CtsR is the master regulator of stress response gene expression in Oenococcus oeni

Journal of Bacteriology

Volumn 187, Issue 16, 2005, Pages 5614-5623

  Grandvalet, Cosette ^a   Coucheney, Françoise ^a   Beltramo, Charlotte ^a   Guzzo, Jean ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; PROTEIN DNAK; SIGMA FACTOR;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GENOME; CLP GENE; CTSR GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUSION; GENETIC TRANSCRIPTION; GRAM POSITIVE BACTERIUM; HRCA GENE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OENOCOCCUS OENI; OPERON; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STRESS;

ADENOSINE TRIPHOSPHATASES; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; CHAPERONINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GRAM-POSITIVE COCCI; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OPERON; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS;

BACILLUS SUBTILIS; BACTERIUM SUBTILIS; OENOCOCCUS OENI; POSIBACTERIA;

EID: 23644453928     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.16.5614-5623.2005     Document Type: Article

References (59)

1. Altschul, S., T. Madden, A. Schaffer, J. Zhang, Z. Zhang, W, Miller, and D. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Avedissian, M., and S. Lopes Gomes. 1996. Expression of the groESL operon is cell-cycle controlled in Caulobacter crescentus. Mol. Microbiol. 19:79-89.
3. Barbosa, M. F., L. P. Yomano, and L. O. Ingram. 1994. Cloning, sequencing and expression of stress genes from the ethanol-producing bacterium Zymomonas mobilis: the groESL operon. Gene 148:51-57.
4. Beltramo, C., C. Grandvalet, F. Pierre, and J. Guzzo. 2004. Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J. Bacteriol. 186:2200-2205.
5. Beltramo, C., M. Oraby, G. Bourel, D. Garmyn, and J. Guzzo. 2004. A new vector, pGID052, for genetic transfer in Oenococcus oeni. FEMS Microbiol. Lett. 236:53-60.
6. Bolotin, A., P. Wincker, S. Mauger, O. Jaillon, K. Malarme, J. Weissenbach, S. D. Ehrlich, and A. Sorokin. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res. 11:731-753.
7. Bourdineaud, J. P., B. Nehme, S. Tesse, and A. Lonvaud-Funel. 2003. The ftsH gene of the wine bacterium Oenococcus oeni is involved in protection against environmental stress. Appl. Environ. Microbiol. 69:2512-2520.
8. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Cavin, J., H. Prevost, J. Lin, P. Schmitt, and C. Diviès. 1989. Medium for screening Leuconostoc oenos strains defective in malolactic fermentation. Appl. Environ. Microbiol. 55:751-753.
10. Chastanet, A., J. Fert, and T. Msadek. 2003. Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol. Microbiol. 47:1061-1073.
11. Chastanet, A., and T. Msadek. 2003. ClpP of Streptococcus salivarius is a novel member of the dually regulated class of stress response genes in Gram-positive bacteria. J. Bacteriol. 185:683-687.
12. Chastanet, A., M. Prudhomme, J. P. Claverys, and T. Msadek. 2001. Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J. Bacteriol. 183:7295-7307.
13. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
14. Chowdhury, S., C. Ragaz, E. Kreuger, and F. Narberhaus. 2003. Temperature-controlled structural alterations of an RNA thermometer. J. Biol. Chem. 278:47915-47921.
15. Derré, I., G. Rapoport, and T. Msadek. 2000. The CtsR regulator of stress response is active as a dimer and specifically degraded in vivo at 37°C. Mol. Microbiol. 38:335-347.
16. Derré, I., G. Rapoport, and T. Msadek. 1999. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol. Microbiol. 31:117-131.
17. Desroche, N., C. Beltramo, and J. Guzzo. 2005. Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J. Microbiol. Methods 60:325-333.
18. Dicks, L. M., F. Dellaglio, and M. D. Collins. 1995. Proposal to reclassify Leuconostoc oenos as Oenococcus oeni [corrig.] gen. nov., comb. nov. Int. J. Syst. Bacteriol. 45:395-397.
19. Emory, S. A., and J. G. Belasco. 1990. The ompA 5′ untranslated RNA segment functions in Escherichia coli as a growth-rate-regulated mRNA stabilizer whose activity is unrelated to translational efficiency. J. Bacteriol. 172:4472-4481.
20. Fernandez, R. C., and A. A. Weiss. 1995. Cloning and sequencing of the Bordetella pertussis cpn10/cpn60 (groESL) homolog. Gene 158:151-152.
21. Gerth, U., E. Kruger, I. Derré, T. Msadek, and M. Hecker. 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.
22. Gerth, U., A. Wipat, C. R. Harwood, N. Carter, P. T. Emmerson, and M. Hecker. 1996. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 181:77-83.
23. Gertz, S., S. Engelmann, R. Schmid, A. K. Ziebandt, K. Tischer, C. Scharf, J. Hacker, and M. Hecker. 2000. Characterization of the sigma (B) regulon in Staphylococcus aureus. J. Bacteriol. 182:6983-6991.
24. Gottesman, S., W. P. Clark, V. de Crecy-Lagard, and M. R. Maurizi. 1993. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J. Biol. Chem. 268:22618-22626.
25. Gottesman, S., S. Wickner, and M. R. Maurizi. 1997. Protein quality control: triage by chaperones and proteases. Genes Dev. 11:815-823.
26. Grandvalet, C., G. Rapoport, and P. Mazodier. 1998. hrcA, encoding the represser of the groEL genes in Streptomyces albus G. is associated with a second dnaJ gene. J. Bacteriol. 180:5129-5134.
27. Grandvalet, C., P. Servant, and P. Mazodier. 1997. Disruption of hspR, the repressor gene of the dnaK operon in Streptomyces albus G. Mol. Microbiol. 23:77-84.
28. Hecker, M., W. Schumann, and U. Volker. 1996. Heat-shock and general stress response in Bacillus subtilis. Mol. Microbiol. 19:417-428.
29. Hirata, H., T. Fukazawa, S. Negoro, and H. Okada. 1986. Structure of a beta-galactosidase gene of Bacillus stearothermophilus. J. Bacteriol. 166:722-727.
30. Jobin, M. P., F. Delmas, D. Garmyn, C. Divies, and J. Guzzo. 1997. Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos. Appl. Environ. Microbiol. 63:609-614.
31. Jobin, M. P., D. Garmyn, C. Divies, and J. Guzzo. 1999. Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiology 145:1245-1251.
32. Jobin, M. P., D. Garmyn, C. Divies, and J. Guzzo. 1999. The Oenococcus oeni clpX homologue is a heat shock gene preferentially expressed in exponential growth phase. J. Bacteriol. 181:6634-6641.
33. Klaenhammer, T., E. Altermann, F. Arigoni, A. Bolotin, F. Breidt, J. Broadbent, R. Cano, S. Chaillou, J. Deutscher, M. Gasson, M. van de Guchte, J. Guzzo, A. Hartke, T. Hawkins, P. Hols, R. Hutkins, M. Kleerebezem, J. Kok, O. Kuipers, M. Lubbers, E. Maguin, L. McKay, D. Mills, A. Nauta, R. Overbeek, H. Pel, D. Pridmore, M. Saier, D. van Sinderen, A. Sorokin, J. Steele, D. O'Sullivan, W. de Vos, B. Weimer, M. Zagorec, and R. Siezen. 2002. Discovering lactic acid bacteria by genomics. Antonie Leeuwenhoek 82:29-58.
34. Kruger, E., T. Msadek, S. Ohlmeier, and M. Hecker. 1997. The Bacillus subtilis clpC operon encodes DNA repair and competence proteins. Microbiology 143:1309-1316.
35. Kruger, E., D. Zuhlke, E. Witt, H. Ludwig, and M. Hecker. 2001. Clp-mediated proteolysis in Gram-positive bacteria is autoregulated by the stability of a repressor. EMBO J. 20:852-863.
36. Kunkee, R. E. 1991. Some roles of malic acid in the malolactic fermentation in wine making. FEMS Microbiol. Lett. 88:55-71.
37. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessieres, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brignell, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S. K. Choi, J. J. Codani, I. F. Connerton, A. Danchin, et al. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249-256.
38. Lundberg, U., A. von Gabain, and O. Melefors. 1990. Cleavages in the 5′ region of the ompA and bla mRNA control stability: studies with an E. coli mutant altering mRNA stability and a novel endoribonuclease. EMBO J. 9:2731-2741.
39. Mantis, N. J., and S. C. Winans. 1992. Characterization of the Agrobacterium tumefaciens heat shock response: evidence for a sigma 32-like sigma factor. J. Bacteriol. 174:991-997.
40. Michel, G. P. 1993. Cloning and expression in Escherichia coli of the dnaK gene of Zymomonas mobilis. J. Bacteriol. 175:3228-3231.
41. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Msadek, T., V. Dartois, F. Kunst, M. Herbaud, F. Denizot, and G. Rapoport. 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.
43. Petersohn, A., M. Brigulla, S. Haas, J. D. Hoheisel, U. Volker, and M. Hecker. 2001. Global analysis of the general stress response of Bacillus subtilis. J. Bacteriol. 183:5617-5631.
44. Price, C. W., P. Fawcett, H. Ceremonie, N. Su, C. K. Murphy, and P. Youngman. 2001. Genome-wide analysis of the general stress response in Bacillus subtilis. Mol. Microbiol. 41:757-774.
45. Reisenauer, A., C. D. Mohr, and L. Shapiro. 1996. Regulation of a heat shock sigma 32 homolog in Caulobacter crescentus. J. Bacteriol. 178:1919-1927.
46. Roberts, R. C., C. Toochinda, M. Avedissian, R. L. Baldini, S. L. Gomes, and L. Shapiro, 1996. Identification of a Caulobacter crescentus operon encoding hrcA. involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE. J. Bacteriol. 178:1829-1841.
47. Rouquette, C., M. T. Ripio, E. Pellegrini, J. M. Bella, R. I. Tascon, J. A. Vazquez-Boland, and P. Berche. 1996. Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol. Microbiol. 21:977-987.
48. Sambrook, J., E. F. Frisch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Schumann, W., M. Hecker, and T, Msadek. 2002. Regulation and function of heat-inducible genes in Bacillus subtilis, p. 359-368. In A. L. Sonenshein, J. A. Hoch, and R. M. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, D.C.
50. Segal, G., and E. Z. Ron. 1995. The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J. Bacteriol. 177:5952-5958.
51. Segal, G., and E. Z. Ron. 1993. Heat shock transcription of the groESL operon of Agrobacterium tumefaciens may involve a hairpin-loop structure. J. Bacteriol. 175:3083-3088.
52. Segal, R., and E. Z. Ron. 1996. Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol. Lett. 138:1-10.
53. Servant, P., C. Grandvalet, and P. Mazodier. 2000. The RheA repressor is the thermosensor of the HSP18 heat shock response in Streptomyces albus. Proc. Natl. Acad. Sci. USA 97:3538-3543.
54. Skinner, M. M., and J. E. Trempy. 2001. Expression of clpX, an ATPase subunit of the Clp protease, is heat and cold shock inducible in Lactococcus lactis. J. Dairy Sci. 84:1783-1785.
55. Ueguchi, C., M. Kakeda, H. Yamada, and T. Mizuno. 1994. An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc. Natl. Acad. Sci. USA 91:1054-1058.
56. Varmanen, P., H. Ingmer, and F. K. Vogensen. 2000. ctsR of Lactococcus lactis encodes a negative regulator of clp gene expression. Microbiology 146:1447-1455.
57. Yuan, G., and S. Wong. 1995. Regulation of groE expression in Bacillus subtilis: the involvement of the sigma A-like promoter and the roles of the inverted repeat sequence (CIRCE). J. Bacteriol. 177:5427-5433.
58. Yura, T., K. Nakahigashi, and M. Kanemori. 1996. Transcriptional regulation of stress-inducible genes in procaryotes. EXS 77:165-181.
59. Zuber, U., and W. Schumann. 1994. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol. 176:1359-1363.