The ClpPX protease is required for radioresistance and regulates cell division after γ-irradiation in Deinococcus radiodurans

Molecular Microbiology

Volumn 66, Issue 5, 2007, Pages 1231-1239

  Servant, Pascale ^a   Jolivet, Edmond ^a   Bentchikou, Esma ^a   Mennecier, Samuel ^a   Bailone, Adriana ^a   Sommer, Suzanne ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; ENDOPEPTIDASE CLP; ENDOPEPTIDASE LA; PROTEIN CLPPX; PUROMYCIN; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CELL CYCLE REGULATION; CELL DAMAGE; CELL DIVISION; CELL SURVIVAL; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; DNA REPAIR; ENZYME INACTIVATION; ENZYME MECHANISM; GAMMA IRRADIATION; GENE DISRUPTION; KINETICS; LUNG CONGESTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FOLDING; RADIATION DOSE; RADIOSENSITIVITY;

DEINOCOCCUS RADIODURANS;

EID: 36148981464     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06003.x     Document Type: Article

References (50)

1. Alba, B.M., Leeds, J.A., Onufryk, C., Lu, C.Z. Gross, C.A. (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev 16 : 2156 2168.
2. Anderson, A.W., Nordon, H.C., Cain, R.F., Parrish, G. Duggan, G. (1956) Studies on a radio-resistant micrococcus. I. Isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol 10 : 575 578.
3. Battista, J.R. (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol 51 : 203 224.
4. Battista, J.R., Earl, A.M. Park, M.J. (1999) Why is Deinococcus radiodurans so resistant to ionizing radiation? Trends Microbiol 7 : 362 365.
5. Bentchikou, E., Servant, P., Coste, G. Sommer, S. (2007) Additive effects of SbcCD and PolX deficiencies in the in vivo repair of DNA double-strand breaks in Deinococcus radiodurans. J Bacteriol 189 : 4784 4790.
6. Bonacossa de Almeida, C., Coste, G., Sommer, S. Bailone, A. (2002) Quantification of RecA protein in Deinococcus radiodurans reveals involvement of RecA, but not LexA, in its regulation. Mol Genet Genomics 268 : 28 41.
7. Burton, B.M. Baker, T.A. (2005) Remodeling protein complexes: insights from the AAA+ unfoldase ClpX and Mu transposase. Protein Sci 14 : 1945 1954.
8. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Venkateswaran, A., et al. (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306 : 1025 1028.
9. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Leapman, R.D., et al. (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5 : e92.
10. Domian, I.J., Quon, K.C. Shapiro, L. (1997) Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90 : 415 424.
11. Earl, A.M., Mohundro, M.M., Mian, I.S. Battista, J.R. (2002a) The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J Bacteriol 184 : 6216 6224.
12. Earl, A.M., Rankin, S.K., Kim, K.P., Lamendola, O.N. Battista, J.R. (2002b) Genetic evidence that the uvsE gene product of Deinococcus radiodurans R1 is a UV damage endonuclease. J Bacteriol 184 : 1003 1009.
13. Fabret, C., Ehrlich, S.D. Noirot, P. (2002) A new mutation delivery system for genome-scale approaches in Bacillus subtilis. Mol Microbiol 46 : 25 36.
14. Frank, E.G., Ennis, D.G., Gonzalez, M., Levine, A.S. Woodgate, R. (1996) Regulation of SOS mutagenesis by proteolysis. Proc Natl Acad Sci USA 93 : 10291 10296.
15. Frees, D. Ingmer, H. (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol Microbiol 31 : 79 87.
16. Frees, D., Qazi, S.N., Hill, P.J. Ingmer, H. (2003) Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol 48 : 1565 1578.
17. Gerth, U., Kruger, E., Derre, I., Msadek, T. Hecker, M. (1998) Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol Microbiol 28 : 787 802.
18. Gottesman, S. (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19 : 565 587.
19. Gottesman, S., Squires, C., Pichersky, E., Carrington, M., Hobbs, M., Mattick, J.S., et al. (1990) Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc Natl Acad Sci USA 87 : 3513 3517.
20. Grimaud, R., Ezraty, B., Mitchell, J.K., Lafitte, D., Briand, C., Derrick, P.J. Barras, F. (2001) Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J Biol Chem 276 : 48915 48920.
21. Harris, D.R., Tanaka, M., Saveliev, S.V., Jolivet, E., Earl, A.M., Cox, M.M. Battista, J.R. (2004) Preserving genome integrity: the DdrA protein of Deinococcus radiodurans R1. PLoS Biol 2 : e304.
22. Hengge, R. Bukau, B. (2003) Proteolysis in prokaryotes: protein quality control and regulatory principles. Mol Microbiol 49 : 1451 1462.
23. Hua, Y., Narumi, I., Gao, G., Tian, B., Satoh, K., Kitayama, S. Shen, B. (2003) PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem Biophys Res Commun 306 : 354 360.
24. Huisman, O. D'Ari, R. (1981) An inducible DNA replication-cell division coupling mechanism in E. coli. Nature 290 : 797 799.
25. Jenal, U. Hengge-Aronis, R. (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6 : 163 172.
26. Joshi, B., Schmid, R., Altendorf, K. Apte, S.K. (2004) Protein recycling is a major component of post-irradiation recovery in Deinococcus radiodurans strain R1. Biochem Biophys Res Commun 320 : 1112 1117.
27. Kock, H., Gerth, U. Hecker, M. (2004) The ClpP peptidase is the major determinant of bulk protein turnover in Bacillus subtilis. J Bacteriol 186 : 5856 5864.
28. Lecointe, F., Shevelev, I.V., Bailone, A., Sommer, S. Hubscher, U. (2004) Involvement of an X family DNA polymerase in double-stranded break repair in the radioresistant organism Deinococcus radiodurans. Mol Microbiol 53 : 1721 1730.
29. McGrath, P.T., Iniesta, A.A., Ryan, K.R., Shapiro, L. McAdams, H.H. (2006) A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124 : 535 547.
30. Makarova, K.S., Aravind, L., Wolf, Y.I., Tatusov, R.L., Minton, K.W., Koonin, E.V. Daly, M.J. (2001) Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65 : 44 79.
31. Mattimore, V. Battista, J.R. (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178 : 633 637.
32. Meima, R., Rothfuss, H.M., Gewin, L. Lidstrom, M.E. (2001) Promoter cloning in the radioresistant bacterium Deinococcus radiodurans. J Bacteriol 183 : 3169 3175.
33. Mennecier, S., Coste, G., Servant, P., Bailone, A. Sommer, S. (2004) Mismatch repair ensures fidelity of replication and recombination in the radioresistant organism Deinococcus radiodurans. Mol Genet Genomics 272 : 460 469.
34. Mennecier, S., Servant, P., Coste, G., Bailone, A. Sommer, S. (2006) Mutagenesis via IS transposition in Deinococcus radiodurans. Mol Microbiol 59 : 317 325.
35. Minton, K.W. (1994) DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol Microbiol 13 : 9 15.
36. Missiakas, D., Schwager, F., Betton, J.M., Georgopoulos, C. Raina, S. (1996) Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J 15 : 6899 6909.
37. Mizusawa, S., Court, D. Gottesman, S. (1983) Transcription of the sulA gene and repression by LexA. J Mol Biol 171 : 337 343.
38. Mizusawa, S. Gottesman, S. (1983) Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein. Proc Natl Acad Sci USA 80 : 358 362.
39. Msadek, T., Dartois, V., Kunst, F., Herbaud, M.L., Denizot, F. Rapoport, G. (1998) ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 27 : 899 914.
40. Narumi, I., Satoh, K., Kikuchi, M., Funayama, T., Yanagisawa, T., Kobayashi, Y., et al. (2001) The LexA protein from Deinococcus radiodurans is not involved in RecA induction following gamma irradiation. J Bacteriol 183 : 6951 6956.
41. Neher, S.B., Villen, J., Oakes, E.C., Bakalarski, C.E., Sauer, R.T., Gygi, S.P. Baker, T.A. (2006) Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol Cell 22 : 193 204.
42. Schirmer, E.C., Glover, J.R., Singer, M.A. Lindquist, S. (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21 : 289 296.
43. Sheng, D., Zheng, Z., Tian, B., Shen, B. Hua, Y. (2004) LexA analog (dra0074) is a regulatory protein that is irrelevant to recA induction. J Biochem (Tokyo) 136 : 787 793.
44. Skerker, J.M. Laub, M.T. (2004) Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2 : 325 337.
45. Tanaka, M., Earl, A.M., Howell, H.A., Park, M.J., Eisen, J.A., Peterson, S.N. Battista, J.R. (2004) Analysis of Deinococcus radiodurans's transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 168 : 21 33.
46. Thomsen, L.E., Olsen, J.E., Foster, J.W. Ingmer, H. (2002) ClpP is involved in the stress response and degradation of misfolded proteins in Salmonella enterica serovar Typhimurium. Microbiology 148 : 2727 2733.
47. Walker, G.C. (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48 : 60 93.
48. Zahradka, K., Slade, D., Bailone, A., Sommer, S., Averbeck, D., Petranovic, M., et al. (2006) Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443 : 569 573.
49. Zhou, Y., Gottesman, S., Hoskins, J.R., Maurizi, M.R. Wickner, S. (2001) The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev 15 : 627 637.
50. Zimmerman, J.M. Battista, J.R. (2005) A ring-like nucleoid is not necessary for radioresistance in the Deinococcaceae. BMC Microbiol 5 : 17.