CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria

Molecular Microbiology

Volumn 31, Issue 1, 1999, Pages 117-131

  Derré, Isabelle ^a   Rapoport, Georges ^a   Msadek, Tarek ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DEOXYRIBONUCLEASE I; FUNGAL DNA; FUNGAL PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; CLOSTRIDIUM ACETOBUTYLICUM; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA FOOTPRINTING; DNA SEQUENCE; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION; GRAM POSITIVE BACTERIUM; HEAT SHOCK RESPONSE; LACTOBACILLUS SAKEI; LACTOCOCCUS LACTIS; LEUCONOSTOC; LISTERIA MONOCYTOGENES; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PURIFICATION; REPRESSOR GENE; SPOROGENESIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SALIVARIUS; STREPTOCOCCUS THERMOPHILUS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; DNA, BACTERIAL; ENDOPEPTIDASE CLP; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-POSITIVE BACTERIA; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; MICROSATELLITE REPEATS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS; REPRESSOR PROTEINS; SERINE ENDOPEPTIDASES;

EID: 0032921346     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01152.x     Document Type: Article

References (75)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Amory, A., Kunst, F., Aubert, E., Klier, A., and Rapoport, G. (1987) Characterization of the sacQ Genes from Bacillus licheniformis and Bacillus subtilis. J Bacteriol 169: 324-333.
3. Antelmann, H., Engelmann, S., Schmid, R., and Hecker, M. (1996) General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J Bacteriol 178: 6571-6578.
4. Arantes, O., and Lereclus, D. (1991) Construction of cloning vectors for Bacillus thuringiensis. Gene 108: 115-119.
5. B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol 175: 1929-1935.
6. 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.
7. Bsat, N., Chen, L, and Helmann, J.D. (1996) Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes. J Bacteriol 178: 6579-6586.
8. Bukau, B. (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9: 671-680.
9. Cohen, S.N., Chang, A.C.Y., and Hsu, L. (1972) Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci USA 69: 2110-2114.
10. Deuerling, E., Mogk, A., Richter, C., Purucker, M., and Schumann, W. (1997) The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol 23: 921-933.
11. Dodd, I.B., and Egan, J.B. (1990) Improved detection of helix-turn-helix DNA-binding motifs in protein sequences. Nucleic Acids Res 18: 5019-5026.
12. Gerth, U., Wipat, A., Harwood, C.R., Carter, N., Emmerson, P.T., and Hecker, M. (1996) Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 181: 77-83.
13. Gerth, U., Krüger, E., Derré, I., Msadek, T., and 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.
14. Gibson, T.J. (1984) Studies on the Epstein-Barr virus genome. PhD Thesis, University of Cambridge, Cambridge, UK.
15. Giffard, P.M., Rathsam, C., Kwan, E., Kwan, D.W., Bunny, K.L., Koo, S.P., et al. (1993) The ftf gene encoding the cell-bound fructosyltransferase of Streptococcus salivarius ATCC 25975 is preceded by an insertion sequence and followed by FUR1 and clpP homologues. J Gen Microbiol 139: 913-920.
16. Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30: 465-506.
17. Gottesman, S., Clark, W.P., de Crécy-Lagard, V., and Maurizi, M.R. (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.
18. Gottesman, S., Maurizi, M.R., and Wickner, S. (1997a) Regulatory subunits of energy-dependent proteases. Cell 91: 435-438.
19. Gottesman, S., Wickner, S., and Maurizi, M.R. (1997b) Protein quality control: triage by chaperones and proteases. Genes Dev 11: 815-823.
20. Gottesman, S., Roche, E., Zhou, Y.N., and Sauer, R.T. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12: 1338-1347.
21. Guedon, E., Delorme, C., Ehrlich, S.D., Bolotine, A., Sorokine, A., and Renault, P. (1998) Inventory of the proteolytic system of Lactococcus lactis from the genome data. In Proceedings of the American Society for Microbiology Conference on Streptococcal Genetics, Vichy, France.
22. Guzzo, J., Delmas, F., Pierre, F., Jobin, M.P., Samyn, B., Van Beeumen, J., et al. (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett Appl Microbiol 24: 393-396.
23. Hecker, M., and Völker, U. (1990) General stress proteins in Bacillus subtilis. FEMS Microbiol Ecol 74: 197-214.
24. Hecker, M., Schumann, W., and Völker, U. (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19: 417-428.
25. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., and Holden, D.W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
26. Higgins, D.G., Bleasby, A.J., and Fuchs, R. (1992) CLUSTAL V - Improved software for multiple sequence alignment. Comput Appl Biosci 8: 189-191.
27. Hirata, H., Fukazawa, T., Negoro, S., and Okada, H. (1986) Structure of a β-galactosidase gene of Bacillus stearothermophilus. J Bacteriol 166: 722-727.
28. Hurme, R., Berndt, K.D., Normark, S.J., and Rhen, M. (1997) A proteinaceous gene regulatory thermometer in Salmonella. Cell 90: 55-64.
29. Jakob, U., and Buchner, J. (1994) Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem Sci 19: 205-211.
30. Jakob, U., Gaestel, M., Engel, K., and Buchner, J. (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268: 1517-1520.
31. Jobin, M.P., Delmas, F., Garmyn, D., Divies, C., and Guzzo, J. (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.
32. 32-dependent heat shock protein F21.5. J Bacterial 172: 6026-6034.
33. Krüger, E., Volker, U., and Hecker, M. (1994) Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J Bacteriol 176: 3360-3367.
34. Krüger, E., Msadek, T., and Hecker, M. (1996) Alternate promoters direct stress-induced transcription of the Bacillus subtilis clpC operon. Mol Microbiol 20: 713-723.
35. Krüger, E., Msadek, T., Ohlmeier, S., and Hecker, M. (1997) The Bacillus subtilis clpC operon encodes DNA repair and competence proteins. Microbiology 143: 1309-1316.
36. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
37. Leung, D.W., Chen, E., and Goeddel, D.V. (1989) A method for random mutagenesis of a defined DNA segment using a modified polymerase chain reaction. Technique 1: 11-15.
38. Maxam, A.M., and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65: 499-560.
39. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
40. Misra, N., Habib, S., Ranjan, A., Hasnain, S.E., and Nath, I. (1996) Expression and functional characterisation of the clpC gene of Mycobacterium leprae: ClpC protein elicits human antibody response. Gene 172: 99-104.
41. Mogk, A., Homuth, G., Scholz, C., Kim, L., Schmid, F.X., and Schumann, W. (1997) The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J 16: 4579-4590.
42. Msadek, T., Kunst, F., Henner, D., Klier, A., Rapoport, G., and Dedonder, R. (1990) Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172: 824-834.
43. Msadek, T., Kunst, F., Klier, A., and Rapoport, G. (1991) DegS-DegU and ComP-ComA modulator-effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ. J Bacteriol 173: 2366-2377.
44. Msadek, T., Kunst, F., and Rapoport, G. (1994) MecB of Bacillus subtilis, a member of the ClpC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc Natl Acad Sci USA 91: 5788-5792.
45. Msadek, T., Dartois, V., Kunst, F., Herbaud, M.-L, Denizot, F., and Rapoport, G. (1998) CIpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 27: 899-914.
46. Mullis, K.B., and Faloona, F.A. (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol 155: 335-350.
47. Murphy, E. (1985) Nucleotide sequence of a spectinomycin adenyltransferase AAD (9) determinant from Staphylococcus aureus and its relationship to AAD (3″) (9). Mol Gen Genet 200: 33-39.
48. Ohta, T., Saito, K., Kuroda, M., Honda, K., Hirata, H., and Hayashi, H. (1994) Molecular cloning of two new heat shock genes related to the hsp70 genes in Staphylococcus aureus. J Bacteriol 176: 4779-4783.
49. Pederson, K.J., Carlson, S., and Pierson, D.E. (1997) The ClpP protein, a subunit of the Clp protease, modulates ail gene expression in Yersinia enterocolitica. Mol Microbiol 26: 99-107.
50. Riethdorf, S., Völker, U., Gerth, U., Winkler, A., Engelmann, S., and Hecker, M. (1994) Cloning, nucleotide sequence, and expression of the Bacillus subtilis Ion gene. J Bacteriol 176: 6518-6527.
51. Rouquette, C., Ripio, M.-T., Pellegrini, E., Bolla, J.-M., Tascon, R.I., Vázquez-Boland, J.-A., et al. (1996) Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol Microbiol 21: 977-987.
52. Rouquette, C., de Chastellier, C., Nair, S., and Berche, P. (1998) The ClpC ATPase of Listeria monocytogenes is a general stress protein required for virulence and promoting early bacterial escape from the phagosome of macrophages. Mol Microbiol 27: 1235-1246.
53. Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., et al. (1980) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487-491.
54. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
55. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
56. Sauer, U., and Dürre, P. (1993) Sequence and molecular characterization of a DNA region encoding a small heat shock protein of Clostridium acetobutylicum. J Bacteriol 175: 3394-3400.
57. Schägger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379.
58. Scharf, C., Riethdorf, S., Ernst, H., Engelmann, S., Völker, U., and Hecker, M. (1998) Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J Bacteriol 180: 1869-1877.
59. Schirmer, E.G., Glover, J.R., Singer, M.A., and Lindquist, S. (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21: 289-296.
60. Schulz, A., Schwab, S., Homuth, G., Versteeg, S., and Schumann, W. (1997) The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control. J Bacteriol 179: 3103-3109.
61. Squires, C.L., Pedersen, S., Ross, B.M., and Squires, C. (1991) ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol 173: 4254-4262.
62. Stentz, R., Lauret, R., Ehrlich, S.D., Morel-Deville, F., and Zagorec, M. (1997) Molecular cloning and analysis of the ptsHI operon in Lactobacillus sake. Appl Environ Microbiol 63: 2111-2116.
63. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
64. Tabor, S., and Richardson, C.C. (1987) DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci USA 84: 4767-4771.
65. Trieu-Cuot, P., Poyart-Salmeron, C., Carlier, C., and Courvalin, P. (1990) Nucleotide sequence of the erythromycin resistance gene of the conjugative transposon Tn1545, Nucleic Acids Res 18: 3660.
66. Turgay, K., Hamoen, L.W., Venema, G., and Dubnau, D. (1997) Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev 11: 119-128.
67. Völker, U., Engelmann, S., Maul, B., Riethdorf, S., Völker, A., Schmid, R., et al. (1994) Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology 140: 741-752.
68. Wawrzynow, A., Wojtkowiak, D., Marszalek, J., Banecki, B., Jonsen, M., Graves, B., et al. (1995) 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: 1867-1877.
69. Wawrzynow, A., Banecki, B., and Zylicz, M. (1996) The Clp ATPases define a novel class of molecular chaperones. Mol Microbiol 21: 895-899.
70. Weinrauch, Y., Msadek, T., Kunst, F., and Dubnau, D. (1991) Sequence and properties of comQ, a new competence regulatory gene of Bacillus subtilis. J Bacteriol 173: 5685-5693.
71. Wickner, S., Gottesman, S., Skowyra, D., Hoskins, J., McKenney, K., and Maurizi, M.R. (1994) A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci USA 91: 12218-12222.
72. Wojtkowiak, D., Georgopoulos, C., and Zylicz, M. (1993) Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J Biol Chem 268: 22609-22617.
73. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.
74. Yuan, G., and Wong, S.L. (1995) Isolation and characterization of Bacillus subtilis groE regulatory mutants: evidence for orf39 in the dnaK operon as a repressor gene in regulating the expression of both groE and dnaK. J Bacteriol 177: 6462-6468.
75. Zuber, U., and Schumann, W. (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 176: 1359-1363.