. Struct. Biol. 4:1997;133-139.
60. 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.
61. Schirmer E.C., Ware D.M., Queitsch C., Kowal A.S., Lindquist S.L. Subunit interactions influence the biochemical and biological properties of Hsp104. Proc. Natl. Acad. Sci. USA. 98:2001;914-919.
62. +]-ched about Trends Cell Biol. 10:2000;98-105.
63. Singh S.K., Maurizi M.R. Mutational analysis demonstrates different functional roles for the two ATP-binding sites in ClpAP protease from Escherichia coli. J. Biol. Chem. 269:1994;29537-29545.
64. Singh S.K., Grimaud R., Hoskins J.R., Wickner S., Maurizi M.R. Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. Proc. Natl. Acad. Sci. USA. 97:2000;8898-8903.
65. Singh S.K., Rozycki J., Ortega J., Ishikawa T., Lo J., Steven A.C., Maurizi M.R. Functional domains of the ClpA and ClpX molecular chaperones identified by limited proteolysis and deletion analysis. J. Biol. Chem. 276:2001;29420-29429.
66. Song H.K., Eck M.J. Structural basis of degradation signal recognition by SspB, a specificity-enhancing factor for the ClpXP proteolytic machine. Mol. Cell. 12:2003;75-86.
67. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D. Crystal and solution structures of an HslUV protease-chaperone complex. Cell. 103:2000;633-643.
68. Strub C., Schlieker C., Bukau B., Mogk A. Poly-L-lysine enhances the protein disaggregation activity of ClpB. FEBS Lett. 553:2003;125-130.
69. 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. 100:2002;2306-2311.
70. Van Melderen L., Thi M.H., Lecchi P., Gottesman S., Couturier M., Maurizi M.R. ATP-dependent degradation of CcdA by Lon protease. Effects of secondary structure and heterologous subunit interactions. J. Biol. Chem. 271:1996;27730-27738.
71. + ATPase. Assembly of SspB dimers with ssrA-tagged proteins and the ClpX hexamer. Chem. Biol. 9:2002;1237-1245.
72. + ClpXP protease. Mol. Cell. 12:2003;355-363.
73. 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 structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure. 9:2001;177-184. a.
74. Wang J., Song J.J., Seong I.S., Franklin M.C., Kamtekar S., Eom S.H., Chung C.H. Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. Structure. 9:2001;1107-1116. b.
75. Xia D., Singh S.K., Esser L., Guo F., Maurizi M.R. Crystallographic investigation of peptide binding sites in the N-domain of the ClpA chaperone. J. Struct. Biol. 146:2004;. in press.
76. Yu R.C., Hanson P.I., Jahn R., Brunger A.T. Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP. Nat. Struct. Biol. 5:1998;803-811.
77. 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.
78. Zhang X., Shaw A., Bates P.A., Newman R.H., Gowen B., Orlova E., Gorman M.A., Kondo H., Dokurno P., Lally J.et al. Structure of the AAA ATPase p97. Mol. Cell. 6:2000;1473-1484.
79. Zhou Y., Gottesman S., Hoskins J.R., Maurizi M.R., Wickner S. The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev. 15:2001;627-637.
80. Zolkiewski M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 274:1999;28083-28086.
81. Zolkiewski M., Kessel M., Ginsburg A., Maurizi M.R. Nucleotide-dependent oligomerization of ClpB from Escherichia coli. Protein Sci. 8:1999;1899-1903.