Critical clamp loader processing by an essential AAA+ protease in Caulobacter crescentus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 45, 2013, Pages 18138-18143

  Vass, Robert H ^a   Chien, Peter ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

ClpP; ClpX internal recognition; Protease stalling

Indexed keywords

AAA PROTEASE; BACTERIAL PROTEIN; CASEIN; CLPXP PROTEIN; DNA; DNAX PROTEIN; GLYCINE; PROTEIN; PROTEINASE; SLIDING CLAMP LOADER; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIABILITY; CAULOBACTER CRESCENTUS; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING;

CLPP; CLPX INTERNAL RECOGNITION; PROTEASE STALLING;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CAULOBACTER CRESCENTUS; CHROMOSOMES, BACTERIAL; DNA POLYMERASE III; DNA REPLICATION; ENDOPEPTIDASE CLP; MICROSCOPY; PROTEIN SUBUNITS;

EID: 84887284045     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311302110     Document Type: Article

References (37)

1. Sauer RT, Baker TA (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80:587-612.
2. Camberg JL, Hoskins JR, Wickner S (2009) ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc Natl Acad Sci USA 106(26): 10614-10619.
3. Neher SB, et al. (2006) Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol Cell 22(2):193-204.
4. Zhou Y, Gottesman S (1998) Regulation of proteolysis of the stationary-phase sigma factor RpoS. J Bacteriol 180(5):1154-1158.
5. Pratt LA, Silhavy TJ (1996) The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci USA 93(6):2488-2492.
6. Hengge R (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160(9):667-676.
7. Kenniston JA, Baker TA, Fernandez JM, Sauer RT (2003) Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114(4):511-520.
8. Martin A, Baker TA, Sauer RT (2008) Protein unfolding by a AAA+ protease is dependent on ATP-hydrolysis rates and substrate energy landscapes. Nat StructMol Biol 15(2):139-145.
9. Maillard RA, et al. (2011) ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145(3):459-469.
10. Aubin-Tam ME, Olivares AO, Sauer RT, Baker TA, Lang MJ (2011) Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145(2):257-267.
11. Kenniston JA, Baker TA, Sauer RT (2005) Partitioning between unfolding and release of native domains during ClpXP degradation determines substrate selectivity and partial processing. Proc Natl Acad Sci USA 102(5):1390-1395.
12. Johnson A, O'Donnell M (2005) Cellular DNA replicases: Components and dynamics at the replication fork. Annu Rev Biochem 74:283-315.
13. Flower AM, McHenry CS (1990) The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci USA 87(10):3713-3717.
14. Tsuchihashi Z, Kornberg A (1990) Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 87(7):2516-2520.
15. Blinkowa AL, Walker JR (1990) Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res 18(7):1725-1729.
16. Blinkova A, et al. (1993) The Escherichia coli DNA polymerase III holoenzyme contains both products of the dnaX gene, tau and gamma, but only tau is essential. J Bacteriol 175(18):6018-6027.
17. McHenry CS (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80:403-436.
18. Gao D, McHenry CS (2001) tau binds and organizes Escherichia coli replication through distinct domains. Partial proteolysis of terminally tagged tau to determine candidate domains and to assign domain V as the alpha binding domain. J Biol Chem 276(6):4433-4440.
19. Gao D, McHenry CS (2001) Tau binds and organizes Escherichia coli replication proteins through distinct domains. Domain III, shared by gamma and tau, binds delta delta ' and chi psi. J Biol Chem 276(6):4447-4453.
20. Bhat NH, Vass RH, Stoddard PR, Shin DK, Chien P (2013) Identification of ClpP substrates in Caulobacter crescentus reveals a role for regulated proteolysis in bacterial development. Mol Microbiol 88(6):1083-1092.
21. Jenal U, Fuchs T (1998) An essential protease involved in bacterial cell-cycle control. EMBO J 17(19):5658-5669.
22. Flynn JM, et al. (2001) Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc Natl Acad Sci USA 98(19):10584-10589.
23. Hoskins JR, Yanagihara K, Mizuuchi K, Wickner S (2002) ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence. Proc Natl Acad Sci USA 99(17):11037-11042.
24. Abdelhakim AH, Oakes EC, Sauer RT, Baker TA (2008) Unique contacts direct highpriority recognition of the tetrameric Mu transposase-DNA complex by the AAA+ unfoldase ClpX. Mol Cell 30(1):39-50.
25. Neher SB, Sauer RT, Baker TA (2003) 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(23):13219-13224.
26. Wojtyra UA, Thibault G, Tuite A, Houry WA (2003) The N-terminal zinc binding domain of ClpX is a dimerization domain that modulates the chaperone function. J Biol Chem 278(49):48981-48990.
27. Lee C, Schwartz MP, Prakash S, Iwakura M, Matouschek A (2001) ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol Cell 7(3):627-637.
28. Tian L, Holmgren RA, Matouschek A (2005) A conserved processing mechanism regulates the activity of transcription factors Cubitus interruptus and NF-kappaB. Nat Struct Mol Biol 12(12):1045-1053.
29. Schrader EK, Harstad KG, Holmgren RA, Matouschek A (2011) A three-part signal governs differential processing of Gli1 and Gli3 proteins by the proteasome. J Biol Chem 286(45):39051-39058.
30. Too PH, Erales J, Simen JD, Marjanovic A, Coffino P (2013) Slippery substrates impair function of a bacterial protease ATPase by unbalancing translocation versus exit. J Biol Chem 288(19):13243-13257.
31. Jeruzalmi D, O'Donnell M, Kuriyan J (2001) Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III. Cell 106(4):429-441.
32. Larsen B, Wills NM, Nelson C, Atkins JF, Gesteland RF (2000) Nonlinearity in genetic decoding: Homologous DNA replicase genes use alternatives of transcriptional slippage or translational frameshifting. Proc Natl Acad Sci USA 97(4):1683-1688.
33. Sutton MD (2010) Coordinating DNA polymerase traffic during high and low fidelity synthesis. Biochim Biophys Acta 1804(5):1167-1179.
34. Langston LD, Indiani C, O'Donnell M (2009) Whither the replisome: Emerging perspectives on the dynamic nature of the DNA replication machinery. Cell Cycle 8(17): 2686-2691.
35. Galhardo RS, Rocha RP, Marques MV, Menck CF (2005) An SOS-regulated operon involved in damage-inducible mutagenesis in Caulobacter crescentus. Nucleic Acids Res 33(8):2603-2614.
36. Reyes-Lamothe R, Sherratt DJ, Leake MC (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328(5977):498-501.
37. Rood KL, Clark NE, Stoddard PR, Garman SC, Chien P (2012) Adaptor-dependent degradation of a cell-cycle regulator uses a unique substrate architecture. Structure 20(7):1223-1232.