Proteomic Profiling of ClpXP Substrates after DNA Damage Reveals Extensive Instability within SOS Regulon

Molecular Cell

Volumn 22, Issue 2, 2006, Pages 193-204

  Neher, Saskia B ^a   Villén, Judit ^b   Oakes, Elizabeth C ^a   Bakalarski, Corey E ^b   Sauer, Robert T ^a   Gygi, Steven P ^b   Baker, Tania A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

DNA; PROTEINS

Indexed keywords

ENDOPEPTIDASE CLPX;

AMINO ACID SEQUENCE; ARTICLE; DNA DAMAGE; DNA REPAIR; GENE CONTROL; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEOMICS; QUANTITATIVE ANALYSIS; REGULON; STRESS; SYNTHESIS; UNINDEXED SEQUENCE;

ADENOSINE TRIPHOSPHATASES; BLOTTING, WESTERN; DNA DAMAGE; ENZYME INHIBITORS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION PROFILING; HALF-LIFE; KINETICS; MASS SPECTROMETRY; NALIDIXIC ACID; PEPTIDE HYDROLASES; PROTEOMICS; REGULON; SOS RESPONSE (GENETICS); SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS);

EID: 33646021005     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.03.007     Document Type: Article

References (46)

1. Buchanan C.E., and Sowell M.O. Synthesis of penicillin-binding protein 6 by stationary-phase Escherichia coli. J. Bacteriol. 151 (1982) 491-494
2. Courcelle J., Khodursky A., Peter B., Brown P.O., and Hanawalt P.C. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158 (2001) 41-64
3. Datsenko K.A., and Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97 (2000) 6640-6645
4. Dougan D.A., Weber-Ban E., and 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
5. Drlica K., and Zhao X. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61 (1997) 377-392
6. Fernandez De Henestrosa A.R., Ogi T., Aoyagi S., Chafin D., Hayes J.J., Ohmori H., and Woodgate R. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol. Microbiol. 35 (2000) 1560-1572
7. Finch P.W., Chambers P., and Emmerson P.T. Identification of the Escherichia coli recN gene product as a major SOS protein. J. Bacteriol. 164 (1985) 653-658
8. 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
9. 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
10. 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
11. Frank E.G., Ennis D.G., Gonzalez M., Levine A.S., and Woodgate R. Regulation of SOS mutagenesis by proteolysis. Proc. Natl. Acad. Sci. USA 93 (1996) 10291-10296
12. Friedberg E.C., Walker G.C., Seide W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis. Second Edition (2006), ASM Press, Washington, D.C.
13. Gonzalez M., Rasulova F., Maurizi M.R., and Woodgate R. Subunit-specific degradation of the UmuD/D′ heterodimer by the ClpXP protease: the role of trans recognition in UmuD′ stability. EMBO J. 19 (2000) 5251-5258
14. Griffith K.L., Shah I.M., and Wolf Jr. R.E. Proteolytic degradation of Escherichia coli transcription activators SoxS and MarA as the mechanism for reversing the induction of the superoxide (SoxRS) and multiple antibiotic resistance (Mar) regulons. Mol. Microbiol. 51 (2004) 1801-1816
15. Hengge-Aronis R. Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr. Opin. Microbiol. 2 (1999) 148-152
16. Ishii Y., Sonezaki S., Iwasaki Y., Miyata Y., Akita K., Kato Y., and 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
17. Karzai A.W., Susskind M.M., and Sauer R.T. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 18 (1999) 3793-3799
18. Krogan N.J., Peng W.T., Cagney G., Robinson M.D., Haw R., Zhong G., Guo X., Zhang X., Canadien V., Richards D.P., et al. High-definition macromolecular composition of yeast RNA-processing complexes. Mol. Cell 13 (2004) 225-239
19. Lange R., and Hengge-Aronis R. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 8 (1994) 1600-1612
20. Layton J.C., and Foster P.L. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol. Microbiol. 50 (2003) 549-561
21. Little J.W. Variations in the in vivo stability of LexA repressor during the SOS regulatory cycle. In: Friedberg E.C., and Bridges B.A. (Eds). Cellular Responses to DNA Damage (1983), Alan Liss, New York 369-378
22. Lutkenhaus J. Dynamic proteins in bacteria. Curr. Opin. Microbiol. 5 (2002) 548-552
23. Martinez A., and Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179 (1997) 5188-5194
24. Mizusawa S., and Gottesman S. Protein degradation in Escherichia coli: the lon gene controls the stability of SulA protein. Proc. Natl. Acad. Sci. USA 80 (1983) 358-362
25. Mosteller R.D., Goldstein R.V., and Nishimoto K.R. Metabolism of individual proteins in exponentially growing Escherichia coli. J. Biol. Chem. 255 (1980) 2524-2532
26. S subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 178 (1996) 1607-1613
27. Nair S., and Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186 (2004) 4192-4198
28. 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
29. 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
30. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., and Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1 (2002) 376-386
31. Peng J., Elias J.E., Thoreen C.C., Licklider L.J., and Gygi S.P. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2 (2003) 43-50
32. Petersen C. Escherichia coli ribosomal protein L10 is rapidly degraded when synthesized in excess of ribosomal protein L7/L12. J. Bacteriol. 172 (1990) 431-436
33. Pine M.J. Steady-state measurement of the turnover of amino acid in the cellular proteins of growing Escherichia coli: existence of two kinetically distinct reactions. J. Bacteriol. 103 (1970) 207-215
34. Quillardet P., Rouffaud M.A., and Bouige P. DNA array analysis of gene expression in response to UV irradiation in Escherichia coli. Res. Microbiol. 154 (2003) 559-572
35. Rappsilber J., Ishihama Y., and Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75 (2003) 663-670
36. Sanchez H., and Alonso J.C. Bacillus subtilis RecN binds and protects 3′-single-stranded DNA extensions in the presence of ATP. Nucleic Acids Res. 33 (2005) 2343-2350
37. Sauer R.T., Bolon D.N., Burton B.M., Burton R.E., Flynn J.M., Grant R.A., Hersch G.L., Joshi S.A., Kenniston J.A., Levchenko I., et al. Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119 (2004) 9-18
38. S, by ClpXP protease. J. Bacteriol. 178 (1996) 470-476
39. Selinger D.W., Cheung K.J., Mei R., Johansson E.M., Richmond C.S., Blattner F.R., Lockhart D.J., and Church G.M. RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nat. Biotechnol. 18 (2000) 1262-1268
40. Stephani K., Weichart D., and Hengge R. Dynamic control of Dps protein levels by ClpXP and ClpAP proteases in Escherichia coli. Mol. Microbiol. 49 (2003) 1605-1614
41. Takeda K., and Yanagida M. Regulation of nuclear proteasome by Rhp6/Ubc2 through ubiquitination and destruction of the sensor and anchor Cut8. Cell 122 (2005) 393-405
42. Wang J., Hartling J.A., and Flanagan J.M. The structure of ClpP at 2.3 A resolution suggests a model for ATP- dependent proteolysis. Cell 91 (1997) 447-456
43. S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187 (2005) 1591-1603
44. Weichart D., Lange R., Henneberg N., and Hengge-Aronis R. Identification and characterization of stationary phase-inducible genes in Escherichia coli. Mol. Microbiol. 10 (1993) 407-420
45. Wu W.F., Zhou Y., and Gottesman S. Redundant in vivo proteolytic activities of Escherichia coli Lon and the ClpYQ (HslUV) protease. J. Bacteriol. 181 (1999) 3681-3687
46. S for degradation by ClpXP. Genes Dev. 15 (2001) 627-637