Broad yet high substrate specificity: The challenge of AAA+ proteins

Journal of Structural Biology

Volumn 146, Issue 1-2, 2004, Pages 90-98

  Mogk, Axel ^a   Dougan, David ^a   Weibezahn, Jimena ^a   Schlieker, Christian ^a   Turgay, Kursad ^a   Bukau, Bernd ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

AAA+ superfamily; Adaptor protein; Chaperone; Protease; Substrate specificity

Indexed keywords

ADAPTOR PROTEIN;

CONFERENCE PAPER; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ENZYME ACTIVATION; NUCLEOSIDE-TRIPHOSPHATASE; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 1642363290     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2003.10.009     Document Type: Conference Paper

References (67)

1. Ault-Rich D., Fraley C.D., Tzeng C.M., Kornberg A. Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180:1998;1841-1847.
2. Banecki B., Wawrzynow A., Puzewicz J., Georgopoulos C., Zylicz M. Structure-function analysis of the zinc-binding region of the ClpX molecular chaperone. J. Biol. Chem. 276:2001;18843-18848.
3. Barnett M.E., Zolkiewski M. Site-Directed mutagenesis of conserved charged amino acid residues in ClpB from Escherichia coli. Biochemistry. 41:2002;11277-11283.
4. 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.
5. 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.
6. Beyer A. Sequence analysis of the AAA protein family. Protein Sci. 6:1997;2043-2058.
7. 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.
8. 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.
9. 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.
10. 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.
11. Dougan D.A., Weber-Ban E.U., Bukau B. Targeted Delivery of an ssrA-tagged substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol. Cell. 12:2003;373-380.
12. Ebel W., Skinner M.M., Dierksen K.P., Scott J.M., Trempy J.E. A conserved domain in Escherichia coli Lon protease is involved in substrate discriminator activity. J. Bacteriol. 181:1999;2236-2243.
13. 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.
14. 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.
15. Glover J.R., Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell. 94:1998;73-82.
16. 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. 96:1999;13732-13737.
17. ′ stability EMBO J. 19:2000;5251-5258.
18. Gottesman S., Roche E., Zhou Y., Sauer R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12:1998;1338-1347.
19. Gottesman S., Wickner S., Maurizi M.R. Protein quality control: triage by chaperones and proteases. Genes Dev. 11:1997;815-823.
20. 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.
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.
22. Jenal U., Hengge-Aronis R. Regulation by proteolysis in bacterial cells. Curr. Opin. Microbiol. 6:2003;163-172.
23. Keiler K.C., Waller P.R.H., Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science. 271:1996;990-993.
24. Kuroda A., Kornberg A. polyphosphate kinase as a nucleoside diphosphate kinase in Escherichia coli and Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA. 94:1997;439-442.
25. Kuroda A., Nomura K., Ohtomo R., Kato J., Ikeda T., Takiguchi N., Ohtake H., Kornberg A. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science. 293:2001;705-708.
26. Kwon A.R., Kessler B.M., Overkleeft H.S., McKay D.B. Structure and reactivity of an asymmetric complex between HslV and I-domain deleted HslU, a prokaryotic homolog of the eukaryotic proteasome. J. Mol. Biol. 330:2003;185-195.
27. Kwon Y.T., Reiss Y., Fried V.A., Hershko A., Yoon J.K., Gonda D.K., Sangan P., Copeland N.G., Jenkins N.A., Varshavsky A. The mouse and human genes encoding the recognition component of the N-end rule pathway. Proc. Natl. Acad. Sci. USA. 95:1998;7898-7903.
28. 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.
29. Leonhard K., Stiegler A., Neupert W., Langer T. Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature. 398:1999;348-351.
30. Levchenko I., Grant R.A., Wah D.A., Sauer R.T., Baker T.A. Structure of a delivery protein for an AAA+ protease in complex with a peptide degradation tag. Mol. Cell. 12:2003;365-372.
31. Levchenko I., Seidel M., Sauer R.T., Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science. 289:2000;2354-2356.
32. Li J., Sha B. Crystal structure of E. coli Hsp100 ClpB nucleotide-binding domain 1 (NBD1) and mechanistic studies onClpB ATPase activity. J. Mol. Biol. 318:2002;1127-1137.
33. Lo J.H., Baker T.A., Sauer R.T. Characterization of the N-terminal repeat domain of Escherichia coli ClpA-A class I Clp/HSP100 ATPase. Protein Sci. 10:2001;551-559.
34. Lupas A.N., Koretke K.K. Bioinformatic analysis of ClpS, a protein module involved in prokaryotic and eukaryotic protein degradation. J. Struct. Biol. 141:2003;77-83.
35. 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;15-24.
36. Mogk A., Tomoyasu T., Goloubinoff P., Rüdiger S., Röder D., Langen H., Bukau B. Identification of thermolabile E. coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18:1999;6934-6949.
37. Muffler A., Fischer D., Altuvia S., Storz G., Hengge-Aronis R. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J. 15:1996;1333-1339.
38. 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.
39. 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.
40. 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.
41. Persuh M., Mandic-Mulec I., Dubnau D. A MecA paralog, YpbH, binds ClpC, affecting both competence and sporulation. J. Bacteriol. 184:2002;2310-2313.
42. Persuh M., Turgay K., Mandic-Mulec I., Dubnau D. The N and the C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol. Microbiol. 33:1999;886-894.
43. Pratt L.A., Silhavy T.J. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. USA. 93:1996;2488-2492.
44. Roudiak S.G., Shrader T.E. Functional role of the N-terminal region of the Lon protease from Mycobacterium smegmatis. Biochemistry. 37:1998;11255-11263.
45. 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.
46. 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.
47. 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.
48. Smith C.K., Baker T.A., Sauer R.T. Lon and Clp family proteases and chaperones share homologous substrate-recognition domains. Proc. Natl. Acad. Sci. USA. 96:1999;6678-6682.
49. Song H.K., Eck M.J. Structural basis of degradation signal recognition SspB, a specificity-enhancing factor for the ClpXP proteolytic machine. Mol. Cell. 12:2003;75-86.
50. Song H.K., Hartmann C., Ramachandran R., Bochtler M., Behrendt R., Moroder L., Huber R. Mutational studies on HslU and its docking mode with HslV. Proc. Natl. Acad. Sci. USA. 97:2000;14103-14108.
51. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D.B. Crystal and solution structures of an HslUV protease-chaperone complex. Cell. 103:2000;633-643.
52. Studemann A., Noirclerc-Savoye M., Klauck E., Becker G., Schneider D., Hengge R. Sequential recognition of two distinct sites in sigma (S) by the proteolytic targeting factor RssB and ClpX. EMBO J. 22:2003;4111-4120.
53. ′ (2)C is an error-prone DNA polymerase, Escherichia coli pol V Proc. Natl. Acad. Sci. USA. 96:1999;8919-8924.
54. Tek V., Zolkiewski M. Stability and interactions of the amino-terminal domain of ClpB from Escherichia coli. Protein Sci. 11:2002;1192-1198.
55. Tobias J.W., Shrader T.E., Rocap G., Varshavsky A. The N-end rule in bacteria. Science. 254:1991;1374-1377.
56. Tomoyasu T., Mogk A., Langen H., Goloubinoff P., 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.
57. Turgay K., Hamoen L.W., Venema G., Dubnau D. Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev. 11:1997;119-128.
58. Wah D.A., Levchenko I., Baker T.A., Sauer R.T. Characterization of a Specificity Factor for an AAA+ ATPase. Assembly of SspB Dimers with ssrA-Tagged Proteins and the ClpX Hexamer. Chem. Biol. 9:2002;1237-1245.
59. Wah D.A., Levchenko I., Rieckhof G.E., Bolon D.N., Baker T.A., Sauer R.T. Flexible linkers leash the substrate binding domain of SspB to a peptide module that stabilizes delivery complexes with the AAA+ ClpXP protease. Mol. Cell. 12:2003;355-363.
60. Wang J., Hartling J.A., Flanagan J.M. The structure of ClpP at 2.3. Å resolution suggests a model for ATP-dependent proteolysis Cell. 91:1997;447-456.
61. Weibezahn J., Schlieker C., Bukau B., Mogk A. Characterization of a trap mutant of the AAA+ chaperone ClpB. J. Biol. Chem. 278:2003;32608-32617.
62. Wojtyra, U.A., Thibault, G., Tuite, A., Houry, W.A., 2003. The N-terminal Zinc binding domain of ClpX is a dimerization domain that modulates the chaperone function. J. Biol. Chem. (in press)
63. 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.
64. Yuan X., Shaw A., Zhang X., Kondo H., Lally J., Freemont P.S., Matthews S. Solution structure and interaction surface of the C-terminal domain from p47: a major p97-cofactor involved in SNARE disassembly. J. Mol. Biol. 311:2001;255-263.
65. 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.
66. 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.
67. 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.