Physiological effects of crl in Salmonella are modulated by σS level and promoter specificity

Journal of Bacteriology

Volumn 189, Issue 8, 2007, Pages 2976-2987

  Robbe Saule, Véronique ^a   Lopes, Miguel Dias ^a,b   Kolb, Annie ^a   Norel, Françoise ^a  

^a CNRS   (France)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; HOLOENZYME; PROTEIN CRL; REGULATOR PROTEIN; RNA POLYMERASE; SIGMA FACTOR RPOS; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; UNCLASSIFIED DRUG;

ACIDITY; ADRA GENE; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CULTURE; CONTROLLED STUDY; CSGD GENE; ENZYME SYNTHESIS; GENE EXPRESSION PROFILING; GENE FUSION; GENE MUTATION; GENETIC TRANSCRIPTION; MORPHOTYPE; MOUSE; NONHUMAN; OPERON; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RPOS GENE; SALMONELLA; SALMONELLA ENTERICA; TEMPERATURE STRESS;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL PROTEINS; FEMALE; MICE; MICE, INBRED BALB C; OPERON; PROMOTER REGIONS (GENETICS); SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGMA FACTOR; SUCCINATE DEHYDROGENASE; VIRULENCE;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 34247890080     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01919-06     Document Type: Article

References (41)

1. S levels. Mol. Microbiol. 56:811-823.
2. Bougdnur, A., C. Lelong, and J. Geiselmann. 2004. Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J. Biol. Chem. 279:19540-19550.
3. Buchmeier, N. A., S. J. Libby, Y. Xu, P. C. Loewen, J. Switiala, and D. G. Guiney. 1995. DNA repair is more important than catalase for Salmonella virulence in mice. J. Clin. Investig. 95:1047-1053.
4. Chang, A. C., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
5. Chen, G., C. L. Patten, and H. E. Schellhorn. 2004. Positive selection for loss of RpoS function in Escherichia coli. Mutat. Res. 554:193-203.
6. Coynault, C., V. Robbe-Saule, and F. Norel. 1996. Virulence and vaccine potential of Salmonella typhimurium mutants deficient in the expression of the RpoS (sigma S) regulon. Mol. Microbiol. 22:149-160.
7. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
8. Ellermeier, C. D., A. Janakiraman, and J. M. Slauch. 2002. Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290:153-161.
9. Fang, F. C., S. J. Libby, N. A. Buchmeier, P. C. Loewen, J. Switala, J. Harwood, and D. G. Guiney. 1992. The alternative sigma factor KatF (RpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. USA 89:11978-11982.
10. Farewell, A., K. Kvint, and T. Nyström. 1998. Negative regulation by RpoS: a case of sigma factor competition. Mol. Microbiol. 29:1039-1051.
11. Faure, D., R. Frederick, D. Wloch, P. Portier, M. Blot, and J. Adams. 2004. Genomic changes arising in long-term stab cultures of Escherichia coli. J. Bacteriol. 186:6437-6442.
12. Gaal, T., M. J. Mandel, T. J. Silhavy, and R. L. Gourse. 2006. Crl facilitates RNA polymerase holoenzyme formation. J. Bacteriol. 188:7966-7970.
13. Grigorova, I. L., N. J. Phleger, V. K. Mutalik, and C. A. Gross. 2006. Insights into transcriptional regulation and σ competition from an equilibrium model of RNA polymerase binding to DNA. Proc. Natl. Acad. Sci. USA 103:5332-5337.
14. S (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66:373-395.
15. S)-regulated genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:5749-5756.
16. Ishihama, A. 2000. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 54:499-518.
17. King, T., A. Ishihama, A. Kori, and T. Ferenci. 2004. A regulatory trade-off as a source of strain variation in the species Escherichia coli. J. Bacteriol. 186:5614-5620.
18. Kowarz, L., C. Coynault, V. Robbe-Saule, and F. Norel. 1994. The Salmonella typhimurium katF (rpoS) gene: cloning, nucleotide sequence, and regulation of spvR and spvABCD virulence plasmid genes. J. Bacteriol. 176:6852-6860.
19. Lee, I. S., J. Lin, H. K. Hall, B. Bearson, and J. W. Foster. 1995. The stationary-phase sigma factor S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol. Microbiol. 17:155-167.
20. Maeda, H., N. Fujita, and A. Ischihama. 2000. Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase. Nucleic Acids Res. 28:3497-3503.
21. Marschall, C., V. Labrousse, M. Kreimer, D. Weichart, A. Kolb, and R. Hengge-Aronis. 1998. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma S and requires activation by cAMP-CRP. J. Mol. Biol. 276:339-353.
22. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Coutney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
23. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Norel, F., V. Robbe-Saule, M. Y. Popoff, and C. Coynault. 1992. The putative sigma factor KatF (RpoS) is required for the transcription of the Salmonella typhimurium virulence gene spvB in Escherichia coli. FEMS Microbiol. Lett. 99:271-276.
25. Notley-McRobb, L., T. King, and T. Ferenci. 2002. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184:806-811.
26. Nystrom, T. 2004. Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol. Microbiol. 54:855-862.
27. Patten, C. L., M. G. Kirchhof, M. R. Schertzberg, R. A. Morton, and H. E. Schellhorn. 2004. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Gen. Genomics 272:580-591.
28. Pratt, L. A., and T. J. Silhavy. 1998. Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 29:1225-1236.
29. Rahman, M., M. R. Hasan, T. Oba, and K. Shimizu. 2006. Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expression, enzyme activities and intracellular metabolite concentrations. Biotechnol. Bioeng. 94:585-595.
30. 70), promoters, and the kinetics of the steps of transcription initiation, p. 792-821. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
31. S). Mol. Microbiol. 39:1533-1545.
32. Robbe-Saule, V., V. Jaumouillé, M.-C. Prévost, S. Guadagnini, C. Talhouarne, H. Mathout, A. Kolb, and F. Norel. 2006. Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:3983-3994.
33. Robbe-Saule, V., F. Schaefler, L. Kowarz, and F. Norel. 1997. Relationships between H-NS, sigma S, SpvR and growth phase in the control of spvR, the regulatory gene of the Salmonella plasmid virulence operon. Mol. Gen. Genet. 256:333-347.
34. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Schmieger, H. 1972. Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:75-88.
36. Silhavy, T. J., M. L. Bernman, and L. W. Ernqvist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Simon, R. J., J. Quandt, and W. Klipp. 1989. New derivatives of transposon Tn5 suitable for mobilization of replicons, generation of operon fusions and induction of genes in gram-negative bacteria. Gene 80:161-169.
38. Sternberg, N. L., and R. Maurer. 1991. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 204:18-43.
39. Tanaka, K., K. Handel, P. C. Loewen, and H. Takahashi. 1997. Identification and analysis of the rpoS-dependent promoter of katE, encoding catalase HP11 in Escherichia coli. Biochim. Biophys. Acta 1352:161-166.
40. Xu, J., and R. C. Johnson. 1995. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J. Bacteriol. 177:938-947.
41. Zambrano, M. M., D. A. Siegele, M. Almiron, A. Tormo, and R. Kolter. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760.