Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens (original) (raw)

• Ruiz, N., Kahne, D. & Silhavy, T. J. Advances in understanding bacterial outer-membrane biogenesis. Nature Rev. Microbiol. 4, 57?66 (2006). A thorough and interesting review of the biogenesis of the bacterial outer membrane, combined with an overview of the techniques involved in achieving this understanding.
  Google Scholar
• De Las, P., Connolly, L. & Gross, C. A. σE is an essential sigma factor in Escherichia coli. J Bacteriol. 179, 6862?6864 (1997).
  Google Scholar
• Erickson, J. W. & Gross, C. A. Identification of the σE subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev. 3, 1462?1471 (1989). A seminal paper for those interested in the ESR of enterics. The first study to identify the σ E subunit through its role in E. coli high-temperature regulation. This same group then began to map the E. coli rpoE operon and dissect its regulation.
  CAS PubMed Google Scholar
• Rouviere, P. E. et al. rpoE, the gene encoding the second heat-shock sigma factor, σE, in Escherichia coli. EMBO J. 14, 1032?1042 (1995).
  CAS PubMed PubMed Central Google Scholar
• Raivio, T. L. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56, 1119?1128 (2005).
  CAS PubMed Google Scholar
• Danese, P. N. & Silhavy, T. J. The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 11, 1183?1193 (1997).
  CAS PubMed Google Scholar
• Raivio, T. L., Popkin, D. L. & Silhavy, T. J. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J. Bacteriol. 181, 5263?5272 (1999).
  CAS PubMed PubMed Central Google Scholar
• Raivio, T. L. & Silhavy, T. J. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179, 7724?7733 (1997).
  CAS PubMed PubMed Central Google Scholar
• Snyder, W. B., Davis, L. J., Danese, P. N., Cosma, C. L. & Silhavy, T. J. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol. 177, 4216?4223 (1995).
  CAS PubMed PubMed Central Google Scholar
• Raffa, R. G. & Raivio, T. L. A third envelope stress signal transduction pathway in Escherichia coli. Mol. Microbiol. 45, 1599?1611 (2002). This group identified the BaeSR two-component system as a third member of the ESR which shares some overlap with the CpxRA pathway in regulating certain genes.
  CAS PubMed Google Scholar
• Jones, S. E., Lloyd, L. J., Tan, K. K. & Buck, M. Secretion defects that activate the phage shock response of Escherichia coli. J. Bacteriol. 185, 6707?6711 (2003).
  CAS PubMed PubMed Central Google Scholar
• Darwin, A. J. The phage-shock-protein response. Mol. Microbiol. 57, 621?628 (2005). An excellent overview of the PSP response in enteric bacteria, discussing signal induction and transduction combined with possible physiological roles.
  CAS PubMed Google Scholar
• Maxson, M. E. & Darwin, A. J. Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J. Bacteriol. 186, 4199?4208 (2004).
  CAS PubMed PubMed Central Google Scholar
• Weiner, L. & Model, P. Role of an Escherichia coli stress-response operon in stationary-phase survival. Proc. Natl Acad. Sci. USA 91, 2191?2195 (1994).
  CAS PubMed Google Scholar
• Helmann, J. D. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46, 47?110 (2002).
  CAS PubMed Google Scholar
• Lonetto, M. A., Brown, K. L., Rudd, K. E. & Buttner, M. J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc. Natl Acad. Sci. USA 91, 7573?7577 (1994).
  CAS PubMed Google Scholar
• Craig, J. E., Nobbs, A. & High, N. J. The extracytoplasmic sigma factor, final σE, is required for intracellular survival of nontypeable Haemophilus influenzae in J774 macrophages. Infect. Immun. 70, 708?715 (2002).
  CAS PubMed PubMed Central Google Scholar
• Humphreys, S., Stevenson, A., Bacon, A., Weinhardt, A. B. & Roberts, M. The alternative sigma factor, σE, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 67, 1560?1568 (1999). A seminal paper discussing the σ E regulon in a pathogen showing that an rpoE mutant is viable in S. typhimurium , but is highly attenuated in a mouse model. This study led the way for later work in S. typhimurium and other organisms.
  CAS PubMed PubMed Central Google Scholar
• Kovacikova, G. & Skorupski, K. The alternative sigma factor σE plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun. 70, 5355?5362 (2002).
  CAS PubMed PubMed Central Google Scholar
• Martin, D. W., Holloway, B. W. & Deretic, V. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J. Bacteriol. 175, 1153?1164 (1993).
  CAS PubMed PubMed Central Google Scholar
• Dartigalongue, C., Missiakas, D. & Raina, S. Characterization of the Escherichia coli σE regulon. J. Biol. Chem. 276, 20866?20875 (2001). Until this publication, relatively few genes were known to be under the control of RpoE. Using promoter-fusion libraries, 20 RpoE-regulated promoters in E. coli were identified from various functional categories.
  CAS PubMed Google Scholar
• Rezuchova, B., Miticka, H., Homerova, D., Roberts, M. & Kormanec, J. New members of the Escherichia coli σE regulon identified by a two-plasmid system. FEMS Microbiol. Lett. 225, 1?7 (2003).
  CAS PubMed Google Scholar
• Rhodius, V. A., Suh, W. C., Nonaka, G., West, J. & Gross, C. A. Conserved and variable functions of the σE stress response in related genomes. PLoS Biol. 4, e2 (2005).
  PubMed Central Google Scholar
• Alba, B. M. & Gross, C. A. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52, 613?619 (2004).
  CAS PubMed Google Scholar
• Dartigalongue, C., Loferer, H. & Raina, S. EcfE, a new essential inner membrane protease: its role in the regulation of heat shock response in Escherichia coli. EMBO J. 20, 5908?5918 (2001).
  CAS PubMed PubMed Central Google Scholar
• Duguay, A. R. & Silhavy, T. J. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694, 121?134 (2004).
  CAS PubMed Google Scholar
• Skovierova, H. et al. Identification of the σE regulon of Salmonella enterica serovar 1 Typhimurium. Microbiology (in the press).
• Miticka, H. et al. Transcriptional analysis of the rpoE gene encoding extracytoplasmic stress response sigma factor σE in Salmonella enterica serovar Typhimurium. FEMS Microbiol. Lett. 226, 307?314 (2003).
  CAS PubMed Google Scholar
• Ehrmann, M. & Clausen, T. Proteolysis as a regulatory mechanism. Annu. Rev. Genet. 38, 709?724 (2004).
  CAS PubMed Google Scholar
• Grigorova, I. L. et al. Fine-tuning of the Escherichia coli σE envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes Dev. 18, 2686?2697 (2004).
  CAS PubMed PubMed Central Google Scholar
• Kenyon, W. J., Thomas, S. M., Johnson, E., Pallen, M. J. & Spector, M. P. Shifts from glucose to certain secondary carbon-sources result in activation of the extracytoplasmic function sigma factor σE in Salmonella enterica serovar Typhimurium. Microbiology 151, 2373?2383 (2005).
  CAS PubMed PubMed Central Google Scholar
• Rowley, G., Stevenson, A., Kormanec, J. & Roberts, M. Effect of inactivation of degS on Salmonella enterica serovar Typhimurium in vitro and in vivo. Infect. Immun. 73, 459?463 (2005).
  CAS PubMed PubMed Central Google Scholar
• Kenyon, W. J., Sayers, D. G., Humphreys, S., Roberts, M. & Spector, M. P. The starvation-stress response of Salmonella enterica serovar Typhimurium requires σE-, but not CpxR-regulated extracytoplasmic functions. Microbiology 148, 113?122 (2002).
  CAS PubMed Google Scholar
• Testerman, T. L. et al. The alternative sigma factor σE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43, 771?782 (2002).
  CAS PubMed Google Scholar
• Govan, J. R. & Deretic, V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60, 539?574 (1996).
  CAS PubMed PubMed Central Google Scholar
• Kunst, F. et al. Deduced polypeptides encoded by the Bacillus subtilis sacU locus share homology with two-component sensor-regulator systems. J. Bacteriol. 170, 5093?5101 (1988).
  CAS PubMed PubMed Central Google Scholar
• Weber, R. F. & Silverman, P. M. The cpx proteins of Escherichia coli K12. Structure of the cpxA polypeptide as an inner membrane component. J. Mol. Biol. 203, 467?478 (1988).
  CAS PubMed Google Scholar
• Gacesa, P. Bacterial alginate biosynthesis ? recent progress and future prospects. Microbiology 144, 1133?1143 (1998).
  CAS PubMed Google Scholar
• Wozniak, D. J., Sprinkle, A. B. & Baynham, P. J. Control of Pseudomonas aeruginosa algZ expression by the alternative sigma factor AlgT. J. Bacteriol. 185, 7297?7300 (2003).
  CAS PubMed PubMed Central Google Scholar
• Boucher, J. C., Yu, H., Mudd, M. H. & Deretic, V. Mucoid Pseudomonas aeruginosa in cystic fibrosis: characterization of muc mutations in clinical isolates and analysis of clearance in a mouse model of respiratory infection. Infect. Immun. 65, 3838?3846 (1997).
  CAS PubMed PubMed Central Google Scholar
• Yu, H., Boucher, J. C., Hibler, N. S. & Deretic, V. Virulence properties of Pseudomonas aeruginosa lacking the extreme-stress sigma factor AlgU (σE). Infect. Immun. 64, 2774?2781 (1996).
  CAS PubMed PubMed Central Google Scholar
• Luzar, M. A. & Montie, T. C. Avirulence and altered physiological properties of cystic fibrosis strains of Pseudomonas aeruginosa. Infect. Immun. 50, 572?576 (1985).
  CAS PubMed PubMed Central Google Scholar
• Wu, W., Badrane, H., Arora, S., Baker, H. V. & Jin, S. MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J. Bacteriol. 186, 7575?7585 (2004).
  CAS PubMed PubMed Central Google Scholar
• Hutchison, M. L. & Govan, J. R. Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect. 1, 1005?1014 (1999).
  CAS PubMed Google Scholar
• Stotland, P. K., Radzioch, D. & Stevenson, M. M. Mouse models of chronic lung infection with Pseudomonas aeruginosa: models for the study of cystic fibrosis. Pediatr. Pulmonol. 30, 413?424 (2000).
  CAS PubMed Google Scholar
• Firoved, A. M., Boucher, J. C. & Deretic, V. Global genomic analysis of AlgU (σE)-dependent promoters (sigmulon) in Pseudomonas aeruginosa and implications for inflammatory processes in cystic fibrosis. J. Bacteriol. 184, 1057?1064 (2002). The first study to use a global genomic approach to characterize a σ E homologue outside of E. coli . Particularly interesting as it is directly relevant to a known clinical condition.
  CAS PubMed PubMed Central Google Scholar
• Potvin, E. et al. In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ. Microbiol. 5, 1294?1308 (2003).
  CAS PubMed Google Scholar
• Gallagher, L. A. & Manoil, C. Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J. Bacteriol. 183, 6207?6214 (2001).
  CAS PubMed PubMed Central Google Scholar
• Carterson, A. J. et al. The transcriptional regulator AlgR controls cyanide production in Pseudomonas aeruginosa. J. Bacteriol. 186, 6837?6844 (2004).
  CAS PubMed PubMed Central Google Scholar
• Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103?118 (2003).
  CAS PubMed Google Scholar
• Rollenhagen, C., Sorensen, M., Rizos, K., Hurvitz, R. & Bumann, D. Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen. Proc. Natl Acad. Sci. USA 101, 8739?8744 (2004).
  CAS PubMed Google Scholar
• Crouch, M. L. et al. The alternative sigma factor σ is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol. Microbiol. 56, 789?799 (2005). An interesting study showing that an S. typhimurium rpoE mutant is still attenuated after oral infection in mice that lack an oxidative burst. The study indicates a role for σ E in defence against known antimicrobial peptides, and investigates the susceptibility of this mutant to these peptides. Although the peptides used are distinct in their mechanisms, both led to induction of RpoE.
  CAS PubMed Google Scholar
• Baumler, A. J., Kusters, J. G., Stojiljkovic, I. & Heffron, F. Salmonella typhimurium loci involved in survival within macrophages. Infect. Immun. 62, 1623?1630 (1994).
  CAS PubMed PubMed Central Google Scholar
• Johnson, K. et al. The role of a stress-response protein in Salmonella typhimurium virulence. Mol. Microbiol. 5, 401?407 (1991).
  CAS PubMed Google Scholar
• Spiess, C., Beil, A. & Ehrmann, M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339?347 (1999).
  CAS PubMed Google Scholar
• Chatfield, S. N. et al. Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microb. Pathog. 12, 145?151 (1992).
  CAS PubMed Google Scholar
• Villarreal-Ramos, B. et al. Susceptibility of calves to challenge with Salmonella typhimurium 4/74 and derivatives harbouring mutations in htrA or purE. Microbiology 146, 2775?2783 (2000).
  CAS PubMed Google Scholar
• Bringer, M. A., Barnich, N., Glasser, A. L., Bardot, O. & Darfeuille-Michaud, A. HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect. Immun. 73, 712?721 (2005).
  CAS PubMed PubMed Central Google Scholar
• Cortes, G., de Astorza, B., Benedi, V. J. & Alberti, S. Role of the htrA gene in Klebsiella pneumoniae virulence. Infect. Immun. 70, 4772?4776 (2002).
  CAS PubMed PubMed Central Google Scholar
• Ibrahim, Y. M., Kerr, A. R., McCluskey, J. & Mitchell, T. J. Role of HtrA in the virulence and competence of Streptococcus pneumoniae. Infect. Immun. 72, 3584?3591 (2004).
  CAS PubMed PubMed Central Google Scholar
• Jones, C. H., Bolken, T. C., Jones, K. F., Zeller, G. O. & Hruby, D. E. Conserved DegP protease in Gram-positive bacteria is essential for thermal and oxidative tolerance and full virulence in Streptococcus pyogenes. Infect. Immun. 69, 5538?5545 (2001).
  CAS PubMed PubMed Central Google Scholar
• Pallen, M. J. & Wren, B. W. The HtrA family of serine proteases. Mol. Microbiol. 26, 209?221 (1997).
  CAS PubMed Google Scholar
• Pedersen, L. L., Radulic, M., Doric, M. & Abu, K. Y. HtrA homologue of Legionella pneumophila: an indispensable element for intracellular infection of mammalian but not protozoan cells. Infect. Immun. 69, 2569?2579 (2001).
  CAS PubMed PubMed Central Google Scholar
• Rigoulay, C. et al. Comparative analysis of the roles of HtrA-like surface proteases in two virulent Staphylococcus aureus strains. Infect. Immun. 73, 563?572 (2005).
  CAS PubMed PubMed Central Google Scholar
• Williams, K. et al. Investigation into the role of the serine protease HtrA in Yersinia pestis pathogenesis. FEMS Microbiol. Lett. 186, 281?286 (2000).
  CAS PubMed Google Scholar
• Humphreys, S. et al. Role of periplasmic peptidylprolyl isomerases in Salmonella enterica serovar Typhimurium virulence. Infect. Immun. 71, 5386?5388 (2003).
  CAS PubMed PubMed Central Google Scholar
• Hacker, J. & Fischer, G. Immunophilins: structure?function relationship and possible role in microbial pathogenicity. Mol. Microbiol. 10, 445?456 (1993).
  CAS PubMed Google Scholar
• Arie, J. P., Sassoon, N. & Betton, J. M. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 39, 199?210 (2001).
  CAS PubMed Google Scholar
• Behrens, S., Maier, R., de Cock, H., Schmid, F. X. & Gross, C. A. The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 20, 285?294 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sydenham, M. et al. Salmonella enterica serovar Typhimurium surA mutants are attenuated and effective live oral vaccines. Infect. Immun. 68, 1109?1115 (2000).
  CAS PubMed PubMed Central Google Scholar
• Horne, S. M., Kottom, T. J., Nolan, L. K. & Young, K. D. Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen. Infect. Immun. 65, 806?810 (1997).
  CAS PubMed PubMed Central Google Scholar
• Horne, S. M. & Young, K. D. Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the family of Mip-like FK506-binding proteins. Arch. Microbiol. 163, 357?365 (1995).
  CAS PubMed Google Scholar
• Sheehan, B. J. et al. Identification of Actinobacillus pleuropneumoniae genes important for survival during infection in its natural host. Infect. Immun. 71, 3960?3970 (2003).
  CAS PubMed PubMed Central Google Scholar
• Redford, P., Roesch, P. L. & Welch, R. A. DegS is necessary for virulence and is among extraintestinal Escherichia coli genes induced in murine peritonitis. Infect. Immun. 71, 3088?3096 (2003).
  CAS PubMed PubMed Central Google Scholar
• DiGiuseppe, P. A. & Silhavy, T. J. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185, 2432?2440 (2003).
  CAS PubMed PubMed Central Google Scholar
• Pogliano, J., Lynch, A. S., Belin, D., Lin, E. C. & Beckwith, J. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev. 11, 1169?1182 (1997).
  CAS PubMed Google Scholar
• Raivio, T. L. & Silhavy, T. J. The σE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2, 159?165 (1999).
  CAS PubMed Google Scholar
• De Wulf, P., McGuire, A. M., Liu, X. & Lin, E. C. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J. Biol. Chem. 277, 26652?26661 (2002). The authors used a bioinformatic rather than a genetic approach to identify putative CpxR-P-binding sites in the E. coli genome. By constructing a weighted promoter screen, they predict that ∼100 operons are under the control of CpxR-P.
  CAS PubMed Google Scholar
• De Wulf, P., Kwon, O. & Lin, E. C. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181, 6772?6778 (1999).
  CAS PubMed PubMed Central Google Scholar
• De Wulf, P. & Lin, E. C. Cpx two-component signal transduction in Escherichia coli: excessive CpxR-P levels underlie CpxA* phenotypes. J. Bacteriol. 182, 1423?1426 (2000).
  CAS PubMed PubMed Central Google Scholar
• Miyadai, H., Tanaka-Masuda, K., Matsuyama, S. & Tokuda, H. Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. J. Biol. Chem. 279, 39807?39813 (2004).
  CAS PubMed Google Scholar
• Mileykovskaya, E. & Dowhan, W. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J. Bacteriol. 179, 1029?1034 (1997).
  CAS PubMed PubMed Central Google Scholar
• Danese, P. N. et al. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J. Bacteriol. 180, 5875?5884 (1998).
  CAS PubMed PubMed Central Google Scholar
• Hung, D. L., Raivio, T. L., Jones, C. H., Silhavy, T. J. & Hultgren, S. J. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20, 1508?1518 (2001).
  CAS PubMed PubMed Central Google Scholar
• Humphreys, S. et al. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect. Immun. 72, 4654?4661 (2004).
  CAS PubMed PubMed Central Google Scholar
• Jones, C. H., Danese, P. N., Pinkner, J. S., Silhavy, T. J. & Hultgren, S. J. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16, 6394?6406 (1997).
  CAS PubMed PubMed Central Google Scholar
• Jubelin, G. et al. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187, 2038?2049 (2005).
  CAS PubMed PubMed Central Google Scholar
• Hernday, A. D., Braaten, B. A., Broitman-Maduro, G., Engelberts, P. & Low, D. A. Regulation of the Pap epigenetic switch by CpxAR; phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. Mol. Cell 16, 537?547 (2004).
  CAS PubMed Google Scholar
• Nevesinjac, A. Z. & Raivio, T. L. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J. Bacteriol. 187, 672?686 (2005).
  CAS PubMed PubMed Central Google Scholar
• Nakayama, S. et al. Activation of hilA expression at low pH requires the signal sensor CpxA, but not the cognate response regulator CpxR, in Salmonella enterica serovar Typhimurium. Microbiology 149, 2809?2817 (2003).
  CAS PubMed Google Scholar
• Leclerc, G. J., Tartera, C. & Metcalf, E. S. Environmental regulation of Salmonella typhi invasion-defective mutants. Infect. Immun. 66, 682?691 (1998).
  CAS PubMed PubMed Central Google Scholar
• Humphries, A. D. et al. The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol. Microbiol. 48, 1357?1376 (2003).
  CAS PubMed Google Scholar
• Tobe, T., Yoshikawa, M., Mizuno, T. & Sasakawa, C. Transcriptional control of the invasion regulatory gene virB of Shigella flexneri: activation by virF and repression by H-NS. J. Bacteriol. 175, 6142?6149 (1993).
  CAS PubMed PubMed Central Google Scholar
• Mitobe, J., Arakawa, E. & Watanabe, H. A sensor of the two-component system CpxA affects expression of the type III secretion system through posttranscriptional processing of InvE. J. Bacteriol. 187, 107?113 (2005).
  CAS PubMed PubMed Central Google Scholar
• Nakayama, S. & Watanabe, H. Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene. J. Bacteriol. 177, 5062?5069 (1995).
  CAS PubMed PubMed Central Google Scholar
• Nakayama, S. & Watanabe, H. Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J. Bacteriol. 180, 3522?3528 (1998).
  CAS PubMed PubMed Central Google Scholar
• Roy, C. R. The Dot/lcm transporter of Legionella pneumophila: a bacterial conductor of vesicle trafficking that orchestrates the establishment of a replicative organelle in eukaryotic hosts. Int. J. Med. Microbiol. 291, 463?467 (2002).
  CAS PubMed Google Scholar
• Cianciotto, N. P. Pathogenicity of Legionella pneumophila. Int. J. Med. Microbiol. 291, 331?343 (2001).
  CAS PubMed Google Scholar
• Gal-Mor, O. & Segal, G. Identification of CpxR as a positive regulator of icm and dot virulence genes of Legionella pneumophila. J. Bacteriol. 185, 4908?4919 (2003).
  CAS PubMed PubMed Central Google Scholar
• Hirakawa, H., Inazumi, Y., Masaki, T., Hirata, T. & Yamaguchi, A. Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol. Microbiol. 55, 1113?1126 (2005).
  CAS PubMed Google Scholar
• Baranova, N. & Nikaido, H. The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J. Bacteriol. 184, 4168?4176 (2002).
  CAS PubMed PubMed Central Google Scholar
• Hirakawa, H., Nishino, K., Hirata, T. & Yamaguchi, A. Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J. Bacteriol. 185, 1851?1856 (2003).
  CAS PubMed PubMed Central Google Scholar
• Brissette, J. L., Russel, M., Weiner, L. & Model, P. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl Acad. Sci. USA 87, 862?866 (1990).
  CAS PubMed Google Scholar
• Kobayashi, H., Yamamoto, M. & Aono, R. Appearance of a stress-response protein, phage-shock protein A, in Escherichia coli exposed to hydrophobic organic solvents. Microbiology 144, 353?359 (1998).
  CAS PubMed Google Scholar
• Model, P., Jovanovic, G. & Dworkin, J. The Escherichia coli phage-shock-protein (psp) operon. Mol. Microbiol. 24, 255?261 (1997).
  CAS PubMed Google Scholar
• Bergler, H., Abraham, D., Aschauer, H. & Turnowsky, F. Inhibition of lipid biosynthesis induces the expression of the pspA gene. Microbiology 140, 1937?1944 (1994).
  CAS PubMed Google Scholar
• Lloyd, L. J. et al. Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG). J. Biol. Chem. 279, 55707?55714 (2004).
  CAS PubMed Google Scholar
• Kleerebezem, M., Crielaard, W. & Tommassen, J. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 15, 162?171 (1996).
  CAS PubMed PubMed Central Google Scholar
• Becker, L. A., Bang, I. S., Crouch, M. L. & Fang, F. C. Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium. Mol. Microbiol. 56, 1004?1016 (2005).
  CAS PubMed Google Scholar
• Darwin, A. J. & Miller, V. L. Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature-tagged transposon mutagenesis. Mol. Microbiol. 32, 51?62 (1999).
  CAS PubMed Google Scholar
• Darwin, A. J. & Miller, V. L. The psp locus of Yersinia enterocolitica is required for virulence and for growth in vitro when the Ysc type III secretion system is produced. Mol. Microbiol. 39, 429?444 (2001).
  CAS PubMed Google Scholar
• Green, R. C. & Darwin, A. J. PspG, a new member of the Yersinia enterocolitica phage shock protein regulon. J. Bacteriol. 186, 4910?4920 (2004).
  CAS PubMed PubMed Central Google Scholar
• Beloin, C. et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51, 659?674 (2004).
  CAS PubMed Google Scholar
• Loosmore, S. M. et al. The Haemophilus influenzae HtrA protein is a protective antigen. Infect. Immun. 66, 899?906 (1998).
  CAS PubMed PubMed Central Google Scholar
• Tacket, C. O. et al. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect. Immun. 65, 452?456 (1997).
  CAS PubMed PubMed Central Google Scholar
• Yang, S. W. et al. Two novel antibiotics, Sch 419558 and Sch 419559, produced by Pseudomonas fluorescens: effect on activity by overexpression of RpoE. Bioorg. Med. Chem. 12, 3333?3338 (2004).
  CAS PubMed Google Scholar
• Flynn, J. M., Levchenko, I., Sauer, R. T. & Baker, T. A. Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev. 18, 2292?2301 (2004). An elegant study that elucidates the final regulatory step in the activation of σ E . The authors implicate ClpXP and SspB in performing the final cleavage of RseA, allowing free σ E to bind to the core RNAP.
  CAS PubMed PubMed Central Google Scholar
• Cascales, E. & Christie, P. J. The versatile bacterial type IV secretion systems. Nature Rev. Microbiol. 1, 137?149 (2003).
  CAS Google Scholar