1887

Microbiology Society logo

Volume 150, Issue 7

A global role for Fis in the transcriptional control of metabolism and type III secretion in serovar Typhimurium Free

Abstract

Fis is a key DNA-binding protein involved in nucleoid organization and modulation of many DNA transactions, including transcription in enteric bacteria. The regulon of genes whose expression is influenced by Fis in serovar Typhimurium () has been defined by DNA microarray analysis. These data suggest that Fis plays a central role in coordinating the expression of both metabolic and type III secretion factors. The genes that were most strongly up-regulated by Fis were those involved in virulence and located in the pathogenicity islands SPI-1, SPI-2, SPI-3 and SPI-5. Similarly, motility and flagellar genes required Fis for full expression. This was shown to be a direct effect as purified Fis protein bound to the promoter regions of representative flagella and SPI-2 genes. Genes contributing to aspects of metabolism known to assist the bacterium during survival in the mammalian gut were also Fis-regulated, usually negatively. This category included components of metabolic pathways for propanediol utilization, biotin synthesis, vitamin B transport, fatty acids and acetate metabolism, as well as genes for the glyoxylate bypass of the tricarboxylic acid cycle. Genes found to be positively regulated by Fis included those for ethanolamine utilization. The data reported reveal the central role played by Fis in coordinating the expression of both housekeeping and virulence factors required by during life in the gut lumen or during systemic infection of host cells.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): FDR, false discovery rate and Fis, factor for inversion stimulation
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27209-0
2004-07-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/7/mic1502037.html?itemId=/content/journal/micro/10.1099/mic.0.27209-0&mimeType=html&fmt=ahah

References

  1. Akbar S., Schechter L. M., Lostroh C. P., Lee C. A. 2003; AraC/XylS family members, HilD and HilC, directly activate virulence gene expression independently of HilA in Salmonella typhimurium. Mol Microbiol 47:715–728 [CrossRef]
     [Google Scholar]
  2. Appleman J. A., Ross W., Salomon J., Gourse R. L. 1998; Activation of Escherichia coli rRNA transcription by Fis during a growth cycle. J Bacteriol 180:1525–1532
     [Google Scholar]
  3. Bajaj V., Lucas R. L., Hwang C., Lee C. A. 1996; Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22:703–714 [CrossRef]
     [Google Scholar]
  4. Ball C. A., Osuna R., Ferguson K. C., Johnson R. C. 1992; Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174:8043–8056
     [Google Scholar]
  5. Boddicker J. D., Knosp B. M., Jones B. D. 2003; Transcription of the Salmonella invasion gene activator, hilA, requires HilD activation in the absence of negative regulators. J Bacteriol 185:525–533 [CrossRef]
     [Google Scholar]
  6. Cashel M., Gentry D. R., Hernandez V. J., Vinella D. 1996; The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 1458–1496Edited by Neidhardt F. C. & others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  7. Chilcott G. S., Hughes K. T. 2000; Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64:694–708 [CrossRef]
     [Google Scholar]
  8. Cirillo D., Valdivia R., Monack D., Falkow S. 1998; Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30:175–188 [CrossRef]
     [Google Scholar]
  9. Claret L., Rouvière-Yaniv J. 1996; Regulation of HU alpha and HU beta by CRP and FIS in Escherichia coli. J Mol Biol 263:126–139 [CrossRef]
     [Google Scholar]
  10. Clements M. O., Eriksson S., Thompson A., Lucchini S., Hinton J. C. D., Normark S., Rhen M. 2002; Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci U S A 99:8784–8789 [CrossRef]
     [Google Scholar]
  11. Cronan J. E. Jr, Rock C. O. 1996; Biosynthesis of membrane lipids. In Escherichia Coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 612–636Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  12. Dailey F. E., Macnab R. M. 2002; Effects of lipoprotein biogenesis mutations on flagellar assembly in Salmonella. J Bacteriol 184:771–776 [CrossRef]
     [Google Scholar]
  13. Deighan P., Beloin C., Dorman C. J. 2003; Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol Microbiol 48:1401–1416 [CrossRef]
     [Google Scholar]
  14. Deiwick J., Nikolaus T., Erdogan S., Hensel M. 1999; Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31:1759–1773 [CrossRef]
     [Google Scholar]
  15. Dersch P., Kneip S., Bremer E. 1994; The nucleoid-associated DNA-binding protein H-NS is required for the efficient adaptation of Escherichia coli K-12 to a cold environment. Mol Gen Genet 245:255–259
     [Google Scholar]
  16. Dorman C. J., Deighan P. 2003; Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev 13:179–184 [CrossRef]
     [Google Scholar]
  17. Eichelberg K., Galan J. E. 2000; The flagellar sigma factor FliA (σ28) regulates the expression of Salmonella genes associated with the centisome 63 type III secretion system. Infect Immun 68:2735–2743 [CrossRef]
     [Google Scholar]
  18. Ellermeier C. D., Slauch J. M. 2003; RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J Bacteriol 185:5096–5108 [CrossRef]
     [Google Scholar]
  19. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J. C. D. 2003; Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47:103–118
     [Google Scholar]
  20. Falconi M., Brandi A., La Teana A., Gualerzi C. O., Pon C. L. 1996; Antagonistic involvement of FIS and H-NS proteins in the transcriptional control of hns expression. Mol Microbiol 19:965–975 [CrossRef]
     [Google Scholar]
  21. Falconi M., Proseda G., Giangrossi M., Beghetto E., Colonna B. 2001; Involvement of Fis in the H-NS-mediated regulation of virF gene in Shigella and enteroinvasive Escherichia coli. Mol Microbiol 42:439–452 [CrossRef]
     [Google Scholar]
  22. Farinha M. A., Kropinski A. M. 1990; Construction of broad-host range plasmid vectors for easy visible selection and analysis of promoters. J Bacteriol 172:3496–3499
     [Google Scholar]
  23. Feng X., Oropeza R., Kenney L. J. 2003a; Dual regulation by phospho-OmpR of ssrA/B gene expression in Salmonella pathogenicity island 2. Mol Microbiol 48:1131–1143 [CrossRef]
     [Google Scholar]
  24. Finkel S. E., Johnson R. C. 1992; The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol 6:3257–3265 [CrossRef]
     [Google Scholar]
  25. Finlay B. B., Brumell J. H. 2000; Salmonella interactions with host cells: in vitro and in vivo. Philos Trans R Soc Lond B Biol Sci 355:623–631 [CrossRef]
     [Google Scholar]
  26. Free A., Dorman C. J. 1997; The Escherichia coli stpA gene is transiently expressed during growth in rich medium and is induced in minimal medium and by stress conditions. J Bacteriol 197:909–918
     [Google Scholar]
  27. Free A., Porter M. E., Deighan P., Dorman C. J. 2001; Requirement for the molecular adapter function of StpA at the Escherichia coli bgl promoter depends upon the level of truncated H-NS protein. Mol Microbiol 42:903–917 [CrossRef]
     [Google Scholar]
  28. Galán J. E. 2001; Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17:53–86 [CrossRef]
     [Google Scholar]
  29. Garmendia J., Beuzon C. R., Ruiz-Albert J., Holden D. W. 2003; The roles of SsrA–SsrB and OmpR–EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. Microbiology 149:2385–2396 [CrossRef]
     [Google Scholar]
  30. Glansdorff N. 1996; Biosynthesis of arginine and polyamines. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 408–433Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  31. Goldberg M. D., Johnson M., Hinton J. C. D., Williams P. H. 2001; Role of the nucleoid-associated protein Fis in the regulation of virulence properties of enteropathogenic Escherichia coli. Mol Microbiol 41:549–559 [CrossRef]
     [Google Scholar]
  32. Gonzalez-Gil G., Bringmann P., Kahmann R. 1996; FIS is a regulator of metabolism in Escherichia coli. Mol Microbiol 22:21–29 [CrossRef]
     [Google Scholar]
  33. Goodier R. I., Ahmer B. M. 2001; SirA orthologs affect both motility and virulence. J Bacteriol 183:2249–2258 [CrossRef]
     [Google Scholar]
  34. Grant A. J., Farris M., Alefounder P., Williams P. H., Woodward M. J., O'Connor C. D. 2003; Co-ordination of pathogenicity island expression by the BipA GTPase in enteropathogenic Escherichia coli (EPEC). Mol Microbiol 48:507–521 [CrossRef]
     [Google Scholar]
  35. Grob P., Guiney D. G. 1996; In vitro binding of the Salmonella dublin virulence plasmid regulatory protein SpvR to the promoter regions of spvA and spvR. J Bacteriol 178:1813–1820
     [Google Scholar]
  36. Grob P., Kahn D., Guiney D. G. 1997; Mutational characterization of promoter regions recognized by the Salmonella dublin virulence plasmid regulatory protein SpvR. J Bacteriol 179:5398–5406
     [Google Scholar]
  37. Groisman E. A. 2001; The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835–1842 [CrossRef]
     [Google Scholar]
  38. Groisman E. A., Mouslim C. 2000; Molecular mechanisms of Salmonella pathogenesis. Curr Opin Infect Dis 13:519–522 [CrossRef]
     [Google Scholar]
  39. Groisman E. A., Ochman H. 1993; Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J 12:3779–3787
     [Google Scholar]
  40. Groisman E. A., Ochman H. 1997; How Salmonella became a pathogen. Trends Microbiol 5:343–349 [CrossRef]
     [Google Scholar]
  41. Hacker J., Kaper J. 1999; The concept of pathogenicity islands. In Pathogenicity Islands and Other Mobile Virulence Elements pp. 1–11Edited by Kaper J., Hacker J. Washington DC: American Society for Microbiology;
     [Google Scholar]
  42. Hardt W.-D., Urlaub H., Gálan J. E. 1998; A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc Natl Acad Sci U S A 95:2574–2579 [CrossRef]
     [Google Scholar]
  43. Heichman K. A., Johnson R. C. 1990; The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science 249:511–517 [CrossRef]
     [Google Scholar]
  44. Hengen P. N., Bartram S. L., Stewart L. E., Schneider T. D. 1997; Information analysis of Fis binding sites. Nucleic Acids Res 25:4994–5002 [CrossRef]
     [Google Scholar]
  45. Hensel M. 2000; Salmonella pathogenicity island 2. Mol Microbiol 36:1015–1023 [CrossRef]
     [Google Scholar]
  46. Hensel M., Shea J. E., Gleeson C., Jones M. D., Dalton E., Holden D. W. 1995; Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400–403 [CrossRef]
     [Google Scholar]
  47. Hensel M., Shea J. E., Waterman S. R. & 7 other authors; 1998; Genes encoding putative effector proteins of the type III secretion of Salmonella pathogenicity island 2. Mol Microbiol 30:163–174 [CrossRef]
     [Google Scholar]
  48. Hensel M., Nikolaus T., Egelseer C. 1999; Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol Microbiol 31:489–498 [CrossRef]
     [Google Scholar]
  49. Hillyard D. R., Edlund M., Hughes K. T., Marsh M., Higgins N. P. 1990; Subunit-specific phenotypes of Salmonella typhimurium HU mutants. J Bacteriol 172:5402–5407
     [Google Scholar]
  50. Hirano T., Minamino T., Namba K., Macnab R. M. 2003; Substrate specificity classes and the recognition signal for Salmonella type III flagellar export. J Bacteriol 185:2485–2492 [CrossRef]
     [Google Scholar]
  51. Hoiseth S. K., Stocker B. A. D. 1981; Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238–239 [CrossRef]
     [Google Scholar]
  52. Holden D. W. 2002; Trafficking of the Salmonella vacuole in macrophages. Traffic 3:161–169 [CrossRef]
     [Google Scholar]
  53. Johansson J., Eriksson S., Wai S. N., Uhlin B. E., Sondén B. 2001; Heteromeric interactions among nucleoid-associated bacterial proteins: localization of StpA-stabilizing regions in H-NS of Escherichia coli. J Bacteriol 183:2343–2347 [CrossRef]
     [Google Scholar]
  54. Johnson R. C. 2002; Bacterial site-specific DNA inversion systems. In Mobile DNA II pp. 230–271Edited by Craig L., Craigie R., Gellert M., Lambowitz A. M. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  55. Kalir S., McClure J., Pabbaraju K., Southward C., Ronen M., Leibler S., Surette M. G., Alon U. 2001; Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science 292:2080–2083 [CrossRef]
     [Google Scholar]
  56. Keane O. M., Dorman C. J. 2003; The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis. Mol Gen Genomics 270:56–65 [CrossRef]
     [Google Scholar]
  57. Knodler L. A., Celli J., Hardt W. D., Vallance B. A., Yip C., Finlay B. B. 2002; Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol Microbiol 43:1089–1103 [CrossRef]
     [Google Scholar]
  58. Lawhon S. D., Frye J. G., Suyemoto M., Porwollik S., McClelland M., Altier C. 2003; Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48:1633–1645 [CrossRef]
     [Google Scholar]
  59. Lee A. K., Detweiler C. S., Falkow S. 2000; OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J Bacteriol 182:771–781 [CrossRef]
     [Google Scholar]
  60. Libby S. J., Lesnick M., Hasegawa P., Weidenhammer E., Guiney D. G. 2000; The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cell Microbiol 2:49–58 [CrossRef]
     [Google Scholar]
  61. Libby S. J., Lesnick M., Hasegawa P., Kurth M., Belcher C., Fierer J., Guiney D. G. 2002; Characterization of the spv locus inSalmonella enterica serovar Arizona.. Infect Immun 70:3290–3294 [CrossRef]
     [Google Scholar]
  62. Lin E. C. C. 1996; Dissimilatory pathways for sugars, polyols, and carboxylates. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 307–342Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  63. Lucas R. L., Lostroh C. P., DiRusso C. C., Spector M. P., Wanner B. L., Lee C. A. 2000; Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. . J Bacteriol 182:1872–1882 [CrossRef]
     [Google Scholar]
  64. Lucchini S., Thompson A., Hinton J. C. D. 2001; Microarrays for microbiologists. Microbiology 147:1403–1414
     [Google Scholar]
  65. Macnab R. M. 1986; Proton-driven bacterial flagellar motor. Methods Enzymol 125:563–581
     [Google Scholar]
  66. Macnab R. M. 1996; Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp. 123–145Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  67. Macnab R. M. 2003; How bacteria assemble flagella. Annu Rev Microbiol 57:77–100 [CrossRef]
     [Google Scholar]
  68. Madrid C., Nieto J. M., Juarez A. 2002; Role of the Hha/YmoA family of proteins in the thermoregulation of the expression of virulence factors. Int J Med Microbiol 291:425–432
     [Google Scholar]
  69. Manna D., Gowrishankar J. 1994; Evidence for involvement of proteins HU and RpoS in transcription of the osmoresponsive proU operon in Escherichia coli. J Bacteriol 176:5378–5384
     [Google Scholar]
  70. Maurelli A. T., Fernandez R. E., Bloch C. A., Rod C. K., Fasano A. 1998; ‘Black holes' and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci U S A 95:3943–3948 [CrossRef]
     [Google Scholar]
  71. McClelland M., Sanderson K. E., Spieth J.23 other authors 2001; Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852–856 [CrossRef]
     [Google Scholar]
  72. Merrell D. S., Butler S. M., Qadri F., Dolganov N. A., Alam A., Cohen M. B., Calderwood S. B., Schoolnik G. K., Camilli A. 2002; Host-induced epidemic spread of the cholera bacterium. Nature 417:642–645 [CrossRef]
     [Google Scholar]
  73. Miller J. H. 1992 A Short Course in Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  74. Mills D. M., Bajaj V., Lee C. A. 1995; A 40 kilobase chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15:749–759
     [Google Scholar]
  75. Minamino T., Macnab R. M. 1999; Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181:1388–1394
     [Google Scholar]
  76. Nieto J. M., Madrid C., Miquelay E., Parra J. L., Rodriguez S., Juarez A. 2002; Evidence for direct protein–protein interaction between members of the enterobacterial Hha/YmoA and H-NS families of proteins. J Bacteriol 184:629–635 [CrossRef]
     [Google Scholar]
  77. Oberto J., Drlica K., Rouvière-Yaniv J. 1994; Histones, HMG, HU, IHF: Même combat. Biochimie 76:901–908 [CrossRef]
     [Google Scholar]
  78. Ochman H., Soncini F. C., Solomoin F., Groisman E. A. 1996; Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A 93:7800–7804 [CrossRef]
     [Google Scholar]
  79. Osuna R., Lienau D., Hughes K. T., Johnson R. C. 1995; Sequence, regulation, and functions of fis in Salmonella typhimurium. J Bacteriol 177:2021–2032
     [Google Scholar]
  80. Paesold G., Guiney D. G., Eckmann L., Kagnoff M. F. 2002; Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol 4:771–781 [CrossRef]
     [Google Scholar]
  81. Park Y. K., Bearson B., Bang S. H., Bang I. S., Foster J. W. 1996; Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol Microbiol 20:605–611 [CrossRef]
     [Google Scholar]
  82. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. 1990; E. coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J 9:3733–3742
     [Google Scholar]
  83. Sambrook J., Russell D. W. 2001 Molecular Cloning, a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  84. Schechter L. M., Jain S., Akbar S., Lee C. A. 2003; The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. . Infect Immun 71:5432–5435 [CrossRef]
     [Google Scholar]
  85. Scherer C. A., Miller S. I. 2001; Molecular pathogenesis of Salmonellae. In Principles of Bacterial Pathogenesis pp. 265–333Edited by Groisman E. A. San Diego: Academic Press;
     [Google Scholar]
  86. Schmitt C. K., Ikeda J. S., Darnell S. C., Watson P. R., Bispham J., Wallis T. S., Weinstein D. L., Metcalf E. S., O'Brien A. D. 2001; Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect Immun 69:5619–5625 [CrossRef]
     [Google Scholar]
  87. Schneider R., Travers A., Kutateladze T., Muskhelishvili G. 1999; A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol 34:953–964 [CrossRef]
     [Google Scholar]
  88. Schneider R., Travers A., Muskhelishvili G. 2000; The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol Microbiol 38:167–175 [CrossRef]
     [Google Scholar]
  89. Shea J. E., Hensel M., Gleeson C., Holden D. W. 1996; Identification of a virulence locus encoding a type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A 93:2593–2597 [CrossRef]
     [Google Scholar]
  90. Sheehan B. J., Dorman C. J. 1998; In vivo analysis of the interactions of the LysR-like regulator SpvR with the operator sequences of the spvA and spvR virulence genes of Salmonella typhimurium. Mol Microbiol 30:91–105 [CrossRef]
     [Google Scholar]
  91. Sheikh J., Hicks S., D'Agnol M., Philips A. D., Nataro J. P. 2001; Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 41:983–997
     [Google Scholar]
  92. Sternberg N. L., Maurer R. 1991; Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol 204:18–43
     [Google Scholar]
  93. Tedin K., Blasi U. 1996; The RNA chain elongation rate of the lambda late mRNA is unaffected by high levels of ppGpp in the absence of amino acid starvation. J Biol Chem 271:17675–17686 [CrossRef]
     [Google Scholar]
  94. Thompson A., Lucchini S., Hinton J. C. D. 2001; It's easy to build your own microarrayer!. Trends Microbiol 9:154–156 [CrossRef]
     [Google Scholar]
  95. Valdivia R. H., Falkow S. 1997; Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277:2007–2011 [CrossRef]
     [Google Scholar]
  96. Wagner R. 2000 Transcription Regulation in Prokaryotes Oxford: Oxford University Press;
  97. Walker K. A., Atkins C. L., Osuna R. 1999; Functional domains of the Escherichia coli fis promoter: roles of the −35, −10, and transcription initiation regions in the response to stringent control and growth phase-dependent regulation. J Bacteriol 181:1269–1280
     [Google Scholar]
  98. Waterman S. R., Holden D. W. 2003; Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5:501–511 [CrossRef]
     [Google Scholar]
  99. Weinstein-Fischer D., Elgrably-Weiss M., Altuvia S. 2000; Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413–1420
     [Google Scholar]
  100. Williams R. M., Rimsky S., Buc H. 1996; Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. J Bacteriol 178:4335–4343
     [Google Scholar]
  101. Wilson R. L., Libby S. J., Freet A. M., Boddicker J. D., Fahlen T. F., Jones B. D. 2001; Fis, a DNA nucleoid-associated protein, is involved in Salmonella typhimurium SPI-1 invasion gene expression. Mol Microbiol 39:79–88 [CrossRef]
     [Google Scholar]
  102. Wood M. W., Rosqvist R., Mullan P. B., Edwards M. H., Galyov E. E. 1996; SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22:327–338 [CrossRef]
     [Google Scholar]
  103. Xu J., Johnson R. C. 1995a; aldB, an RpoS-dependent gene in Escherichia coli encoding an aldehyde dehydrogenase that is repressed by Fis and activated by Crp. J Bacteriol 177:3166–3175
     [Google Scholar]
  104. Xu J., Johnson R. C. 1995b; Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J Bacteriol 177:938–947
     [Google Scholar]
  105. Yoon H., Lim S., Heu S., Choi S., Tyu S. 2003; Proteome of Salmonella enterica serovar Typhimurium fis mutant. FEMS Microbiol Lett 226:391–396 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27209-0
Loading
A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium
Microbiology 150, 2037 (2004); https://doi.org/10.1099/mic.0.27209-0
/content/journal/micro/10.1099/mic.0.27209-0
/content/journal/micro/10.1099/mic.0.27209-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error