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Bacterial Stress Response

  • Reference work entry
The Prokaryotes

1 Introduction

Most bacteria live in a dynamic environment where temperature, availability of nutrients, and presence of various chemicals vary. Quick adaptation to these environmental changes is carried out by a series of global regulatory networks that control the simultaneous expression of a large number of genes. There are global regulatory systems that respond to change of temperature, pH, nutrients, salts and oxidation. The level of response by these regulatory networks is proportional to the extent of the change. Since the response level is highest under changes that constitute a stress condition, the control networks are labeled “stress response” systems.

The stress response systems show a high degree of similarity in prokaryotes, and some (e.g., the heat shock response) are also conserved in eukaryotes and archaea. However, the conditions under which the response systems are activated differ significantly from one organism to another. Clearly, the temperatures in which the...

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Literature Cited

  • Akbar, S., and C. W. Price. 1996 Isolation and characterization of csbB, a gene controlled by Bacillus subtilis general stress transcription factor sigma B Gene 177 123–128

    Article  PubMed  CAS  Google Scholar 

  • Akbar, S., T. A. Gaidenko, C. M. Kang, M. O’Reilly, K. M. Devine, and C. W. Price. 2001 New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigma(B) of Bacillus subtilis J. Bacteriol. 183 1329–1338

    Article  PubMed  CAS  Google Scholar 

  • Alba, B. M., and C. A. Gross. 2004 Regulation of the Escherichia colisigma-dependent envelope stress response Molec. Microbiol. 52 613–619

    Article  CAS  Google Scholar 

  • Allen, S. P., J. O. Polazzi, J. K. Gierse, and A. M. Easton. 1992 Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli J. Bacteriol. 174 6938–6947

    PubMed  CAS  Google Scholar 

  • Andersson, S. G., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. Alsmark, R. M. Podowski, A. K. Naslund, A. S. Eriksson, H. H. Winkler, and C. G. Kurland. 1998 The genome sequence of Rickettsia prowazekii and the origin of mitochondria [see comments] Nature 396 133–140

    Article  PubMed  CAS  Google Scholar 

  • Antelmann, H., J. Bernhardt, R. Schmid, and M. Hecker. 1995 A gene at 333 degrees on the Bacillus subtilis chromosome encodes the newly identified sigma B-dependent general stress protein GspA J. Bacteriol. 177 3540–3545

    PubMed  CAS  Google Scholar 

  • Antelmann, H., J. Bernhardt, R. Schmid, H. Mach, U. Volker, and M. Hecker. 1997a First steps from a two-dimensional protein index towards a response-regulation map for Bacillus subtilis Electrophoresis 18 1451–1463

    Article  PubMed  CAS  Google Scholar 

  • Antelmann, H., S. Engelmann, R. Schmid, A. Sorokin, A. Lapidus, and M. Hecker. 1997b Expression of a stress-and starvation-induced dps/pexB-homologous gene is controlled by the alternative sigma factor sigmaB in Bacillus subtilis J. Bacteriol. 179 7251–7256

    PubMed  CAS  Google Scholar 

  • Babst, M., H. Hennecke, and H. M. Fischer. 1996 Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum Molec. Microbiol. 19 827–839

    Article  CAS  Google Scholar 

  • Baird, P. N., L. M. Hall, and A. R. Coates. 1989 Cloning and sequence analysis of the 10 kDa antigen gene of Mycobacterium tuberculosis J. Gen. Microbiol. 135(4) 931–939

    Google Scholar 

  • Bardwell, J. C., and E. A. Craig. 1984 Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous Proc. Natl. Acad. Sci. USA 81 848–852

    Article  PubMed  CAS  Google Scholar 

  • Bardwell, J. C., K. Tilly, E. Craig, J. King, M. Zylicz, and C. Georgopoulos. 1986 The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene: A gene that encodes a heat shock protein J. Biol. Chem. 261 1782–1785

    PubMed  CAS  Google Scholar 

  • Bardwell, J. C., and E. A. Craig. 1987 Eukaryotic Mr 83,000 heat shock protein has a homologue in Escherichia coli Proc. Natl. Acad. Sci. USA 84 5177–5181

    Article  PubMed  CAS  Google Scholar 

  • Becker, G., and R. Hengge-Aronis. 2001 What makes an Escherichia coli promoter sigma(S) dependent? Role of the-13/-14 nucleotide promoter positions and region 2.5 of sigma(S) Molec. Microbiol. 39 1153–1165

    Article  CAS  Google Scholar 

  • Bernhardt, J., U. Volker, A. Volker, H. Antelmann, R. Schmid, H. Mach, and M. Hecker. 1997 Specific and general stress proteins in Bacillus subtilis—a two-dimensional protein electrophoresis study Microbiology 143 999–1017

    Article  PubMed  CAS  Google Scholar 

  • Bernhardt, J., K. Buttner, C. Scharf, and M. Hecker. 1999 Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis Electrophoresis 20 2225–2240

    Article  PubMed  CAS  Google Scholar 

  • Biran, D., N. Brot, H. Weissbach, and E. Z. Ron. 1995 Heat shock-dependent transcriptional activation of the metA gene of Escherichia coli J. Bacteriol. 177 1374–1379

    PubMed  CAS  Google Scholar 

  • Boorstein, W. R., T. Ziegelhoffer, and E. A. Craig. 1994 Molecular evolution of the HSP70 multigene family J. Molec. Evol. 38 1–17

    Article  PubMed  CAS  Google Scholar 

  • Bouche, S., E. Klauck, D. Fischer, M. Lucassen, K. Jung, and R. Hengge-Aronis. 1998 Regulation of RssB-dependent proteolysis in Escherichia coli: A role for acetyl phosphate in a response regulator-controlled process Molec. Microbiol. 27 787–795

    Article  CAS  Google Scholar 

  • Bucca, G., G. Ferina, A. M. Puglia, and C. P. Smith. 1995 The dnaK operon of Streptomyces coelicolor encodes a novel heat-shock protein which binds to the promoter region of the operon Molec. Microbiol. 17 663–674

    Article  CAS  Google Scholar 

  • Bucca, G., Z. Hindle, and C. P. Smith. 1997 Regulation of the dnaK operon of Streptomyces coelicolor A3(2) is governed by HspR, an autoregulatory repressor protein J. Bacteriol. 179 5999–6004

    PubMed  CAS  Google Scholar 

  • Bucca, G., A. M. Brassington, H. J. Schonfeld, and C. P. Smith. 2000 The HspR regulon of Streptomyces coelicolor: A role for the DnaK chaperone as a transcriptional co-repressordagger Molec. Microbiol. 38 1093–103

    Article  CAS  Google Scholar 

  • Burgess, R. R., A. A. Travers, J. J. Dunn, and E. K. Bautz. 1969 Factor stimulating transcription by RNA polymerase Nature 221 43–46

    Article  PubMed  CAS  Google Scholar 

  • Burgess, R. R., and L. Anthony. 2001 How sigma docks to RNA polymerase and what sigma does Curr. Opin. Microbiol. 4 126–131

    Article  PubMed  CAS  Google Scholar 

  • Burton, Z., R. R. Burgess, J. Lin, D. Moore, S. Holder, and C. A. Gross. 1981 The nucleotide sequence of the cloned rpoD gene for the RNA polymerase sigma subunit from E coli K12 Nucleic Acids Res. 9 2889–2903

    Article  PubMed  CAS  Google Scholar 

  • Buttner, K., J. Bernhardt, C. Scharf, R. Schmid, U. Mader, C. Eymann, H. Antelmann, A. Volker, U. Volker, and M. Hecker. 2001 A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis Electrophoresis 22 2908–2935

    Article  PubMed  CAS  Google Scholar 

  • Christians, E. S., L. J. Yan, and I. J. Benjamin. 2002 Heat shock factor 1 and heat shock proteins: Critical partners in protection against acute cell injury Crit. Care Med. 30 S43–S50

    Article  CAS  Google Scholar 

  • Chuang, S. E., and F. R. Blattner. 1993a Characterization of twenty-six new heat shock genes of Escherichia coli J. Bacteriol. 175 5242–5252

    PubMed  CAS  Google Scholar 

  • Chuang, S. E., V. Burland, G. Plunkett, D. L. Daniels, and F. R. Blattner. 1993b Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli Gene 134 1–6

    Article  PubMed  CAS  Google Scholar 

  • Craig, E. A. 1985 The heat shock response CRC Crit. Rev. Biochem. 18 239–280

    Article  PubMed  CAS  Google Scholar 

  • Craig, E. A., and C. A. Gross. 1991 Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16 135–140

    Article  PubMed  CAS  Google Scholar 

  • Dartigalongue, C., and S. Raina. 1998 A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli EMBO J. 17 3968–3980

    Article  PubMed  CAS  Google Scholar 

  • De Las Penas, A., L. Connolly, and C. A. Gross. 1997 SigmaE is an essential sigma factor in Escherichia coli J. Bacteriol. 179 6862–6864

    Google Scholar 

  • Derre, I., G. Rapoport, K. Devine, M. Rose, and T. Msadek. 1999a ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis Molec. Microbiol. 32 581–593

    Article  CAS  Google Scholar 

  • Derre, I., G. Rapoport, and T. Msadek. 1999b CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria Molec. Microbiol. 31 117–131

    Article  CAS  Google Scholar 

  • Deuerling, E., A. Mogk, C. Richter, M. Purucker, and W. Schumann. 1997 The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion Molec. Microbiol. 23 921–933

    Article  CAS  Google Scholar 

  • Emetz, D., and G. Klug. 1998 Cloning and characterization of the rpoH gene of Rhodobacter capsulatus Molec. Gen. Genet. 260 212–217

    Article  PubMed  CAS  Google Scholar 

  • Engelmann, S., C. Lindner, and M. Hecker. 1995 Cloning, nucleotide sequence, and regulation of katE encoding a sigma B-dependent catalase in Bacillus subtilis J. Bacteriol. 177 5598–5605

    PubMed  CAS  Google Scholar 

  • Erickson, J. W., V. Vaughn, W. A. Walter, F. C. Neidhardt, and C. A. Gross. 1987 Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene Genes Dev. 1 419–432

    Article  PubMed  CAS  Google Scholar 

  • Erickson, J. W., and C. A. Gross. 1989 Identification of the sigma E subunit of Escherichia coli RNA polymerase: A second alternate sigma factor involved in high-temperature gene expression Genes Dev. 3 1462–1471

    Article  PubMed  CAS  Google Scholar 

  • Eymann, C., and M. Hecker. 2001 Induction of sigma(B)-dependent general stress genes by amino acid starvation in a spo0H mutant of Bacillus subtilis FEMS Microbiol. Lett. 199 221–227

    PubMed  CAS  Google Scholar 

  • Gaal, T., W. Ross, S. T. Estrem, L. H. Nguyen, R. R. Burgess, and R. L. Gourse. 2001 Promoter recognition and discrimination by EsigmaS RNA polymerase Molec. Microbiol. 42 939–954

    Article  CAS  Google Scholar 

  • Gamer, J., H. Bujard, and B. Bukau. 1992 Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32 Cell 69 833–842

    Article  PubMed  CAS  Google Scholar 

  • Gamer, J., G. Multhaup, T. Tomoyasu, J. S. McCarty, S. Rudiger, H. J. Schonfeld, C. Schirra, H. Bujard, and B. Bukau. 1996 A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor sigma32 EMBO J. 15 607–617

    PubMed  CAS  Google Scholar 

  • Gayda, R. C., P. E. Stephens, R. Hewick, J. M. Schoemaker, W. J. Dreyer, and A. Markovitz. 1985 Regulatory region of the heat shock-inducible capR (lon) gene: DNA and protein sequences J. Bacteriol. 162 271–275

    PubMed  CAS  Google Scholar 

  • Gerth, U., E. Kruger, I. Derre, 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 Molec. Microbiol. 28 787–802

    Article  CAS  Google Scholar 

  • Goldberg, A. L. 1972 Degradation of abnormal proteins in Escherichia coli (protein breakdown-protein structure-mistranslation-amino acid analogs-puromycin) Proc. Natl. Acad. Sci. USA 69 422–426

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gottesman, S. 1996 Proteases and their targets in Escherichia coli Ann. Rev. Genet. 30 465–506

    Article  PubMed  CAS  Google Scholar 

  • Grossman, A. D., J. W. Erickson, and C. A. Gross. 1984 The htpR gene product of E. coli is a sigma factor for heat-shock promoters Cell 38 383–390

    Article  PubMed  CAS  Google Scholar 

  • Gupta, R. S. 1995 Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells Molec. Microbiol. 15 1–11

    Article  CAS  Google Scholar 

  • Hatfield, G. W., S. P. Hung, and P. Baldi. 2003 Differential analysis of DNA microarray gene expression data Molec. Microbiol. 47 871–877

    Article  CAS  Google Scholar 

  • Hecker, M., W. Schumann, and U. Volker. 1996 Heat-shock and general stress response in Bacillus subtilis Molec. Microbiol. 19 417–428

    Article  CAS  Google Scholar 

  • Hecker, M., and U. Volker. 1998 Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the sigmaB regulon Molec. Microbiol. 29 1129–1136

    Article  CAS  Google Scholar 

  • Helmann, J. D., and M. J. Chamberlin. 1988 Structure and function of bacterial sigma factors Ann. Rev. Biochem. 57 839–872

    Article  PubMed  CAS  Google Scholar 

  • Helmann, J. D. 1999 Anti-sigma factors Curr. Opin. Microbiol. 2 135–141

    Article  PubMed  CAS  Google Scholar 

  • Hengge, R., and B. Bukau. 2003 Proteolysis in prokaryotes: Protein quality control and regulatory principles Molec. Microbiol. 49 1451–1462

    Article  CAS  Google Scholar 

  • Hengge-Aronis, R. 2000 The general stress response in Escherichia coli In: G. Storz and R. Hengge-Aronis (Eds.) Bacterial Stress Responses ASM Press Washington, DC 161–178

    Google Scholar 

  • Hengge-Aronis, R. 2002 Stationary phase gene regulation: What makes an Escherichia coli promoter sigmaS-selective? Curr. Opin. Microbiol. 5 591–595

    Article  PubMed  CAS  Google Scholar 

  • Herman, C., D. Thevenet, R. D’Ari, and P. Bouloc. 1995 Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB Proc. Natl. Acad. Sci. USA 92 3516–3520

    Article  PubMed  CAS  Google Scholar 

  • Huang, L. H., Y. H. Tseng, and M. T. Yang. 1998 Isolation and characterization of the Xanthomonas campestris rpoH gene coding for a 32-kDa heat shock sigma factor Biochem. Biophys. Res. Commun. 244 854–860

    Article  PubMed  CAS  Google Scholar 

  • Hughes, K. T., and K. Mathee. 1998 The anti-sigma factors Ann. Rev. Microbiol. 52 231–286

    Article  CAS  Google Scholar 

  • Humphreys, S., A. Stevenson, A. Bacon, A. B. Weinhardt, and M. Roberts. 1999 The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium Infect. Immun. 67 1560–1568

    PubMed  CAS  Google Scholar 

  • Inbar, O., and E. Z. Ron. 1993 Induction of cadmium tolerance in Escherichia coli K-12 FEMS Microbiol. Lett. 113 197–200

    Article  PubMed  CAS  Google Scholar 

  • Ishihama, A. 2000 Functional modulation of Escherichia coli RNA polymerase Ann. Rev. Microbiol. 54 499–518

    Article  CAS  Google Scholar 

  • Jovanovic, G., L. Weiner, and P. Model. 1996 Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon J. Bacteriol. 178 1936–1945

    PubMed  CAS  Google Scholar 

  • Kaan, T., B. Jurgen, and T. Schweder. 1999 Regulation of the expression of the cold shock proteins CspB and CspC in Bacillus subtilis Molec. Gen. Genet. 262 351–354

    Article  PubMed  CAS  Google Scholar 

  • Kallipolitis, B. H., and P. Valentin-Hansen. 1998 Transcription of rpoH, encoding the Escherichia coli heat-shock regulator sigma32, is negatively controlled by the cAMP-CRP/CytR nucleoprotein complex Molec. Microbiol. 29 1091–1099

    Article  CAS  Google Scholar 

  • Kandror, O., L. Busconi, M. Sherman, and A. L. Goldberg. 1994 Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES J. Biol. Chem. 269 23575–23582

    PubMed  CAS  Google Scholar 

  • Kanemori, M., K. Nishihara, H. Yanagi, and T. Yura. 1997 Synergistic roles of HslVU and other ATP-dependent proteases in controlling in vivo turnover of sigma32 and abnormal proteins in Escherichia coli J. Bacteriol. 179 7219–7225

    PubMed  CAS  Google Scholar 

  • Kanemori, M., H. Yanagi, and T. Yura. 1999 Marked instability of the sigma(32) heat shock transcription factor at high temperature. Implications for heat shock regulation J. Biol. Chem. 274 22002–22007

    Article  PubMed  CAS  Google Scholar 

  • Karls, R. K., J. Brooks, P. Rossmeissl, J. Luedke, and T. J. Donohue. 1998 Metabolic roles of a Rhodobacter sphaeroides member of the sigma32 family J. Bacteriol. 180 10–19

    PubMed  CAS  Google Scholar 

  • Kitagawa, M., C. Wada, S. Yoshioka, and T. Yura. 1991 Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32) J. Bacteriol. 173 4247–4253

    PubMed  CAS  Google Scholar 

  • Kornitzer, D., D. Teff, S. Altuvia, and A. B. Oppenheim. 1991 Isolation, characterization, and sequence of an Escherichia coli heat shock gene, htpX J. Bacteriol. 173 2944–2953

    PubMed  CAS  Google Scholar 

  • Kruger, E., U. Volker, and M. Hecker. 1994 Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance J. Bacteriol. 176 3360–3367

    PubMed  CAS  Google Scholar 

  • Kruger, E., T. Msadek, and M. Hecker. 1996 Alternate promoters direct stress-induced transcription of the Bacillus subtilis clpC operon Molec. Microbiol. 20 713–723

    Article  CAS  Google Scholar 

  • Kruger, E., and M. Hecker. 1998 The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes J. Bacteriol. 180 6681–6688

    PubMed  CAS  Google Scholar 

  • Landick, R., V. Vaughn, E. T. Lau, R. A. VanBogelen, J. W. Erickson, and F. C. Neidhardt. 1984 Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product may be a transcription factor Cell 38 175–182

    Article  PubMed  CAS  Google Scholar 

  • Lange, R., and R. Hengge-Aronis. 1991 Identification of a central regulator of stationary-phase gene expression in Escherichia coli Molec. Microbiol. 5 49–59

    Article  CAS  Google Scholar 

  • Lee, S. J., and J. D. Gralla. 2002 Promoter use by sigma 38 (rpoS) RNA polymerase: Amino acid clusters for DNA binding and isomerization J. Biol. Chem. 277 47420–47427

    Article  PubMed  CAS  Google Scholar 

  • Li, Z., A. Menoret, and P. Srivastava. 2002 Roles of heat-shock proteins in antigen presentation and cross-presentation Curr. Opin. Immunol. 14 45–51

    Article  PubMed  CAS  Google Scholar 

  • Liberek, K., T. P. Galitski, M. Zylicz, and C. Georgopoulos. 1992 The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the sigma 32 transcription factor Proc. Natl. Acad. Sci. USA 89 3516–3520

    Article  PubMed  CAS  Google Scholar 

  • Liberek, K., and C. Georgopoulos. 1993 Autoregulation of the Escherichia coli heat shock response by the DnaK and DnaJ heat shock proteins Proc. Natl. Acad. Sci. USA 90 11019–11023

    Article  PubMed  CAS  Google Scholar 

  • Lipinska, B., J. King, D. Ang, and C. Georgopoulos. 1988 Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein Nucleic Acids Res. 16 7545–7562

    Article  PubMed  CAS  Google Scholar 

  • Lonetto, M., M. Gribskov, and C. A. Gross. 1992 The sigma 70 family: Sequence conservation and evolutionary relationships J. Bacteriol. 174 3843–3849

    PubMed  CAS  Google Scholar 

  • Maul, B., U. Volker, S. Riethdorf, S. Engelmann, and M. Hecker. 1995 Sigma B-dependent regulation of gsiB in response to multiple stimuli in Bacillus subtilis Molec. Gen. Genet. 248 114–120

    Article  PubMed  CAS  Google Scholar 

  • Maurizi, M. R., W. P. Clark, Y. Katayama, S. Rudikoff, J. Pumphrey, B. Bowers, and S. Gottesman. 1990 Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli J. Biol. Chem. 265 12536–12545

    PubMed  CAS  Google Scholar 

  • Maurizi, M. R. 1992 Proteases and protein degradation in Escherichia coli Experientia 48 178–201

    Article  PubMed  CAS  Google Scholar 

  • Michaud, S., R. Marin, and R. M. Tanguay. 1997 Regulation of heat shock gene induction and expression during Drosophila development Cell. Molec. Life Sci. 53 104–113

    Article  PubMed  CAS  Google Scholar 

  • Missiakas, D., C. Georgopoulos, and S. Raina. 1993 The Escherichia coli heat shock gene htpY: Mutational analysis, cloning, sequencing, and transcriptional regulation J. Bacteriol. 175 2613–2624

    PubMed  CAS  Google Scholar 

  • Missiakas, D., and S. Raina. 1997 Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli: Role of two new phosphoprotein phosphatases PrpA and PrpB EMBO J. 16 1670–1685

    Article  PubMed  CAS  Google Scholar 

  • Mogk, A., G. Homuth, C. Scholz, L. Kim, F. X. Schmid, and W. Schumann. 1997 The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis EMBO J. 16 4579–4590

    Article  PubMed  CAS  Google Scholar 

  • Morita, M., M. Kanemori, H. Yanagi, and T. Yura. 1999 Heat-induced synthesis of sigma32 in Escherichia coli: Structural and functional dissection of rpoH mRNA secondary structure J. Bacteriol. 181 401–410

    PubMed  CAS  Google Scholar 

  • Morita, M. T., M. Kanemori, H. Yanagi, and T. Yura. 2000 Dynamic interplay between antagonistic pathways controlling the sigma 32 level in Escherichia coli Proc. Natl. Acad. Sci. USA 97 5860–5865

    Article  PubMed  CAS  Google Scholar 

  • Msadek, T., F. Kunst, and G. Rapoport. 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

    Article  PubMed  CAS  Google Scholar 

  • Mueller, J. P., G. Bukusoglu, and A. L. Sonenshein. 1992 Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: Control of gsiA by the ComP-ComA signal transduction system J. Bacteriol. 174 4361–4373

    PubMed  CAS  Google Scholar 

  • Munchbach, M., P. Dainese, W. Staudenmann, F. Narberhaus, and P. James. 1999a Proteome analysis of heat shock protein expression in Bradyrhizobium japonicum Eur. J. Biochem. 264 39–48

    Article  PubMed  CAS  Google Scholar 

  • Munchbach, M., A. Nocker, and F. Narberhaus. 1999b Multiple small heat shock proteins in rhizobia J. Bacteriol. 181 83–90

    PubMed  CAS  Google Scholar 

  • Nagai, H., R. Yano, J. W. Erickson, and T. Yura. 1990 Transcriptional regulation of the heat shock regulatory gene rpoH in Escherichia coli: Involvement of a novel catabolite-sensitive promoter J. Bacteriol. 172 2710–2715

    PubMed  CAS  Google Scholar 

  • Nagai, H., H. Yuzawa, and T. Yura. 1991 Interplay of two cis-acting mRNA regions in translational control of sigma 32 synthesis during the heat shock response of Escherichia coli Proc. Natl. Acad. Sci. USA 88 10515–10519

    Article  PubMed  CAS  Google Scholar 

  • Nair, S., I. Derre, T. Msadek, O. Gaillot, and P. Berche. 2000 CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes Molec. Microbiol. 35 800–811

    Article  CAS  Google Scholar 

  • Nakahigashi, K., H. Yanagi, and T. Yura. 1995 Isolation and sequence analysis of rpoH genes encoding sigma 32 homologs from Gram negative bacteria: Conserved mRNA and protein segments for heat shock regulation Nucleic Acids Res. 23 4383–4390

    PubMed  CAS  Google Scholar 

  • Nakahigashi, K., H. Yanagi, and T. Yura. 1998 Regulatory conservation and divergence of sigma32 homologs from Gram-negative bacteria: Serratia marcescens, Proteus mirabilis, Pseudomonas aeruginosa, and Agrobacterium tumefaciens J. Bacteriol. 180 2402–2408

    PubMed  CAS  Google Scholar 

  • Nakahigashi, K., E. Z. Ron, H. Yanagi, and T. Yura. 1999 Differential and independent roles of a sigma(32) homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens J. Bacteriol. 181 7509–7515

    PubMed  CAS  Google Scholar 

  • Nakahigashi, K., H. Yanagi, and T. Yura. 2001 DnaK chaperone-mediated control of activity of a sigma(32) homolog (RpoH) plays a major role in the heat shock response of Agrobacterium tumefaciens J. Bacteriol. 183 5302–5310

    Article  PubMed  CAS  Google Scholar 

  • Narberhaus, F., P. Krummenacher, H. M. Fischer, and H. Hennecke. 1997 Three disparately regulated genes for sigma 32-like transcription factors in Bradyrhizobium japonicum Molec. Microbiol. 24 93–104

    Article  CAS  Google Scholar 

  • Narberhaus, F., R. Kaser, A. Nocker, and H. Hennecke. 1998 A novel DNA element that controls bacterial heat shock gene expression Molec. Microbiol. 28 315–323

    Article  CAS  Google Scholar 

  • Narberhaus, F. 1999 Negative regulation of bacterial heat shock genes Molec. Microbiol. 31 1–8

    Article  CAS  Google Scholar 

  • Neidhardt, F. C., T. A. Phillips, R. A. VanBogelen, M. W. Smith, Y. Georgalis, and A. R. Subramanian. 1981 Identity of the B56.5 protein, the A-protein, and the groE gene product of Escherichia coli J. Bacteriol. 145 513–520

    PubMed  CAS  Google Scholar 

  • Nocker, A., N. P. Krstulovic, X. Perret, and F. Narberhaus. 2001 ROSE elements occur in disparate rhizobia and are functionally interchangeable between species Arch. Microbiol. 176 44–51

    Article  PubMed  CAS  Google Scholar 

  • O’Farrell, P. H. 1975 High resolution two-dimensional electrophoresis of proteins J. Biol. Chem. 250 4007–4021

    PubMed  Google Scholar 

  • Peake, P., N. Winter, and W. Britton. 1998 Phosphorylation of Mycobacterium leprae heat-shock 70 protein at threonine 175 alters its substrate binding characteristics Biochim. Biophys. Acta 1387 387–394

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pruteanu, M., and R. Hengge-Aronis. 2002 The cellular level of the recognition factor RssB is rate-limiting for sigmaS proteolysis: Implications for RssB regulation and signal transduction in sigmaS turnover in Escherichia coli Molec. Microbiol. 45 1701–1713

    Article  CAS  Google Scholar 

  • Raina, S., and C. Georgopoulos. 1990 A new Escherichia coli heat shock gene, htrC, whose product is essential for viability only at high temperatures J. Bacteriol. 172 3417–3426

    PubMed  CAS  Google Scholar 

  • Raina, S., and C. Georgopoulos. 1991 The htrM gene, whose product is essential for Escherichia coli viability only at elevated temperatures, is identical to the rfaD gene Nucleic Acids Res. 19 3811–3819

    Article  PubMed  CAS  Google Scholar 

  • Raina, S., D. Missiakas, and C. Georgopoulos. 1995 The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli EMBO J. 14 1043–1055

    PubMed  CAS  Google Scholar 

  • Repoila, F., N. Majdalani, and S. Gottesman. 2003 Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: The RpoS paradigm Molec. Microbiol. 48 855–861

    Article  CAS  Google Scholar 

  • Richmond, C. S., J. D. Glasner, R. Mau, H. Jin, and F. R. Blattner. 1999 Genome-wide expression profiling in Escherichia coli K-12 Nucleic Acids Res. 27 3821–3835

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ron, E. Z., G. Segal, M. Robinson, and D. Graur. 1999 Control elements in the regulation of bacterial heat shock response In: E. Rosenberg (Ed.) Microbial Ecology and Infectious Disease American Society for Microbiology Washington, DC 143–152

    Google Scholar 

  • Rose, J. K., and C. H. Rankin. 2001 Analyses of habituation in Caenorhabditis elegans Learn. Mem. 8 63–69

    Article  PubMed  CAS  Google Scholar 

  • Rosen, R., K. Buttner, R. Schmid, M. Hecker, and E. Z. Ron. 2001 Stress-induced proteins of Agrobacterium tumefaciens FEMS Microbiol. Ecol. 35 277–285

    Article  PubMed  CAS  Google Scholar 

  • Rosen, R., and E. Z. Ron. 2002a Proteome analysis in the study of the bacterial heat-shock response Mass Spectrom. Rev. 21 244–265

    Article  PubMed  CAS  Google Scholar 

  • Rosen, R., K. Buttner, D. Becher, K. Nakahigashi, T. Yura, M. Hecker, and E. Z. Ron. 2002b Heat shock proteome of Agrobacterium tumefaciens: Evidence for new control systems J. Bacteriol. 184 1772–1778

    Article  PubMed  CAS  Google Scholar 

  • Rosen, R., D. Becher, K. Buettner, D. Biran, M. Hecker, and E. Z. Ron. 2004 Highly phosphorylated bacterial proteins Proteomics 4(10) 3068–3077

    Article  CAS  Google Scholar 

  • Sahu, G. K., R. Chowdhury, and J. Das. 1997 The rpoH gene encoding sigma 32 homolog of Vibrio cholerae Gene 189 203–207

    Article  PubMed  CAS  Google Scholar 

  • Scharf, C., S. Riethdorf, H. Ernst, S. Engelmann, U. Volker, and M. Hecker. 1998 Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis J. Bacteriol. 180 1869–1877

    PubMed  CAS  Google Scholar 

  • Schulz, A., B. Tzschaschel, and W. Schumann. 1995 Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis Molec. Microbiol. 15 421–429

    Article  CAS  Google Scholar 

  • Schuster, M., A. C. Hawkins, C. S. Harwood, and E. P. Greenberg. 2004 The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing Molec. Microbiol. 51 973–985

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Segal, G., and E. Z. Ron. 1995a The dnaKJ operon of Agrobacterium tumefaciens: Transcriptional analysis and evidence for a new heat shock promoter J. Bacteriol. 177 5952–5958

    PubMed  CAS  Google Scholar 

  • Segal, G., and E. Z. Ron. 1995b The groESL operon of Agrobacterium tumefaciens: Evidence for heat shock-dependent mRNA cleavage J. Bacteriol. 177 750–757

    PubMed  CAS  Google Scholar 

  • Segal, G., and E. Z. Ron. 1996 Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat J. Bacteriol. 178 3634–3640

    PubMed  CAS  Google Scholar 

  • Segal, G., and E. Z. Ron. 1998 Regulation of heat-shock response in bacteria Ann. NY Acad. Sci. 851 147–151

    Article  PubMed  CAS  Google Scholar 

  • Segal, R., and E. Z. Ron. 1996 Regulation and organization of the groE and dnaK operons in Eubacteria FEMS Microbiol. Lett. 138 1–10

    Article  PubMed  CAS  Google Scholar 

  • Servant, P., and P. Mazodier. 1996 Heat induction of hsp18 gene expression in Streptomyces albus G: Transcriptional and posttranscriptional regulation J. Bacteriol. 178 7031–7036

    PubMed  CAS  Google Scholar 

  • Servant, P., G. Rapoport, and P. Mazodier. 1999 RheA, the repressor of hsp18 in Streptomyces albus G Microbiology 145 2385–2391

    PubMed  CAS  Google Scholar 

  • Severinov, K. 2000 RNA polymerase structure-function: Insights into points of transcriptional regulation Curr. Opin. Microbiol. 3 118–125

    Article  PubMed  CAS  Google Scholar 

  • Sherman, M., and A. L. Goldberg. 1992 Involvement of the chaperonin dnaK in the rapid degradation of a mutant protein in Escherichia coli EMBO J. 11 71–77

    PubMed  CAS  Google Scholar 

  • Sherman, M. Y., and A. L. Goldberg. 1996 Involvement of molecular chaperones in intracellular protein breakdown Exs 77 57–78

    PubMed  CAS  Google Scholar 

  • Sparrer, H., K. Rutkat, and J. Buchner. 1997 Catalysis of protein folding by symmetric chaperone complexes Proc. Natl. Acad. Sci. USA 94 1096–1100

    Article  PubMed  CAS  Google Scholar 

  • Srivastava, P. 2002 Roles of heat-shock proteins in innate and adaptive immunity Nature Rev. Immunol. 2 185–194

    Article  CAS  Google Scholar 

  • Strauch, K. L., K. Johnson, and J. Beckwith. 1989 Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature J. Bacteriol. 171 2689–2696

    PubMed  CAS  Google Scholar 

  • Straus, D. B., W. A. Walter, and C. A. Gross. 1987 The heat shock response of E. coli is regulated by changes in the concentration of sigma 32 Nature 329 348–351

    Article  PubMed  CAS  Google Scholar 

  • Straus, D. B., W. A. Walter, and C. A. Gross. 1989 The activity of sigma 32 is reduced under conditions of excess heat shock protein production in Escherichia coli Genes Dev. 3 2003–2010

    Article  PubMed  CAS  Google Scholar 

  • Straus, D., W. Walter, and C. A. Gross. 1990 DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32 Genes Dev. 4 2202–2209

    Article  PubMed  CAS  Google Scholar 

  • Studemann, A., M. Noirclerc-Savoye, E. Klauck, G. Becker, D. Schneider, and R. Hengge. 2003 Sequential recognition of two distinct sites in sigma(S) by the proteolytic targeting factor RssB and ClpX EMBO J. 22 4111–4120

    Article  PubMed  Google Scholar 

  • Taura, T., N. Kusukawa, T. Yura, and K. Ito. 1989 Transient shut off of Escherichia coli heat shock protein synthesis upon temperature shift down Biochem. Biophys. Res. Commun. 163 438–443

    Article  PubMed  CAS  Google Scholar 

  • Tilly, K., N. McKittrick, M. Zylicz, and C. Georgopoulos. 1983a The dnaK protein modulates the heat shock response of Escherichia coli Cell 34 641–646

    Article  PubMed  CAS  Google Scholar 

  • Tilly, K., R. A. VanBogelen, C. Georgopoulos, and F. C. Neidhardt. 1983b Identification of the heat-inducible protein C15.4 as the groES gene product in Escherichia coli J. Bacteriol. 154 1505–1507

    PubMed  CAS  Google Scholar 

  • Tilly, K., J. Spence, and C. Georgopoulos. 1989 Modulation of stability of the Escherichia coli heat shock regulatory factor sigma J. Bacteriol. 171 1585–1589

    PubMed  CAS  Google Scholar 

  • Tomoyasu, T., J. Gamer, B. Bukau, M. Kanemori, H. Mori, A. J. Rutman, A. B. Oppenheim, T. Yura, K. Yamanaka, and H. Niki. 1995 Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32 EMBO J. 14 2551–2560

    PubMed  CAS  Google Scholar 

  • Tomoyasu, T., A. Mogk, H. Langen, P. Goloubinoff, and B. Bukau. 2001 Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol Molec. Microbiol. 40 397–413

    Article  CAS  Google Scholar 

  • Ueki, T., and S. Inouye. 2002 Transcriptional activation of a heat-shock gene, lonD, of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system J. Biol. Chem. 277 6170–6177

    Article  PubMed  CAS  Google Scholar 

  • Van Asseldonk, M., A. Simons, H. Visser, W. M. de Vos, and G. Simons. 1993 Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene J. Bacteriol. 175 1637–1644

    PubMed  Google Scholar 

  • VanBogelen, R. A., M. A. Acton, and F. C. Neidhardt. 1987a Induction of the heat shock regulon does not produce thermotolerance in Escherichia coli Genes Dev. 1 525–531

    Article  PubMed  CAS  Google Scholar 

  • VanBogelen, R. A., P. M. Kelley, and F. C. Neidhardt. 1987b Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli J. Bacteriol. 169 26–32

    PubMed  CAS  Google Scholar 

  • Varon, D., S. A. Boylan, K. Okamoto, and C. W. Price. 1993 Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B J. Bacteriol. 175 3964–3971

    PubMed  CAS  Google Scholar 

  • Varon, D., M. S. Brody, and C. W. Price. 1996 Bacillus subtilis operon under the dual control of the general stress transcription factor sigma B and the sporulation transcription factor sigma H Molec. Microbiol. 20 339–350

    Article  CAS  Google Scholar 

  • Vicente, M., K. F. Chater, and V. De Lorenzo. 1999 Bacterial transcription factors involved in global regulation Molec. Microbiol. 33 8–17

    Article  CAS  Google Scholar 

  • Vogel, J., V. Bartels, T. H. Tang, G. Churakov, J. G. Slagter-Jager, A. Huttenhofer, and E. G. Wagner. 2003 RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria Nucleic Acids Res. 31 6435–6443

    Article  PubMed  CAS  Google Scholar 

  • Volker, U., S. Engelmann, B. Maul, S. Riethdorf, A. Volker, R. Schmid, H. Mach, and M. Hecker. 1994 Analysis of the induction of general stress proteins of Bacillus subtilis Microbiology 140(4) 741–752

    Article  Google Scholar 

  • Von Blohn, C., B. Kempf, R. M. Kappes, and E. Bremer. 1997 Osmostress response in Bacillus subtilis: Characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B Molec. Microbiol. 25 175–187

    Article  Google Scholar 

  • Wang, Q. P., and J. M. Kaguni. 1989 dnaA protein regulates transcriptions of the rpoH gene of Escherichia coli J. Biol. Chem. 264 7338–7344

    PubMed  CAS  Google Scholar 

  • Wassarman, K. M., and G. Storz. 2000 6S RNA regulates E. coli RNA polymerase activity Cell 101 613–623

    Article  PubMed  CAS  Google Scholar 

  • Wawrzynow, A., D. Wojtkowiak, J. Marszalek, B. Banecki, M. Jonsen, B. Graves, C. Georgopoulos, and M. Zylicz. 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

    PubMed  CAS  Google Scholar 

  • Yang, X., C. M. Kang, M. S. Brody, and C. W. Price. 1996 Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor Genes Dev. 10 2265–2275

    Article  PubMed  CAS  Google Scholar 

  • Yu, H., M. J. Schurr, and V. Deretic. 1995 Functional equivalence of Escherichia coli sigma E and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa J. Bacteriol. 177 3259–3268

    PubMed  CAS  Google Scholar 

  • Yuan, G., and S. L. Wong. 1995a 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

    PubMed  CAS  Google Scholar 

  • Yuan, G., and S. L. Wong. 1995b 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

    PubMed  CAS  Google Scholar 

  • Yura, T., T. Tobe, K. Ito, and T. Osawa. 1984 Heat shock regulatory gene (htpR) of Escherichia coli is required for growth at high temperature but is dispensable at low temperature Proc. Natl. Acad. Sci. USA 81 6803–6807

    Article  PubMed  CAS  Google Scholar 

  • Zhang, S., J. M. Scott, and W. G. Haldenwang. 2001 Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma(B) J. Bacteriol. 183 2316–2321

    Article  PubMed  CAS  Google Scholar 

  • Zhou, Y. N., N. Kusukawa, J. W. Erickson, C. A. Gross, and T. Yura. 1988 Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32 J. Bacteriol. 170 3640–3649

    PubMed  CAS  Google Scholar 

  • Zhou, Y., S. Gottesman, J. R. Hoskins, M. R. Maurizi, and S. Wickner. 2001 The RssB response regulator directly targets sigma(S) for degradation by ClpXP Genes Dev. 15 627–637

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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Authors
  1. Eliora Z. Ron
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Editors and Affiliations

  1. Department of Microbiology, University of Minnesota, Box 196, Twin Cities, Minneapolis, MN 55455-0312, USA

    Martin Dworkin Professor Dr. (Editor-in-Chief) (Editor-in-Chief)

  2. Department of Microbiology and Immunology, Stanford University Medical School, 299 Campus Drive, Fairchild, D039, Stanford, CA, 94305-5124, USA

    Stanley Falkow

  3. Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Ramat-Aviv, 69978, Israel

    Eugene Rosenberg

  4. Department of Microbiology, Technical University Munich, 80290, Munich, Germany

    Karl-Heinz Schleifer

  5. DSMZ- German Collection of Microorganisms and Cell Cultures GmbH, Mascheroder Weg 1b, 38124, Braunschweig, Germany

    Erko Stackebrandt

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Ron, E.Z. (2006). Bacterial Stress Response. In: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, KH., Stackebrandt, E. (eds) The Prokaryotes. Springer, New York, NY. https://doi.org/10.1007/0-387-30742-7_32

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