Bacterial Stress Response

  • Eliora Z. RonEmail author


Bacteria respond to stress by regulatory networks which modulate gene expression. These response mechanisms are essential for coping with the stress and for adapting to the new conditions. The regulation of the stress response involves several molecular pathways which control transcription, translation, and stability of transcripts and of proteins. These molecular responses are the topic of this chapter, which focuses on adaptation to upshift in temperature (heat-shock response) and to starvation-stationary conditions (general stress response).


Sigma Factor General Stress Response Nicotinamide Adenine Dinucleotide Phosphate Alternative Sigma Factor Severe Heat Shock 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Akbar S, Price CW (1996) Isolation and characterization of csbB, a gene controlled by Bacillus subtilis general stress transcription factor sigma B. Gene 177:123–128PubMedCrossRefGoogle Scholar
  2. Akbar S, Gaidenko TA, Kang CM, O’Reilly M, Devine KM, Price CW (2001) New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigma(B) of Bacillus subtilis. J Bacteriol 183:1329–1338PubMedCrossRefGoogle Scholar
  3. Alba BM, Gross CA (2004) Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol Microbiol 52:613–619PubMedCrossRefGoogle Scholar
  4. Allen SP, Polazzi JO, Gierse JK, Easton AM (1992) Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol 174:6938–6947PubMedGoogle Scholar
  5. Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140PubMedCrossRefGoogle Scholar
  6. Antelmann H, Bernhardt J, Schmid R, Hecker M (1995) A gene at 333 degrees on the Bacillus subtilis chromosome encodes the newly identified sigma B-dependent general stress protein GspA. J Bacteriol 177:3540–3545PubMedGoogle Scholar
  7. Antelmann H, Bernhardt J, Schmid R, Mach H, Volker U, Hecker M (1997a) First steps from a two-dimensional protein index towards a response-regulation map for Bacillus subtilis. Electrophoresis 18:1451–1463PubMedCrossRefGoogle Scholar
  8. Antelmann H, Engelmann S, Schmid R, Sorokin A, Lapidus A, Hecker M (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 179:7251–7256PubMedGoogle Scholar
  9. Babst M, Hennecke H, Fischer HM (1996) Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol Microbiol 19:827–839PubMedCrossRefGoogle Scholar
  10. Baird PN, Hall LM, Coates AR (1989) Cloning and sequence analysis of the 10 kDa antigen gene of Mycobacterium tuberculosis. J Gen Microbiol 135(Pt 4):931–939PubMedGoogle Scholar
  11. Bardwell JC, Craig EA (1984) Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci USA 81:848–852PubMedCrossRefGoogle Scholar
  12. Bardwell JC, Craig EA (1987) Eukaryotic Mr 83,000 heat shock protein has a homologue in Escherichia coli. Proc Natl Acad Sci USA 84:5177–5181PubMedCrossRefGoogle Scholar
  13. Bardwell JC, Tilly K, Craig E, King J, Zylicz M, Georgopoulos C (1986) The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene. A gene that encodes a heat shock protein. J Biol Chem 261:1782–1785PubMedGoogle Scholar
  14. Basineni SR, Madhugiri R, Kolmsee T, Hengge R, Klug G (2009) The influence of Hfq and ribonucleases on the stability of the small non-coding RNA OxyS and its target rpoS in E. coli is growth phase dependent. RNA Biol 6:584–594PubMedCrossRefGoogle Scholar
  15. Bernhardt J, Volker U, Volker A, Antelmann H, Schmid R, Mach H, Hecker M (1997) Specific and general stress proteins in Bacillus subtilis–a two-dimensional protein electrophoresis study. Microbiology 143:999–1017PubMedCrossRefGoogle Scholar
  16. Bernhardt J, Buttner K, Scharf C, Hecker M (1999) Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 20:2225–2240PubMedCrossRefGoogle Scholar
  17. Biran D, Brot N, Weissbach H, Ron EZ (1995) Heat shock-dependent transcriptional activation of the metA gene of Escherichia coli. J Bacteriol 177:1374–1379PubMedGoogle Scholar
  18. Boorstein WR, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evol 38:1–17PubMedCrossRefGoogle Scholar
  19. Bouche S, Klauck E, Fischer D, Lucassen M, Jung K, Hengge-Aronis R (1998) Regulation of RssB-dependent proteolysis in Escherichia coli: a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol 27:787–795PubMedCrossRefGoogle Scholar
  20. Bucca G, Ferina G, Puglia AM, Smith CP (1995) The dnaK operon of Streptomyces coelicolor encodes a novel heat-shock protein which binds to the promoter region of the operon. Mol Microbiol 17:663–674PubMedCrossRefGoogle Scholar
  21. Bucca G, Hindle Z, Smith CP (1997) Regulation of the dnaK operon of Streptomyces coelicolor A3(2) is governed by HspR, an autoregulatory repressor protein. J Bacteriol 179:5999–6004PubMedGoogle Scholar
  22. Bucca G, Brassington AM, Schonfeld HJ, Smith CP (2000) The HspR regulon of Streptomyces coelicolor: a role for the DnaK chaperone as a transcriptional co-repressordagger. Mol Microbiol 38:1093–1103PubMedCrossRefGoogle Scholar
  23. Bugl H, Fauman EB, Staker BL, Zheng F, Kushner SR, Saper MA, Bardwell JC, Jakob U (2000) RNA methylation under heat shock control. Mol Cell 6:349–360PubMedCrossRefGoogle Scholar
  24. Burgess RR, Anthony L (2001) How sigma docks to RNA polymerase and what sigma does. Curr Opin Microbiol 4:126–131PubMedCrossRefGoogle Scholar
  25. Burgess RR, Travers AA, Dunn JJ, Bautz EK (1969) Factor stimulating transcription by RNA polymerase. Nature 221:43–46PubMedCrossRefGoogle Scholar
  26. Burton Z, Burgess RR, Lin J, Moore D, Holder S, Gross CA (1981) The nucleotide sequence of the cloned rpoD gene for the RNA polymerase sigma subunit from E coli K12. Nucleic Acids Res 9:2889–2903PubMedCrossRefGoogle Scholar
  27. Buttner K, Bernhardt J, Scharf C, Schmid R, Mader U, Eymann C, Antelmann H, Volker A, Volker U, Hecker M (2001) A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis. Electrophoresis 22:2908–2935PubMedCrossRefGoogle Scholar
  28. Caldas T, Binet E, Bouloc P, Costa A, Desgres J, Richarme G (2000a) The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23S ribosomal RNA methyltransferase. J Biol Chem 275:16414–16419PubMedCrossRefGoogle Scholar
  29. Caldas T, Binet E, Bouloc P, Richarme G (2000b) Translational defects of Escherichia coli mutants deficient in the Um(2552) 23S ribosomal RNA methyltransferase RrmJ/FTSJ. Biochem Biophys Res Commun 271:714–718PubMedCrossRefGoogle Scholar
  30. Caron MP, Lafontaine DA, Masse E (2010) Small RNA-mediated regulation at the level of transcript stability. RNA Biol 7:140–144PubMedCrossRefGoogle Scholar
  31. Chuang SE, Blattner FR (1993) Characterization of twenty-six new heat shock genes of Escherichia coli. J Bacteriol 175:5242–5252PubMedGoogle Scholar
  32. Craig EA (1985) The heat shock response. CRC Crit Rev Biochem 18:239–280PubMedCrossRefGoogle Scholar
  33. Craig EA, Gross CA (1991) Is hsp70 the cellular thermometer? Trends Biochem Sci 16:135–140PubMedCrossRefGoogle Scholar
  34. Dartigalongue C, Raina S (1998) A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J 17:3968–3980PubMedCrossRefGoogle Scholar
  35. De Las Penas A, Connolly L, Gross CA (1997) SigmaE is an essential sigma factor in Escherichia coli. J Bacteriol 179:6862–6864PubMedGoogle Scholar
  36. Derre I, Rapoport G, Devine K, Rose M, Msadek T (1999a) ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol Microbiol 32:581–593PubMedCrossRefGoogle Scholar
  37. Derre I, Rapoport G, Msadek T (1999b) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol Microbiol 31:117–131PubMedCrossRefGoogle Scholar
  38. Deuerling E, Mogk A, Richter C, Purucker M, Schumann W (1997) The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol 23:921–933PubMedCrossRefGoogle Scholar
  39. Emetz D, Klug G (1998) Cloning and characterization of the rpoH gene of Rhodobacter capsulatus. Mol Gen Genet 260:212–217PubMedCrossRefGoogle Scholar
  40. Engelmann S, Lindner C, Hecker M (1995) Cloning, nucleotide sequence, and regulation of katE encoding a sigma B-dependent catalase in Bacillus subtilis. J Bacteriol 177:5598–5605PubMedGoogle Scholar
  41. Erickson JW, Gross CA (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 3:1462–1471PubMedCrossRefGoogle Scholar
  42. Erickson JW, Vaughn V, Walter WA, Neidhardt FC, Gross CA (1987) Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene. Genes Dev 1:419–432PubMedCrossRefGoogle Scholar
  43. Eymann C, Hecker M (2001) Induction of sigma(B)-dependent general stress genes by amino acid starvation in a spo0H mutant of Bacillus subtilis. FEMS Microbiol Lett 199:221–227PubMedGoogle Scholar
  44. Frohlich KS, Vogel J (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12:674–682PubMedCrossRefGoogle Scholar
  45. Gamer J, Bujard H, Bukau B (1992) Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell 69:833–842PubMedCrossRefGoogle Scholar
  46. Gamer J, Multhaup G, Tomoyasu T, McCarty JS, Rudiger S, Schonfeld HJ, Schirra C, Bujard H, Bukau B (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 15:607–617PubMedGoogle Scholar
  47. Gayda RC, Stephens PE, Hewick R, Schoemaker JM, Dreyer WJ, Markovitz A (1985) Regulatory region of the heat shock-inducible capR (lon) gene: DNA and protein sequences. J Bacteriol 162:271–275PubMedGoogle Scholar
  48. 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 28:787–802PubMedCrossRefGoogle Scholar
  49. Goldberg AL (1972) Degradation of abnormal proteins in Escherichia coli (protein breakdown- protein structure-mistranslation-amino acid analogs-puromycin). Proc Natl Acad Sci USA 69:422–426PubMedCrossRefGoogle Scholar
  50. Gottesman S (1989) Genetics of proteolysis in Escherichia coli. Annu Rev Genet 23:163–198PubMedCrossRefGoogle Scholar
  51. Gottesman S (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30:465–506PubMedCrossRefGoogle Scholar
  52. Gottesman S, Clark WP, de Crecy-Lagard V, Maurizi MR (1993) ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J Biol Chem 268:22618–22626PubMedGoogle Scholar
  53. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J, Thompson KM, FitzGerald PC, Sowa NA, FitzGerald DJ (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71:1–11PubMedCrossRefGoogle Scholar
  54. Grossman AD, Erickson JW, Gross CA (1984) The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38:383–390PubMedCrossRefGoogle Scholar
  55. Gupta RS (1995) Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 15:1–11PubMedCrossRefGoogle Scholar
  56. Gur E, Biran D, Ron EZ (2011) Regulated proteolysis in gram-negative bacteria–how and when? Nat Rev Microbiol 9:839–848PubMedCrossRefGoogle Scholar
  57. Hatfield GW, Hung SP, Baldi P (2003) Differential analysis of DNA microarray gene expression data. Mol Microbiol 47:871–877PubMedCrossRefGoogle Scholar
  58. Hecker M, Volker U (1990) General stress proteins in Bacillus subtilis. FEMS Microbiol Ecol 74:197–214CrossRefGoogle Scholar
  59. Hecker M, Volker U (1998) Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the sigmaB regulon. Mol Microbiol 29:1129–1136PubMedCrossRefGoogle Scholar
  60. Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417–428PubMedCrossRefGoogle Scholar
  61. Helmann JD (1999) Anti-sigma factors. Curr Opin Microbiol 2:135–141PubMedCrossRefGoogle Scholar
  62. Helmann JD, Chamberlin MJ (1988) Structure and function of bacterial sigma factors. Annu Rev Biochem 57:839–872PubMedCrossRefGoogle Scholar
  63. Hengge R (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160:667–676PubMedCrossRefGoogle Scholar
  64. Hengge-Aronis R (2000) The general stress response in Escherichia coli. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington, DC, pp 161–178Google Scholar
  65. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395, table of contentsPubMedCrossRefGoogle Scholar
  66. Henkin TM (2009) RNA-dependent RNA switches in bacteria. Methods Mol Biol 540:207–214PubMedCrossRefGoogle Scholar
  67. Herman C, Lecat S, D’Ari R, Bouloc P (1995a) Regulation of the heat-shock response depends on divalent metal ions in an hflB mutant of Escherichia coli. Mol Microbiol 18:247–255PubMedCrossRefGoogle Scholar
  68. Herman C, Thevenet D, D’Ari R, Bouloc P (1995b) Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc Natl Acad Sci USA 92:3516–3520PubMedCrossRefGoogle Scholar
  69. Huang LH, Tseng YH, Yang MT (1998) Isolation and characterization of the Xanthomonas campestris rpoH gene coding for a 32-kDa heat shock sigma factor. Biochem Biophys Res Commun 244:854–860PubMedCrossRefGoogle Scholar
  70. Hughes KT, Mathee K (1998) The anti-sigma factors. Annu Rev Microbiol 52:231–286PubMedCrossRefGoogle Scholar
  71. Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M (1999) The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67:1560–1568PubMedGoogle Scholar
  72. Inbar O, Ron EZ (1993) Induction of cadmium tolerance in Escherichia coli K-12. FEMS Lett 113:197–200CrossRefGoogle Scholar
  73. Ishihama A (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54:499–518PubMedCrossRefGoogle Scholar
  74. Jenal U, Hengge-Aronis R (2003) Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 6:163–172PubMedCrossRefGoogle Scholar
  75. Jovanovic G, Weiner L, Model P (1996) Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J Bacteriol 178:1936–1945PubMedGoogle Scholar
  76. Kaan T, Jurgen B, Schweder T (1999) Regulation of the expression of the cold shock proteins CspB and CspC in Bacillus subtilis. Mol Gen Genet 262:351–354PubMedCrossRefGoogle Scholar
  77. Kallipolitis BH, Valentin-Hansen P (1998) Transcription of rpoH, encoding the Escherichia coli heat-shock regulator sigma32, is negatively controlled by the cAMP-CRP/CytR nucleoprotein complex. Mol Microbiol 29:1091–1099PubMedCrossRefGoogle Scholar
  78. Kandror O, Busconi L, Sherman M, Goldberg AL (1994) Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES. J Biol Chem 269:23575–23582PubMedGoogle Scholar
  79. Kanemori M, Nishihara K, Yanagi H, Yura T (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 179:7219–7225PubMedGoogle Scholar
  80. Kanemori M, Yanagi H, Yura T (1999) The ATP-dependent HslVU/ClpQY protease participates in turnover of cell division inhibitor SulA in Escherichia coli. J Bacteriol 181:3674–3680PubMedGoogle Scholar
  81. Karls RK, Brooks J, Rossmeissl P, Luedke J, Donohue TJ (1998) Metabolic roles of a Rhodobacter sphaeroides member of the sigma32 family. J Bacteriol 180:10–19PubMedGoogle Scholar
  82. Kitagawa M, Wada C, Yoshioka S, Yura T (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 173:4247–4253PubMedGoogle Scholar
  83. Klauck E, Typas A, Hengge R (2007) The sigmaS subunit of RNA polymerase as a signal integrator and network master regulator in the general stress response in Escherichia coli. Sci Prog 90:103–127PubMedGoogle Scholar
  84. Klinkert B, Narberhaus F (2009) Microbial thermosensors. Cell Mol Life Sci 66:2661–2676PubMedCrossRefGoogle Scholar
  85. Korber P, Zander T, Herschlag D, Bardwell JC (1999) A new heat shock protein that binds nucleic acids. J Biol Chem 274:249–256PubMedCrossRefGoogle Scholar
  86. Korber P, Stahl JM, Nierhaus KH, Bardwell JC (2000) Hsp15: a ribosome-associated heat shock protein. EMBO J 19:741–748PubMedCrossRefGoogle Scholar
  87. Kornitzer D, Teff D, Altuvia S, Oppenheim AB (1991) Isolation, characterization, and sequence of an Escherichia coli heat shock gene, htpX. J Bacteriol 173:2944–2953PubMedGoogle Scholar
  88. Kruger E, Hecker M (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 180:6681–6688PubMedGoogle Scholar
  89. Kruger E, Volker U, Hecker M (1994) Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J Bacteriol 176:3360–3367PubMedGoogle Scholar
  90. Kruger E, Msadek T, Hecker M (1996) Alternate promoters direct stress-induced transcription of the Bacillus subtilis clpC operon. Mol Microbiol 20:713–723PubMedCrossRefGoogle Scholar
  91. Landick R, Vaughn V, Lau ET, VanBogelen RA, Erickson JW, Neidhardt FC (1984) Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product may be a transcription factor. Cell 38:175–182PubMedCrossRefGoogle Scholar
  92. Lange R, Hengge-Aronis R (1991) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5:49–59PubMedCrossRefGoogle Scholar
  93. Liberek K, Georgopoulos C (1993) Autoregulation of the Escherichia coli heat shock response by the DnaK and DnaJ heat shock proteins. Proc Natl Acad Sci USA 90:11019–11023PubMedCrossRefGoogle Scholar
  94. Liberek K, Galitski TP, Zylicz M, Georgopoulos C (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 89:3516–3520PubMedCrossRefGoogle Scholar
  95. Lipinska B, Sharma S, Georgopoulos C (1988) Sequence analysis and regulation of the htrA gene of Escherichia coli: a sigma 32-independent mechanism of heat-inducible transcription. Nucleic Acids Res 16:10053–10067PubMedCrossRefGoogle Scholar
  96. Lomakin IB, Shirokikh NE, Yusupov MM, Hellen CU, Pestova TV (2006) The fidelity of translation initiation: reciprocal activities of eIF1, IF3 and YciH. EMBO J 25:196–210PubMedCrossRefGoogle Scholar
  97. Lonetto M, Gribskov M, Gross CA (1992) The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849PubMedGoogle Scholar
  98. Maul B, Volker U, Riethdorf S, Engelmann S, Hecker M (1995) Sigma B-dependent regulation of gsiB in response to multiple stimuli in Bacillus subtilis. Mol Gen Genet 248:114–120PubMedCrossRefGoogle Scholar
  99. Maurizi MR (1992) Proteases and protein degradation in Escherichia coli. Experientia 48:178–201PubMedCrossRefGoogle Scholar
  100. Maurizi MR, Clark WP, Katayama Y, Rudikoff S, Pumphrey J, Bowers B, Gottesman S (1990a) Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265:12536–12545PubMedGoogle Scholar
  101. Maurizi MR, Clark WP, Kim SH, Gottesman S (1990b) Clp P represents a unique family of serine proteases. J Biol Chem 265:12546–12552PubMedGoogle Scholar
  102. Michaud S, Marin R, Tanguay RM (1997) Regulation of heat shock gene induction and expression during Drosophila development. Cell Mol Life Sci 53:104–113PubMedCrossRefGoogle Scholar
  103. Missiakas D, Georgopoulos C, Raina S (1993) The Escherichia coli heat shock gene htpY: mutational analysis, cloning, sequencing, and transcriptional regulation. J Bacteriol 175:2613–2624PubMedGoogle Scholar
  104. Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W (1997) The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J 16:4579–4590PubMedCrossRefGoogle Scholar
  105. Morita M, Kanemori M, Yanagi H, Yura T (1999a) Heat-induced synthesis of sigma32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J Bacteriol 181:401–410PubMedGoogle Scholar
  106. Morita MT, Tanaka Y, Kodama TS, Kyogoku Y, Yanagi H, Yura T (1999b) Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. Genes Dev 13:655–665PubMedCrossRefGoogle Scholar
  107. Morita MT, Kanemori M, Yanagi H, Yura T (2000) Dynamic interplay between antagonistic pathways controlling the sigma 32 level in Escherichia coli. Proc Natl Acad Sci USA 97:5860–5865PubMedCrossRefGoogle Scholar
  108. Msadek T, Kunst F, 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 91:5788–5792PubMedCrossRefGoogle Scholar
  109. Mueller JP, Bukusoglu G, Sonenshein AL (1992) Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol 174:4361–4373PubMedGoogle Scholar
  110. Mujacic M, Bader MW, Baneyx F (2004) Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK-DnaJ-GrpE system in the management of protein misfolding under severe stress conditions. Mol Microbiol 51:849–859PubMedCrossRefGoogle Scholar
  111. Munchbach M, Dainese P, Staudenmann W, Narberhaus F, James P (1999a) Proteome analysis of heat shock protein expression in Bradyrhizobium japonicum. Eur J Biochem 264:39–48PubMedCrossRefGoogle Scholar
  112. Munchbach M, Nocker A, Narberhaus F (1999b) Multiple small heat shock proteins in rhizobia. J Bacteriol 181:83–90PubMedGoogle Scholar
  113. Nagai H, Yano R, Erickson JW, Yura T (1990) Transcriptional regulation of the heat shock regulatory gene rpoH in Escherichia coli: involvement of a novel catabolite-sensitive promoter. J Bacteriol 172:2710–2715PubMedGoogle Scholar
  114. Nagai H, Yuzawa H, Yura T (1991a) 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 88:10515–10519PubMedCrossRefGoogle Scholar
  115. Nagai H, Yuzawa H, Yura T (1991b) Regulation of the heat shock response in E coli: involvement of positive and negative cis-acting elements in translation control of sigma 32 synthesis. Biochimie 73:1473–1479PubMedCrossRefGoogle Scholar
  116. Nair S, Derre I, Msadek T, Gaillot O, Berche P (2000) CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol Microbiol 35:800–811PubMedCrossRefGoogle Scholar
  117. Nakahigashi K, Yanagi H, Yura T (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 23:4383–4390PubMedGoogle Scholar
  118. Nakahigashi K, Yanagi H, Yura T (1998) Regulatory conservation and divergence of sigma32 homologs from gram- negative bacteria: Serratia marcescens, Proteus mirabilis, Pseudomonas aeruginosa, and Agrobacterium tumefaciens. J Bacteriol 180:2402–2408PubMedGoogle Scholar
  119. Nakahigashi K, Ron EZ, Yanagi H, Yura T (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 181:7509–7515PubMedGoogle Scholar
  120. Nakahigashi K, Yanagi H, Yura T (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 183:5302–5310PubMedCrossRefGoogle Scholar
  121. Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8PubMedCrossRefGoogle Scholar
  122. Narberhaus F, Krummenacher P, Fischer HM, Hennecke H (1997) Three disparately regulated genes for sigma 32-like transcription factors in Bradyrhizobium japonicum. Mol Microbiol 24:93–104PubMedCrossRefGoogle Scholar
  123. Narberhaus F, Kaser R, Nocker A, Hennecke H (1998) A novel DNA element that controls bacterial heat shock gene expression. Mol Microbiol 28:315–323PubMedCrossRefGoogle Scholar
  124. Narberhaus F, Obrist M, Fuehrer F, Langklotz S (2009) Degradation of cytoplasmic substrates by FtsH, a membrane-anchored protease with many talents. Res Microbiol 160(9):652–659PubMedCrossRefGoogle Scholar
  125. Neidhardt FC, Phillips TA, VanBogelen RA, Smith MW, Georgalis Y, Subramanian AR (1981) Identity of the B56.5 protein, the A-protein, and the groE gene product of Escherichia coli. J Bacteriol 145:513–520PubMedGoogle Scholar
  126. Nocker A, Hausherr T, Balsiger S, Krstulovic NP, Hennecke H, Narberhaus F (2001a) A mRNA-based thermosensor controls expression of rhizobial heat shock genes. Nucleic Acids Res 29:4800–4807PubMedCrossRefGoogle Scholar
  127. Nocker A, Krstulovic NP, Perret X, Narberhaus F (2001b) ROSE elements occur in disparate rhizobia and are functionally interchangeable between species. Arch Microbiol 176:44–51PubMedCrossRefGoogle Scholar
  128. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedGoogle Scholar
  129. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74:139–158PubMedCrossRefGoogle Scholar
  130. Peake P, Winter N, Britton W (1998) Phosphorylation of Mycobacterium leprae heat-shock 70 protein at threonine 175 alters its substrate binding characteristics. Biochim Biophys Acta 1387:387–394PubMedCrossRefGoogle Scholar
  131. Petersohn A, Brigulla M, Haas S, Hoheisel JD, Volker U, Hecker M (2001) Global analysis of the general stress response of Bacillus subtilis. J Bacteriol 183:5617–5631PubMedCrossRefGoogle Scholar
  132. Podkaminski D, Vogel J (2010) Small RNAs promote mRNA stability to activate the synthesis of virulence factors. Mol Microbiol 78:1327–1331PubMedCrossRefGoogle Scholar
  133. Pruteanu M, Hengge-Aronis R (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. Mol Microbiol 45:1701–1713PubMedCrossRefGoogle Scholar
  134. Raina S, Georgopoulos C (1990) A new Escherichia coli heat shock gene, htrC, whose product is essential for viability only at high temperatures. J Bacteriol 172:3417–3426PubMedGoogle Scholar
  135. Raina S, Georgopoulos C (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 19:3811–3819PubMedCrossRefGoogle Scholar
  136. Raina S, Missiakas D, Georgopoulos C (1995) The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. EMBO J 14:1043–1055PubMedGoogle Scholar
  137. Rasouly A, Shenhar Y, Ron EZ (2007) Thermoregulation of Escherichia coli hchA transcript stability. J Bacteriol 189:5779–5781PubMedCrossRefGoogle Scholar
  138. Rene O, Alix JH (2011) Late steps of ribosome assembly in E. coli are sensitive to a severe heat stress but are assisted by the HSP70 chaperone machine. Nucleic Acids Res 39:1855–1867PubMedCrossRefGoogle Scholar
  139. Richmond CS, Glasner JD, Mau R, Jin H, Blattner FR (1999) Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res 27:3821–3835PubMedCrossRefGoogle Scholar
  140. Roberts RC, Toochinda C, Avedissian M, Baldini RL, Gomes SL, Shapiro L (1996) Identification of a Caulobacter crescentus operon encoding hrcA, involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE. J Bacteriol 178:1829–1841PubMedGoogle Scholar
  141. Ron EZ, Segal G, Robinson M, Graur D (1999) Control elements in the regulation of bacterial heat shock response. In: Rosenberg E (ed) Microbial ecology and infectious disease. ASM Press, Washington, DCGoogle Scholar
  142. Rose JK, Rankin CH (2001) Analyses of habituation in Caenorhabditis elegans. Learn Mem 8:63–69PubMedCrossRefGoogle Scholar
  143. Rosen R, Ron EZ (2002) Proteome analysis in the study of the bacterial heat-shock response. Mass Spectrom Rev 21:244–265PubMedCrossRefGoogle Scholar
  144. Rosen R, Buttner K, Schmid R, Hecker M, Ron EZ (2001) Stress-induced proteins of Agrobacterium tumefaciens. FEMS Microbiol Ecol 35:277–285PubMedCrossRefGoogle Scholar
  145. Rosen R, Buttner K, Becher D, Nakahigashi K, Yura T, Hecker M, Ron EZ (2002) Heat shock proteome of Agrobacterium tumefaciens: evidence for new control systems. J Bacteriol 184:1772–1778PubMedCrossRefGoogle Scholar
  146. Rosen R, Becher D, Buttner K, Biran D, Hecker M, Ron EZ (2004) Highly phosphorylated bacterial proteins. Proteomics 4:3068–3077PubMedCrossRefGoogle Scholar
  147. Sahu GK, Chowdhury R, Das J (1997) The rpoH gene encoding sigma 32 homolog of Vibrio cholerae. Gene 189:203–207PubMedCrossRefGoogle Scholar
  148. Sastry MS, Korotkov K, Brodsky Y, Baneyx F (2002) Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J Biol Chem 277:46026–46034PubMedCrossRefGoogle Scholar
  149. Scharf C, Riethdorf S, Ernst H, Engelmann S, Volker U, Hecker M (1998) Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J Bacteriol 180:1869–1877PubMedGoogle Scholar
  150. Schmidt R, Bukau B, Mogk A (2009) Principles of general and regulatory proteolysis by AAA+ proteases in Escherichia coli. Res Microbiol 160:629–636PubMedCrossRefGoogle Scholar
  151. Schulz A, Tzschaschel B, Schumann W (1995) Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol Microbiol 15:421–429PubMedCrossRefGoogle Scholar
  152. Schuster M, Hawkins AC, Harwood CS, Greenberg EP (2004) The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol Microbiol 51:973–985PubMedCrossRefGoogle Scholar
  153. Segal G, Ron EZ (1993) Heat shock transcription of the groESL operon of Agrobacterium tumefaciens may involve a hairpin-loop structure. J Bacteriol 175:3083–3088PubMedGoogle Scholar
  154. Segal G, Ron EZ (1995a) The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J Bacteriol 177:5952–5958PubMedGoogle Scholar
  155. Segal G, Ron EZ (1995b) The groESL operon of Agrobacterium tumefaciens: evidence for heat shock-dependent mRNA cleavage. J Bacteriol 177:750–757PubMedGoogle Scholar
  156. Segal G, Ron EZ (1996a) Heat shock activation of the groESL operon of Agrobacterium tumefaciens and the regulatory roles of the inverted repeat. J Bacteriol 178:3634–3640PubMedGoogle Scholar
  157. Segal R, Ron EZ (1996b) Regulation and organization of the groE and dnaK operons in Eubacteria. FEMS Microbiol Lett 138:1–10PubMedCrossRefGoogle Scholar
  158. Segal G, Ron EZ (1998) Regulation of heat-shock response in bacteria. Ann N Y Acad Sci 851:147–151PubMedCrossRefGoogle Scholar
  159. Servant P, Mazodier P (1996) Heat induction of hsp18 gene expression in Streptomyces albus G: transcriptional and posttranscriptional regulation. J Bacteriol 178:7031–7036PubMedGoogle Scholar
  160. Servant P, Rapoport G, Mazodier P (1999) RheA, the repressor of hsp18 in Streptomyces albus G. Microbiology 145:2385–2391PubMedGoogle Scholar
  161. Severinov K (2000) RNA polymerase structure-function: insights into points of transcriptional regulation. Curr Opin Microbiol 3:118–125PubMedCrossRefGoogle Scholar
  162. Shenhar Y, Rasouly A, Biran D, Ron EZ (2009) Adaptation of Escherichia coli to elevated temperatures involves a change in stability of heat shock gene transcripts. Environ Microbiol 11:2989–2997PubMedCrossRefGoogle Scholar
  163. Sherman M, Goldberg AL (1992) Involvement of the chaperonin dnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO J 11:71–77PubMedGoogle Scholar
  164. Sherman MY, Goldberg AL (1996) Involvement of molecular chaperones in intracellular protein breakdown. EXS 77:57–78PubMedGoogle Scholar
  165. Singh SS, Typas A, Hengge R, Grainger DC (2011) Escherichia coli sigma senses sequence and conformation of the promoter spacer region. Nucleic Acids Res 39:5109–5118PubMedCrossRefGoogle Scholar
  166. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator. Hfq PLoS Genet 4:e1000163CrossRefGoogle Scholar
  167. Sparrer H, Rutkat K, Buchner J (1997) Catalysis of protein folding by symmetric chaperone complexes. Proc Natl Acad Sci USA 94:1096–1100PubMedCrossRefGoogle Scholar
  168. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nature Rev Immunol 2:185–194CrossRefGoogle Scholar
  169. Storz G, Vogel J, Wassarman KM (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43:880–891PubMedCrossRefGoogle Scholar
  170. Strauch KL, Johnson K, Beckwith J (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 171:2689–2696PubMedGoogle Scholar
  171. Straus DB, Walter WA, Gross CA (1987) The heat shock response of E. coli is regulated by changes in the concentration of sigma 32. Nature 329:348–351PubMedCrossRefGoogle Scholar
  172. Straus DB, Walter WA, Gross CA (1989) The activity of sigma 32 is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes Dev 3:2003–2010PubMedCrossRefGoogle Scholar
  173. Straus D, Walter W, Gross CA (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 4:2202–2209PubMedCrossRefGoogle Scholar
  174. Studemann A, Noirclerc-Savoye M, Klauck E, Becker G, Schneider D, Hengge R (2003) Sequential recognition of two distinct sites in sigma(S) by the proteolytic targeting factor RssB and ClpX. EMBO J 22:4111–4120PubMedCrossRefGoogle Scholar
  175. Taura T, Kusukawa N, Yura T, Ito K (1989) Transient shut off of Escherichia coli heat shock protein synthesis upon temperature shift down. Biochem Biophys Res Commun 163:438–443PubMedCrossRefGoogle Scholar
  176. Tilly K, McKittrick N, Zylicz M, Georgopoulos C (1983) The dnaK protein modulates the heat shock response of Escherichia coli. Cell 34:641–646PubMedCrossRefGoogle Scholar
  177. Tilly K, Spence J, Georgopoulos C (1989) Modulation of stability of the Escherichia coli heat shock regulatory factor sigma. J Bacteriol 171:1585–1589PubMedGoogle Scholar
  178. Tomoyasu T, Gamer J, Bukau B, Kanemori M, Mori H, Rutman AJ, Oppenheim AB, Yura T, Yamanaka K, Niki H et al (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J 14:2551–2560PubMedGoogle Scholar
  179. Tomoyasu T, Mogk A, Langen H, Goloubinoff P, Bukau B (2001) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40:397–413PubMedCrossRefGoogle Scholar
  180. Typas A, Barembruch C, Possling A, Hengge R (2007a) Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine-tuner of sigmaS activity and levels. EMBO J 26:1569–1578PubMedCrossRefGoogle Scholar
  181. Typas A, Becker G, Hengge R (2007b) The molecular basis of selective promoter activation by the sigmaS subunit of RNA polymerase. Mol Microbiol 63:1296–1306PubMedCrossRefGoogle Scholar
  182. Typas A, Stella S, Johnson RC, Hengge R (2007c) The −35 sequence location and the Fis-sigma factor interface determine sigmas selectivity of the proP (P2) promoter in Escherichia coli. Mol Microbiol 63:780–796PubMedGoogle Scholar
  183. Ueki T, Inouye S (2002) Transcriptional activation of a heat-shock gene, lonD, of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system. J Biol Chem 277:6170–6177PubMedCrossRefGoogle Scholar
  184. Val DL, Cronan JE Jr (1998) In vivo evidence that S-adenosylmethionine and fatty acid synthesis intermediates are the substrates for the LuxI family of autoinducer synthases. J Bacteriol 180:2644–2651PubMedGoogle Scholar
  185. van Asseldonk M, Simons A, Visser H, de Vos WM, Simons G (1993) Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene. J Bacteriol 175:1637–1644PubMedGoogle Scholar
  186. Van Bogelen RA, Kelley PM, Neidhardt FC (1987) Differential induction of heat shock, SOS and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol 169:26–32Google Scholar
  187. Varon D, Boylan SA, Okamoto K, Price CW (1993) Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B. J Bacteriol 175:3964–3971PubMedGoogle Scholar
  188. Varon D, Brody MS, Price CW (1996) Bacillus subtilis operon under the dual control of the general stress transcription factor sigma B and the sporulation transcription factor sigma H. Mol Microbiol 20:339–350PubMedCrossRefGoogle Scholar
  189. Vicente M, Chater KF, De Lorenzo V (1999) Bacterial transcription factors involved in global regulation. Mol Microbiol 33:8–17PubMedCrossRefGoogle Scholar
  190. Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9:578–589PubMedCrossRefGoogle Scholar
  191. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31:6435–6443PubMedCrossRefGoogle Scholar
  192. Volker U, Engelmann S, Maul B, Riethdorf S, Volker A, Schmid R, Mach H, Hecker M (1994) Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology 140(Pt 4):741–752PubMedCrossRefGoogle Scholar
  193. von Blohn C, Kempf B, Kappes RM, Bremer E (1997) Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Mol Microbiol 25:175–187CrossRefGoogle Scholar
  194. Waldminghaus T, Gaubig LC, Klinkert B, Narberhaus F (2009) The Escherichia coli ibpA thermometer is comprised of stable and unstable structural elements. RNA Biol 6:455–463PubMedCrossRefGoogle Scholar
  195. Wang QP, Kaguni JM (1989) dnaA protein regulates transcriptions of the rpoH gene of Escherichia coli. J Biol Chem 264:7338–7344PubMedGoogle Scholar
  196. Wassarman KM, Storz G (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell 101:613–623PubMedCrossRefGoogle Scholar
  197. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 15:1637–1651PubMedCrossRefGoogle Scholar
  198. Wawrzynow A, Wojtkowiak D, Marszalek J, Banecki B, Jonsen M, Graves B, Georgopoulos C, Zylicz M (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 14:1867–1877PubMedGoogle Scholar
  199. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603PubMedCrossRefGoogle Scholar
  200. Widerak M, Kern R, Malki A, Richarme G (2005) U2552 methylation at the ribosomal A-site is a negative modulator of translational accuracy. Gene 347:109–114PubMedCrossRefGoogle Scholar
  201. Yang X, Kang CM, Brody MS, Price CW (1996) Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev 10:2265–2275PubMedCrossRefGoogle Scholar
  202. Yu H, Schurr MJ, Deretic V (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 177:3259–3268PubMedGoogle Scholar
  203. Yuan G, Wong SL (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 177:6462–6468PubMedGoogle Scholar
  204. Yuan G, Wong SL (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 177:5427–5433PubMedGoogle Scholar
  205. Yuzawa H, Nagai H, Mori H, Yura T (1993) Heat induction of sigma 32 synthesis mediated by mRNA secondary structure: a primary step of the heat shock response in Escherichia coli. Nucleic Acids Res 21:5449–5455PubMedCrossRefGoogle Scholar
  206. Zhang S, Scott JM, Haldenwang WG (2001) Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma(B). J Bacteriol 183:2316–2321PubMedCrossRefGoogle Scholar
  207. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50:1111–1124PubMedCrossRefGoogle Scholar
  208. Zhou YN, Kusukawa N, Erickson JW, Gross CA, Yura T (1988) Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J Bacteriol 170:3640–3649PubMedGoogle Scholar
  209. Zhou Y, Gottesman S, Hoskins JR, Maurizi MR, Wickner S (2001) The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev 15:627–637PubMedCrossRefGoogle Scholar
  210. Zuber U, Schumann W (1994) CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 176:1359–1363PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and Biotechnology, The George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

Personalised recommendations