Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals

Molecular Cell

Volumn 11, Issue 3, 2003, Pages 671-683

  Flynn, Julia M ^a   Neher, Saskia B ^a   Kim, Yong In ^a,c   Sauer, Robert T ^a   Baker, Tania A ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c ABBOTT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HYBRID PROTEIN; PEPTIDE HISTIDINE ISOLEUCINE; PROTEIN; PROTEIN CLP X; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; MASS SPECTROMETRY; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN TARGETING; PROTEOMICS; STARVATION; UNINDEXED SEQUENCE;

ESCHERICHIA COLI;

EID: 0037351068     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00060-1     Document Type: Article

References (62)

1. Alba B.M., Leeds J.A., Onufryk C., Lu C.Z., Gross C.A. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev. 16:2002;2156-2168.
2. Almiron M., Link A.J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:1992;2646-2654.
3. Anderson L.A., McNairn E., Leubke T., Pau R.N., Boxer D.H. ModE-dependent molybdate regulation of the molybdenum cofactor operon moa in Escherichia coli. J. Bacteriol. 182:2000;7035-7043.
4. Ben-Bassat A., Bauer K., Chang S.Y., Myambo K., Boosman A., Chang S. Processing of the initiation methionine from proteins. properties of the Escherichia coli methionine aminopeptidase and its gene structure J. Bacteriol. 169:1987;751-757.
5. Bjellqvist B., Pasquali C., Ravier F., Sanchez J.C., Hochstrasser D. A nonlinear wide-range immobilized pH gradient for two-dimensional electrophoresis and its definition in a relevant pH scale. Electrophoresis. 14:1993;1357-1365.
6. Burton R.E., Siddiqui S.M., Kim Y.I., Baker T.A., Sauer R.T. Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J. 20:2001;3092-3100.
7. Damerau K., St. John A.C. Role of Clp protease subunits in degradation of carbon starvation proteins in Escherichia coli. J. Bacteriol. 175:1993;53-63.
8. Davis B.D., Luger S.M., Tai P.C. Role of ribosome degradation in the death of starved Escherichia coli cells. J. Bacteriol. 166:1986;439-445.
9. 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.
10. Frank E.G., Ennis D.G., Gonzalez M., Levine A.S., Woodgate R. Regulation of SOS mutagenesis by proteolysis. Proc. Natl. Acad. Sci. USA. 93:1996;10291-10296.
11. 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 λ O replication protein by the ClpP/ClpX protease. J. Biol. Chem. 274:1999;13999-14005.
12. Gonzalez M., Rasulova F., Maurizi M.R., 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.
13. Gottesman S. Proteases and their targets in Escherichia coli. Annu. Rev. Genet. 30:1996;465-506.
14. Gottesman S., Clark W.P., de Crecy-Lagard V., Maurizi M.R. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J. Biol. Chem. 268:1993;22618-22626.
15. 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.
16. Grant R.A., Filman D.J., Finkel S.E., Kolter R., Hogle J.M. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 5:1998;294-303.
17. 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.
18. Harlow E., Lane D. Antibodies, A Laboratory Manual. 1988;Cold Spring Harbor Laboratory Press, Plainview, NY.
19. Hengge-Aronis R. Regulation of gene expression during entry into stationary phase. Neidhardt F.C. Escherichia coli and Salmonella. 1996;American Society for Microbiology, Washington, DC. 1497-1512.pp.
20. Herman C., Thevenet D., Bouloc P., Walker G.C., D'Ari R. Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH). Genes Dev. 12:1998;1338-1347.
21. Hoskins J.R., Yanagihara K., Mizuuchi K., Wickner S. ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence. Proc. Natl. Acad. Sci. USA. 99:2002;11037-11042.
22. Jenal U., Fuchs T. An essential protease involved in bacterial cell-cycle control. EMBO J. 17:1998;5658-5669.
23. Jishage M., Ishihama A. A stationary phase protein in Escherichia coli with binding activity to the major sigma subunit of RNA polymerase. Proc. Natl. Acad. Sci. USA. 95:1998;4953-4958.
24. Kang P.J., Craig E.A. Identification and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J. Bacteriol. 172:1990;2055-2064.
25. Karzai A.W., Susskind M.M., Sauer R.T. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 18:1999;3793-3799.
26. Katayama Y., Gottesman S., Pumphrey J., Rudikoff S., Clark W.P., Maurizi M.R. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J. Biol. Chem. 263:1988;15226-15236.
27. Keiler K.C., Waller P.R., Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science. 271:1996;990-993.
28. Kiley P.J., Beinert H. Oxygen sensing by the global regulator, FNR. the role of the iron-sulfur cluster FEMS Microbiol. Rev. 22:1998;341-352.
29. Kim S.J., Han Y.H., Kim I.H., Kim H.K. Involvement of ArcA and Fnr in expression of Escherichia coli thiol peroxidase gene. IUBMB Life. 48:1999;215-218.
30. 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.
31. Konieczny I., Helinski D.R. The replication initiation protein of the broad-host-range plasmid RK2 is activated by the ClpX chaperone. Proc. Natl. Acad. Sci. USA. 94:1997;14378-14382.
32. Levchenko I., Luo L., Baker T.A. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9:1995;2399-2408.
33. Levchenko I., Yamauchi M., Baker T.A. ClpX and MuB interact with overlapping regions of Mu transposase. implications for control of the transposition pathway Genes Dev. 11:1997;1561-1572.
34. Little, J.W. (1983). Variations in the in vivo stability of LexA repressor during the SOS regulatory cycle. Paper presented at: Cellular Responses to DNA Damage, April 10-15, 1983.
35. Little J.W., Edmiston S.H., Pacelli L.Z., Mount D.W. Cleavage of the Escherichia coli LexA protein by the RecA protease. Proc. Natl. Acad. Sci. USA. 77:1980;3225-3229.
36. Luo Y., Pfuetzner R.A., Mosimann S., Paetzel M., Frey E.A., Cherney M., Kim B., Little J.W., Strynadka N.C. Crystal structure of LexA. a conformational switch for regulation of self-cleavage Cell. 106:2001;585-594.
37. Lupas A., Flanagan J.M., Tamura T., Baumeister W. Self-compartmentalizing proteases. Trends Biochem. Sci. 22:1997;399-404.
38. Lynch A.S., Lin E.C.C. Responses to molecular oxygen. Frederick N.C. Escherichia coli and Salmonella. 1996;American Society for Microbiology, Washington, DC. 1526-1538.pp.
39. Makovets S., Titheradge A.J., Murray N.E. ClpX and ClpP are essential for the efficient acquisition of genes specifying type IA and IB restriction systems. Mol. Microbiol. 28:1998;25-35.
40. Martinez A., Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179:1997;5188-5194.
41. Maurizi M.R., Clark W.P., Katayama Y., Rudikoff S., Pumphrey J., Bowers B., Gottesman S. Sequence and structure of ClpP, the proteolytic component of the ATP- dependent Clp protease of Escherichia coli. J. Biol. Chem. 265:1990;12536-12545. a.
42. Msadek T., Dartois V., Kunst F., Herbaud M.L., Denizot F., Rapoport G. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol. Microbiol. 27:1998;899-914.
43. 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.
44. Ogura T., Wilkinson A.J. AAA+ superfamily ATPases. common structure-diverse function Genes Cells. 6:2001;575-597.
45. 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.
46. Ortega J., Lee H.S., Maurizi M.R., Steven A.C. Alternating translocation of protein substrates from both ends of ClpXP protease. EMBO J. 21:2002;4938-4949.
47. Pelham H.R. Speculations on the functions of the major heat shock and glucose- regulated proteins. Cell. 46:1986;959-961.
48. Pellicer M.T., Fernandez C., Badia J., Aguilar J., Lin E.C., Baldom L. Cross-induction of glc and ace operons of Escherichia coli attributable to pathway intersection. Characterization of the glc promoter. J. Biol. Chem. 274:1999;1745-1752. a.
49. Pellicer M.T., Lynch A.S., De Wulf P., Boyd D., Aguilar J., Lin E.C. A mutational study of the ArcA-P binding sequences in the aldA promoter of Escherichia coli. Mol. Gen. Genet. 261:1999;170-176. b.
50. 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.
51. Pratt L.A., Silhavy T.J. Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 29:1998;1225-1236.
52. Robinson C.R., Sauer R.T. Equilibrium stability and sub-millisecond refolding of a designed single-chain Arc repressor. Biochemistry. 35:1996;13878-13884.
53. 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.
54. Schweder T., Lee K.H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J. Bacteriol. 178:1996;470-476.
55. 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.
56. 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.
57. Wawrzynow A., Wojtkowiak D., Marszalek J., Banecki B., Jonsen M., Graves B., Georgopoulos C., Zylicz M. The ClpX heat-shock protein of Escherichia coli, the ATP-dependent substrate specificity component of the ClpP-ClpX protease, is a novel molecular chaperone. EMBO J. 14:1995;1867-1877.
58. Webb C., Moreno M., Wilmes-Riesenberg M., Curtiss R. 3rd, Foster J.W. Effects of DksA and ClpP protease on Sigma S production and virulence in Salmonella typhimurium. Mol. Microbiol. 34:1999;112-123.
59. 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.
60. Wojtkowiak D., Georgopoulos C., Zylicz M. Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J. Biol. Chem. 268:1993;22609-22617.
61. Wu W.F., Zhou Y., Gottesman S. Redundant in vivo proteolytic activities of Escherichia coli Lon and the ClpYQ (HslUV) protease. J. Bacteriol. 181:1999;3681-3687.
62. Yakhnin A.V., Vinokurov L.M., Surin A.K., Alakhov Y.B. Green fluorescent protein purification by organic extraction. Protein Expr. Purif. 14:1998;382-386.