Principles of general and regulatory proteolysis by AAA+ proteases in Escherichia coli

Research in Microbiology

Volumn 160, Issue 9, 2009, Pages 629-636

  Schmidt, Ronny ^a   Bukau, Bernd ^a   Mogk, Axel ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

AAA protein; Clp Hsp100; N end rule; Protein quality control; Proteolysis

Indexed keywords

ADAPTOR PROTEIN; ATPASE ASSOCIATED WITH A VARIETY OF CELLULAR ACTIVITIES PROTEIN; CHAPERONE; ESCHERICHIA COLI PROTEIN; POLYPEPTIDE; PROTEIN DERIVATIVE; PROTEINASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL PROTECTION; CRYSTAL STRUCTURE; CYTOSOL; DNA DAMAGE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEFECT; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN VARIANT; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATASES; BIOCATALYSIS; CARRIER PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; PEPTIDE HYDROLASES; PROTEIN STABILITY; PROTEINS; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 71749111749     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.08.018     Document Type: Article

References (50)

1. Abdelhakim A.H., Oakes E.C., Sauer R.T., and Baker T.A. Unique contacts direct high-priority recognition of the tetrameric Mu transposase-DNA complex by the AAA+ unfoldase ClpX. Mol. Cell 30 (2008) 39-50
2. Andersson F.I., Tryggvesson A., Sharon M., Diemand A.V., Classen M., Best C., et al. Structure and function of a novel type of ATP-dependent Clp protease. J. Biol. Chem. 284 (2009) 13519-13532
3. Bachmair A., Finley D., and Varshavsky A. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234 (1986) 179-186
4. Bougdour A., Cunning C., Baptiste P.J., Elliott T., and Gottesman S. Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol. Microbiol. 68 (2008) 298-313
5. Bougdour A., Wickner S., and Gottesman S. Modulating RssB activity: IraP, a novel regulator of sigma(S) stability in Escherichia coli. Genes Dev. 20 (2006) 884-897
6. 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
7. Erbse A., Schmidt R., Bornemann T., Schneider-Mergener J., Mogk A., Zahn R., et al. ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439 (2006) 753-756
8. Flynn J.M., Levchenko I., Sauer R.T., and Baker T.A. Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev. 18 (2004) 2292-2301
9. Flynn J.M., Levchenko I., Seidel M., Wickner S.H., Sauer R.T., and Baker T.A. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc. Natl. Acad. Sci. USA 98 (2001) 10584-10589
10. Flynn J.M., Neher S.B., Kim Y.I., Sauer R.T., and 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
11. Frottin F., Martinez A., Peynot P., Mitra S., Holz R.C., Giglione C., et al. The proteomics of N-terminal methionine cleavage. Mol. Cell. Proteomics 5 (2006) 2336-2349
12. Gonciarz-Swiatek M., Wawrzynow A., Um S.J., Learn B.A., McMacken R., Kelley W.L., et al. Recognition, targeting, and hydrolysis of the l O replication protein by the ClpP/ClpX protease. J. Biol. Chem. 274 (1999) 13999-14005
13. Gottesman S., Roche E., Zhou Y., and 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
14. Gur E., and Sauer R.T. Recognition of misfolded proteins by Lon, a AAA(+) protease. Genes Dev. 22 (2008) 2267-2277
15. Hou J.Y., Sauer R.T., and Baker T.A. Distinct structural elements of the adaptor ClpS are required for regulating degradation by ClpAP. Nat. Struct. Mol. Biol. 15 (2008) 288-294
16. 32 and abnormal proteins in Escherichia coli. J. Bacteriol. 179 (1997) 7219-7225
17. Keiler K.C., Waller P.R.H., and Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271 (1996) 990-993
18. Kirstein J., Hoffmann A., Lilie H., Schmidt R., Rübsamen-Waigmann H., Brötz-Oesterhelt H., et al. The antibiotic ADEP reprogrammes ClpP, switiching it from a regulated to an uncontrolled protease. EMBO Mol. Med. 1 (2009) 37-49
19. Kowit J.D., and Goldberg A.L. Intermediate steps in the degradation of a specific abnormal protein in Escherichia coli. J. Biol. Chem. 252 (1977) 8350-8357
20. Kuroda A., Nomura K., Ohtomo R., Kato J., Ikeda T., Takiguchi N., et al. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293 (2001) 705-708
21. Levchenko I., Grant R.A., Flynn J.M., Sauer R.T., and Baker T.A. Versatile modes of peptide recognition by the AAA+ adaptor protein SspB. Nat. Struct. Mol. Biol. 12 (2005) 520-525
22. Levchenko I., Grant R.A., Wah D.A., Sauer R.T., and 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
23. Levchenko I., Seidel M., Sauer R.T., and Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 289 (2000) 2354-2356
24. Lupas A.N., and Koretke K.K. Bioinformatic analysis of ClpS, a protein module involved in prokaryotic and eukaryotic protein degradation. J. Struct. Biol. 141 (2003) 77-83
25. Maglica Z., Striebel F., and Weber-Ban E. An intrinsic degradation tag on the ClpA C-terminus regulates the balance of ClpAP complexes with different substrate specificity. J. Mol. Biol. 384 (2008) 503-511
26. McGinness K.E., Baker T.A., and Sauer R.T. Engineering controllable protein degradation. Mol. Cell 22 (2006) 701-707
27. Mika F., and Hengge R. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes Dev. 19 (2005) 2770-2781
28. Mogk A., Schmidt R., and Bukau B. The N-end rule pathway for regulated proteolysis: prokaryotic and eukaryotic strategies. Trends Cell. Biol. 17 (2007) 165-172
29. Muffler A., Fischer D., Altuvia S., Storz G., and 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
30. Neher S.B., Flynn J.M., Sauer R.T., and Baker T.A. Latent ClpX-recognition signals ensure LexA destruction after DNA damage. Genes Dev. 17 (2003) 1084-1089
31. Neher S.B., Sauer R.T., and Baker T.A. Distinct peptide signals in the UmuD and UmuD′ subunits of UmuD/D′ mediate tethering and substrate processing by the ClpXP protease. Proc. Natl. Acad. Sci. USA 100 (2003) 13219-13224
32. Neher S.B., Villen J., Oakes E.C., Bakalarski C.E., Sauer R.T., Gygi S.P., et al. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol. Cell 22 (2006) 193-204
33. Ninnis R.L., Spall S.K., Talbo G.H., Truscott K.N., and Dougan D.A. Modification of PATase by L/F-transferase generates a ClpS-dependent N-end rule substrate in Escherichia coli. EMBO J. 28 (2009) 1732-1744
34. Peterson C.N., Ruiz N., and Silhavy T.J. RpoS proteolysis is regulated by a mechanism that does not require the SprE (RssB) response regulator phosphorylation site. J. Bacteriol. 186 (2004) 7403-7410
35. Pierechod M., Nowak A., Saari A., Purta E., Bujnicki J.M., and Konieczny I. Conformation of a plasmid replication initiator protein affects its proteolysis by ClpXP system. Protein Sci. 18 (2009) 637-649
36. Pratt L.A., and Silhavy T.J. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. USA 93 (1996) 2488-2492
37. Pruteanu M., Neher S.B., and Baker T.A. Ligand-controlled proteolysis of the Escherichia coli transcriptional regulator ZntR. J. Bacteriol. 189 (2007) 3017-3025
38. Rüdiger S., Germeroth L., Schneider-Mergener J., and Bukau B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16 (1997) 1501-1507
39. Sauer R.T., Bolon D.N., Burton B.M., Burton R.E., Flynn J.M., Grant R.A., et al. Sculpting the Proteome with AAA+ proteases and disassembly machines. Cell 119 (2004) 9-18
40. Schmidt R., Zahn R., Bukau B., and Mogk A. ClpS is the recognition component for Escherichia coli substrates of the N-end rule degradation pathway. Mol. Microbiol. 72 (2009) 506-517
41. Schuenemann V.J., Kralik S.M., Albrecht R., Spall S.K., Truscott K.N., Dougan D.A., et al. Structural basis of N-end rule substrate recognition in Escherichia coli by the ClpAP adaptor protein ClpS. EMBO Rep. 10 (2009) 508-514
42. Song H.K., and 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
43. Tobias J.W., Shrader T.E., Rocap G., and Varshavsky A. The N-end rule in bacteria. Science 254 (1991) 1374-1377
44. 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
45. Wang J., Hartling J.A., and Flanagan J.M. The Structure of ClpP at 2.3 Å Resolution Suggests a Model for ATP-Dependent Proteolysis. Cell 91 (1997) 447-456
46. Wang K.H., Oakes E.S., Sauer R.T., and Baker T.A. Tuning the strength of a bacterial N-end rule degradation signal. J. Biol. Chem (2008)
47. Wang K.H., Roman-Hernandez G., Grant R.A., Sauer R.T., and Baker T.A. The molecular basis of N-end rule recognition. Mol. Cell 32 (2008) 406-414
48. Zeth K., Ravelli R.B., Paal K., Cusack S., Bukau B., and 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
49. Zhou Y., Gottesman S., Hoskins J.R., Maurizi M.R., and Wickner S. The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev. 15 (2001) 627-637
50. Zylicz M., Liberek K., Wawrzynow A., and Georgopoulos C. Formation of the preprimosome protects lambda O from RNA transcription-dependent proteolysis by ClpP/ClpX. Proc. Natl. Acad. Sci. USA 95 (1998) 15259-15263