1887

Abstract

The DNA static curvature has been described to play a key role as a regulatory element in the transcription process of several bacterial genes. Here, the role of DNA curvature in the expression of the porin gene in serovar Typhi is described. The web server was used to predict mutations that diminished or restored the extent of DNA curvature in the 5′ regulatory region of . Using these predictions, curvature was diminished by site-directed mutagenesis of only two residues, and curvature was restored by further mutagenesis of the same two residues. Lowering the extent of DNA curvature resulted in an increase in expression and in the diminution of the affinity of the silencer proteins H-NS and StpA for the 5′ regulatory region. These mutations were in a region shown not to contain the H-NS nucleation site, consistent with the notion that the effect on expression was due to changes in DNA structural topology.

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2009-07-01
2024-03-28
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References

  1. Asayama M., Kato H., Shibato J., Shirai M., Ohyama T. 2002; The curved DNA structure in the 5′-upstream region of the light-responsive genes: its universality, binding factor and function for cyanobacterial psbA transcription. Nucleic Acids Res 30:4658–4666
    [Google Scholar]
  2. Atlung T., Ingmer H. 1997; H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24:7–17
    [Google Scholar]
  3. Bouffartigues E., Buckle M., Badaut C., Travers A., Rimsky S. 2007; H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol 14:441–448
    [Google Scholar]
  4. Casadaban M. J. 1976; Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104:541–555
    [Google Scholar]
  5. Cobbett C., Dickson B., Farmer L. 1989; The role of a static bend in the DNA of the aroF regulatory region of Escherichia coli . Gene 75:185–191
    [Google Scholar]
  6. Dame R. T., Luijsterburg M. S., Krin E., Bertin P. N., Wagner R., Wuite G. J. L. 2005; DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187:1845–1848
    [Google Scholar]
  7. Dame R. T., Noom M. C., Wuite G. J. L. 2006; Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444:387–390
    [Google Scholar]
  8. De la Cruz M. A., Fernández-Mora M., Guadarrama C., Flores-Valdez M. A., Bustamante V. H., Vázquez A., Calva E. 2007; LeuO antagonizes the H-NS and StpA-dependent repression in Salmonella enterica ompS1 . Mol Microbiol 66:727–743
    [Google Scholar]
  9. Dorman C. J., Kane K. A. 2009; DNA bridging and antibridging: a role for bacterial nucleoid-associated proteins in regulating the expression of laterally acquired genes. FEMS Microbiol Rev 33:587–592
    [Google Scholar]
  10. Falconi M., Higgins N. P., Spurio R., Pon C. L., Gualerzi C. O. 1993; Expression of the gene encoding the major bacterial nucleoide protein H-NS is subject to transcriptional auto-repression. Mol Microbiol 10:273–282
    [Google Scholar]
  11. Fang M., Majumder A., Tsai K. J., Wu H.-Y. 2000; ppGpp-dependent leuO expression in bacteria under stress. Biochem Biophys Res Commun 276:64–70
    [Google Scholar]
  12. Fernández-Mora M., Oropeza R., Puente J. L., Calva E. 1995; Isolation and characterization of ompS1, a novel Salmonella typhi outer membrane protein-encoding gene. Gene 158:67–72
    [Google Scholar]
  13. Flores-Valdez M. A., Puente J. L., Calva E. 2003; Negative osmoregulation of the Salmonella ompS1 porin gene independently of OmpR in an hns background. J Bacteriol 185:6497–6506
    [Google Scholar]
  14. Goodsell D. S., Dickerson R. E. 1994; Bending and curvature calculations in B-DNA. Nucleic Acids Res 22:5497–5503
    [Google Scholar]
  15. Gourse R. L., Ross W., Gaal T. 2000; Ups and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition. Mol Microbiol 37:687–695
    [Google Scholar]
  16. Hadjifrangiskou M. G., Koehler T. M. 2008; Intrinsic curvature associated with the coordinately regulated anthrax toxin gene promoters. Microbiology 154:2501–2512
    [Google Scholar]
  17. Hernández-Lucas I., Gallego-Hernández A. L., Encarnación S., Fernández-Mora M., Martínez-Batallar A. G., Salgado H., Oropeza R., Calva E. 2008; The LysR-type transcriptional regulator LeuO controls the expression of several genes in Salmonella enterica serovar Typhi. J Bacteriol 190:1658–1670
    [Google Scholar]
  18. Jáuregui R., Abreu-Goodger C., Moreno-Hagelsieb G., Collado-Vides J., Merino E. 2003; Conservation of DNA curvature signals in regulatory regions of prokaryotic genes. Nucleic Acids Res 31:6770–6777
    [Google Scholar]
  19. Kaji M., Matsushita O., Tamai E., Miyata S., Taniguchi Y., Shimamoto S., Katayama S., Morita S., Okabe A. 2003; A novel type of DNA curvature present in a Clostridium perfringens ferredoxin gene: characterization and role in gene expression. Microbiology 149:3083–3091
    [Google Scholar]
  20. Lawley T. D., Chan K., Thompson L. J., Kim C. C., Govoni G. R., Monack D. M. 2006; Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2:e11
    [Google Scholar]
  21. Lucchini S., Rowley G., Goldberg M. D., Hurd D., Harrison M., Hinton J. C. D. 2006; H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2:e81
    [Google Scholar]
  22. Majumder A., Fang M., Tsai K.-J., Ueguchi C., Mizuno T., Wu H.-Y. 2001; LeuO expression in response to starvation for branched-chain amino acids. J Biol Chem 276:19046–19051
    [Google Scholar]
  23. Mireles J. R. II, Toguchi A., Harshey R. M. 2001; Salmonella enterica serovar Typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183:5848–5854
    [Google Scholar]
  24. Mizuno T. 1987; Static bend of DNA helix at the activator recognition site of the ompF promoter in Escherichia coli . Gene 54:57–64
    [Google Scholar]
  25. Moorthy S., Watnick P. 2005; Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol 57:1623–1635
    [Google Scholar]
  26. Navarre W. W., Porwollik S., Wang Y., McClelland M., Rosen H., Libby S. J., Fang F. C. 2006; Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella . Science 313:236–238
    [Google Scholar]
  27. Noom M. C., Navarre W. W., Oshima T., Wuite G. J. L., Dame R. T. 2007; H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17:R913–R914
    [Google Scholar]
  28. Olivares-Zavaleta N., Jáuregui R., Merino E. 2006; Genome analysis of Escherichia coli promoter sequences evidences that DNA static curvature plays a more important role in gene transcription than has previously been anticipated. Genomics 87:329–337
    [Google Scholar]
  29. Oropeza R., Sampieri C. L., Puente J. L., Calva E. 1999; Negative and positive regulation of the non-osmoregulated ompS1 porin gene in Salmonella typhi: a novel regulatory mechanism that involves OmpR. Mol Microbiol 32:243–252
    [Google Scholar]
  30. Pang T., Levine M. M., Ivanoff B., Wain J., Finlay B. B. 1998; Typhoid fever: important issues still remain. Trends Microbiol 6:131–133
    [Google Scholar]
  31. Pérez-Martín J., Rojo F., De Lorenzo V. 1994; Promoters responsive to DNA bending: a common theme in prokaryotic gene expression. Microbiol Rev 58:268–290
    [Google Scholar]
  32. Poore C. A., Mobley H. L. T. 2003; Differential regulation of the Proteus mirabilis urease gene cluster by UreR and H-NS. Microbiology 149:3383–3394
    [Google Scholar]
  33. Prosseda G., Falconi M., Giangrossi M., Gualerzi C. O., Micheli G., Colonna B. 2004; The virF promoter in Shigella: more than just a curved DNA stretch. Mol Microbiol 51:523–537
    [Google Scholar]
  34. Puente J. L., Flores V., Fernández M., Fuchs Y., Calva E. 1987; Isolation of an ompC-like outer membrane protein gene from Salmonella typhi . Gene 61:75–83
    [Google Scholar]
  35. Pul Ü., Lux B., Wurm R., Wagner R. 2008; Effect of upstream curvature and transcription factors H-NS and LRP on the efficiency of Escherichia coli rRNA promoters P1 and P2-a phasing analysis. Microbiology 154:2546–2558
    [Google Scholar]
  36. Ramani N., Huang L., Freundlich M. 1992; In vitro interactions of integration host factor with the ompF promoter-regulatory region of Escherichia coli . Mol Gen Genet 231:248–255
    [Google Scholar]
  37. Rodríguez-Morales O., Fernández-Mora M., Hernández-Lucas I., Vázquez A., Puente J. L., Calva E. 2006; Salmonella enterica serovar Typhimurium ompS1 and ompS2 mutants are attenuated for virulence in mice. Infect Immun 74:1398–1402
    [Google Scholar]
  38. Satchwell S. C., Drew H. R., Travers A. A. 1986; Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 191:659–675
    [Google Scholar]
  39. Tenor J. L., McCormick B. A., Ausubel F. M., Aballay A. 2004; Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14:1018–1024
    [Google Scholar]
  40. Toguchi A., Siano M., Burkart M., Harshey R. M. 2000; Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J Bacteriol 182:6308–6321
    [Google Scholar]
  41. VanBogelen R. A., Olson E. R., Wanner B. L., Neidhardt F. C. 1996; Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli . J Bacteriol 178:4344–4366
    [Google Scholar]
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