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Volume 154, Issue 9

Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria Free

Abstract

The H-NS nucleoid-associated DNA-binding protein is an important global repressor of transcription in Gram-negative bacteria. Recently, H-NS has been implicated in the process of xenogeneic silencing, where it represses the transcription of foreign genes acquired by horizontal transfer. This raises interesting questions about the integration of the horizontally acquired genes into the existing gene regulatory networks of the microbe. In particular, how do bacteria derepress silenced genes in order to benefit from their expression without compromising competitive fitness through doing so inappropriately? This article reviews current knowledge about the derepression of genes that are transcriptionally silenced by H-NS. It describes a variety of anti-silencing mechanisms involving (i) protein-independent processes that operate at the level of local DNA structure, (ii) DNA-binding proteins such as Ler, LeuO, RovA, SlyA, VirB, and proteins related to AraC, and (iii) modulatory mechanisms in which H-NS forms heteromeric protein–protein complexes with full-length or partial paralogues such as StpA, Sfh, Hha, YdgT, YmoA or H-NST. The picture that emerges is one of apparently ad hoc solutions to the problem of H-NS-mediated silencing, suggesting that microbes are capable of evolving anti-silencing methods based on the redeployment of existing regulatory proteins rather than employing dedicated, bespoke antagonists. There is also evidence that in a number of cases more sophisticated regulatory processes have been superimposed on these rather simple anti-silencing mechanisms, broadening the range of environmental signals to which H-NS-repressed genes respond.

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2008-09-01
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References

  1. Abrahams G. L., Hensel M. 2006; Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol 8:728–737
     [Google Scholar]
  2. Adler B., Sasakawa C., Tobe T., Makino S., Komatsu K., Yoshikawa M. 1989; A dual transcriptional activation system for the 230 kb plasmid genes coding for virulence-associated antigens of Shigella flexneri . Mol Microbiol 3:627–635
     [Google Scholar]
  3. Afflerbach H., Schröder O., Wagner R. 1998; Effects of the Escherichia coli DNA-binding protein H-NS on rRNA synthesis in vivo . Mol Microbiol 28:641–653
     [Google Scholar]
  4. Atlung T., Sund S., Olesen K., Brøndsted L. 1996; The histone-like protein H-NS acts as a transcriptional repressor for expression of the anaerobic and growth phase activator AppY of Escherichia coli . J Bacteriol 178:3418–3425
     [Google Scholar]
  5. Badaut C., Williams R., Arluison V., Bouffartigues E., Robert B., Buc H., Rimsky S. 2002; The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J Biol Chem 277:41657–41666
     [Google Scholar]
  6. Balsalobre C., Juarez A., Madrid C., Mourino M., Prenafeta A., Munoa F. J. 1996; Complementation of the hha mutation in Escherichia coli by the ymoA gene from Yersinia enterocolitica : dependence on the gene dosage. Microbiology 142:1841–1846
     [Google Scholar]
  7. Baños R. C., Pons J. I., Madrid C., Juárez A. 2008; A global modulatory role for the Yersinia enterocolitica H-NS protein. Microbiology 154:1281–1289
     [Google Scholar]
  8. Barba J., Bustamante V. H., Flores-Valdez M. A., Deng W., Finlay B. B., Puente J. L. 2005; A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators Ler and GrlA. J Bacteriol 187:7918–7930
     [Google Scholar]
  9. Barth M., Marschall C., Muffler A., Fischer D., Hengge-Aronis R. 1995; Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of σ S and many σ S-dependent genes in Escherichia coli . J Bacteriol 177:3455–3464
     [Google Scholar]
  10. Beloin C., Dorman C. J. 2003; An extended role for the nucleoid structuring protein H-NS in the virulence gene regulatory cascade of Shigella flexneri . Mol Microbiol 47:825–838
     [Google Scholar]
  11. Beloin C., McKenna S., Dorman C. J. 2002; Molecular dissection of VirB, a key regulator of the virulence cascade of Shigella flexneri . J Biol Chem 277:15333–15344
     [Google Scholar]
  12. Beloin C., Deighan P., Doyle M., Dorman C. J. 2003; Shigella flexneri 2a strain 2457T expresses three members of the H-NS-like protein family: characterization of the Sfh protein. Mol Genet Genomics 270:66–77
     [Google Scholar]
  13. 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]
  14. Brescia C. C., Kaw M. K., Sledjeski D. D. 2004; The DNA binding protein H-NS binds to and alters the stability of RNA in vitro and in vivo . J Mol Biol 339:505–514
     [Google Scholar]
  15. Bustamante V. H., Santana F. J., Calva E., Puente J. L. 2001; Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli : Ler antagonizes H-NS-dependent repression. Mol Microbiol 39:664–678
     [Google Scholar]
  16. Cathelyn J. S., Crosby S. D., Lathem W. W., Goldman W. E., Miller V. L. 2006; RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci U S A 103:13514–13519
     [Google Scholar]
  17. Cathelyn J. S., Ellison D. W., Hinchliffe S. J., Wren B. W., Miller V. L. 2007; The RovA regulons of Yersinia enterocolitica and Yersinia pestis are distinct: evidence that many RovA-regulated genes were acquired more recently than the core genome. Mol Microbiol 66:189–205
     [Google Scholar]
  18. Chen C. C., Wu H. Y. 2005; LeuO protein delimits the transcriptionally active and repressive domains on the bacterial chromosome. J Biol Chem 280:15111–15121
     [Google Scholar]
  19. Chen C. C., Chou M. Y., Huang C. H., Majumder A., Wu H. Y. 2005; A cis -spreading nucleoprotein filament is responsible for the gene silencing activity found in the promoter relay mechanism. J Biol Chem 280:5101–5112
     [Google Scholar]
  20. Coker C., Bakare O. O., Mobley H. L. 2000; H-NS is a repressor of the Proteus mirabilis urease transcriptional activator gene ureR . J Bacteriol 182:2649–2653
     [Google Scholar]
  21. Coombes B. K., Wickham M. E., Lowden M. J., Brown N. F., Finlay B. B. 2005; Negative regulation of Salmonella pathogenicity island 2 is required for contextual control of virulence during typhoid. Proc Natl Acad Sci U S A 102:17460–17465
     [Google Scholar]
  22. Corbett D., Bennett H. J., Askar H., Green J., Roberts I. S. 2007; SlyA and H-NS regulate transcription of the Escherichia coli K5 capsule gene cluster, and expression of slyA in Escherichia coli is temperature-dependent, positively autoregulated, and independent of H-NS. J Biol Chem 282:33326–33335
     [Google Scholar]
  23. Cornelis G. R., Sluiters C., Delor I., Geib D., Kaniga K., Lambert de Rouvroit C., Sory M. P., Vanooteghem J. C., Michiels T. 1991; ymoA , a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Mol Microbiol 5:1023–1034
     [Google Scholar]
  24. Dame R. T., Wyman C., Goosen N. 2001; Structural basis for preferential binding of H-NS to curved DNA. Biochimie 83:231–234
     [Google Scholar]
  25. Dame R. T., Wyman C., Wurm R., Wagner R., Goosen N. 2002; Structural basis for H-NS-mediated trapping of RNA polymerase in the open initiation complex at the rrnB P1. J Biol Chem 277:2146–2150
     [Google Scholar]
  26. Dame R. T., Luijsterburg M. S., Krin E., Bertin P. N., Wagner R., Wuite G. J. 2005; DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187:1845–1848
     [Google Scholar]
  27. Dame R. T., Noom M. C., Wuite G. J. 2006; Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444:387–390
     [Google Scholar]
  28. Davis B. M., Waldor M. K. 2003; Filamentous phages linked to virulence of Vibrio cholerae . Curr Opin Microbiol 6:35–42
     [Google Scholar]
  29. De la Cruz M. A., Fernández-Mora M., Guadarrama C., Flores-Valdez M. A., Bustamante V. H., Vázquez A., Calva E. 2007; LeuO antagonizes H-NS and StpA-dependent repression in Salmonella enterica ompS1 . Mol Microbiol 66:727–743
     [Google Scholar]
  30. Deighan P., Free A., Dorman C. J. 2000; A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol Microbiol 38:126–139
     [Google Scholar]
  31. 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
     [Google Scholar]
  32. Dorman C. J. 2004; H-NS, a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400
     [Google Scholar]
  33. Dorman C. J. 2007a; Probing bacterial nucleoid structure with optical tweezers. Bioessays 29:212–216
     [Google Scholar]
  34. Dorman C. J. 2007b; H-NS, the genome sentinel. Nat Rev Microbiol 5:157–161
     [Google Scholar]
  35. Dorman C. J., Hinton J. C. D., Free A. 1999; Domain organization and oligomerization among H-NS-like nucleoid-associated proteins in bacteria. Trends Microbiol 7:124–128
     [Google Scholar]
  36. Dorman C. J., McKenna S., Beloin C. 2001; Regulation of virulence gene expression in Shigella flexneri , a facultative intracellular pathogen. Int J Med Microbiol 291:89–96
     [Google Scholar]
  37. Doyle M., Dorman C. J. 2006; Reciprocal transcriptional and posttranscriptional growth-phase-dependent expression of sfh , a gene that encodes a paralogue of the nucleoid-associated protein H-NS. J Bacteriol 188:7581–7591
     [Google Scholar]
  38. Doyle M., Fookes M., Ivens A., Mangan M. W., Wain J., Dorman C. J. 2007; An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315:251–252
     [Google Scholar]
  39. Egan S. M. 2002; Growing repertoire of AraC/XylS activators. J Bacteriol 184:5529–5532
     [Google Scholar]
  40. Ellermeier J. R., Slauch J. M. 2007; Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10:24–29
     [Google Scholar]
  41. Elliott S. J., Sperandio V., Girón J. A., Shin S., Mellies J. L., Wainwright L., Hutcheson S. W., McDaniel T. K., Kaper J. B. 2000; The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli . Infect Immun 68:6115–6126
     [Google Scholar]
  42. Ellison D. W., Miller V. L. 2006a; Regulation of virulence by members of the MarR/SlyA family. Curr Opin Microbiol 9:153–159
     [Google Scholar]
  43. Ellison D. W., Miller V. L. 2006b; H-NS represses inv transcription in Yersinia enterocolitica through competition with RovA and interaction with YmoA. J Bacteriol 188:5101–5112
     [Google Scholar]
  44. Falconi M., Colonna B., Prosseda G., Micheli G., Gualerzi C. O. 1998; Thermoregulation of Shigella and Escherichia coli EIEC pathogenicity. A temperature-dependent structural transition of DNA modulates accessibility of virF promoter to transcriptional repressor H-NS. EMBO J 17:7033–7043
     [Google Scholar]
  45. Fang F. C., Rimsky S. 2008; New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11:113–120
     [Google Scholar]
  46. Fang M., Wu H. Y. 1998; A promoter relay mechanism for sequential gene activation. J Bacteriol 180:626–633
     [Google Scholar]
  47. 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 179:909–918
     [Google Scholar]
  48. 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
     [Google Scholar]
  49. Ghosh A., Paul K., Chowdhury R. 2006; Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae . Infect Immun 74:3060–3064
     [Google Scholar]
  50. Göransson M., Sondén B., Nilsson P., Dagberg B., Forsman K., Emanuelsson K., Uhlin B. E. 1990; Transcriptional silencing and thermoregulation of gene expression in Escherichia coli . Nature 344:682–685
     [Google Scholar]
  51. Grainger D. C., Hurd D., Goldberg M. D., Busby S. J. W. 2006; Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34:4642–4652
     [Google Scholar]
  52. Grewal S. I., Elgin S. C. 2007; Transcription and RNA interference in the formation of heterochromatin. Nature 447:399–406
     [Google Scholar]
  53. Haack K. R., Robinson C. L., Miller K. J., Fowlkes J. W., Mellies J. L. 2003; Interaction of Ler at the LEE5 ( tir ) operon of enteropathogenic Escherichia coli . Infect Immun 71:384–392
     [Google Scholar]
  54. 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 expression of several genes in Salmonella enterica serovar Typhi. J Bacteriol 190:1658–1670
     [Google Scholar]
  55. Heroven A. K., Nagel G., Tran H. J., Parr S., Dersch P. 2004; RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis . Mol Microbiol 53:871–888
     [Google Scholar]
  56. Heroven A. K., Böhme K., Tran-Winkler H., Dersch P. 2007; Regulatory elements implicated in the environmental control of invasin expression in enteropathogenic Yersinia . Adv Exp Med Biol 603:156–166
     [Google Scholar]
  57. Hulbert R. R., Taylor R. K. 2002; Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA promoter. J Bacteriol 184:5533–5544
     [Google Scholar]
  58. Johansson J., Uhlin B. E. 1999; Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary-phase survival of Escherichia coli . Proc Natl Acad Sci U S A 96:10776–10781
     [Google Scholar]
  59. Jordi B. J., Dagberg B., de Haan L. A., Hamers A. M., van der Zeijst B. A., Gaastra W., Uhlin B. E. 1992; The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli . EMBO J 11:2627–2632
     [Google Scholar]
  60. Kim S.-K., Wang J. C. 1999; Gene silencing via protein-mediated subcellular localization of DNA. Proc Natl Acad Sci U S A 96:8557–8561
     [Google Scholar]
  61. Klauck E., Böhringer J., Hengge-Aronis R. 1997; The LysR-like regulator LeuO in Escherichia coli is involved in the translational regulation of rpoS by affecting the expression of the small regulatory DsrA-RNA. Mol Microbiol 25:559–569
     [Google Scholar]
  62. Kong W., Weatherspoon N., Shi Y. 2008; Molecular mechanism for establishment of signal-dependent regulation in the PhoP/PhoQ system. J Biol Chem 283:16612–16621
     [Google Scholar]
  63. Laaberki M. H., Janabi N., Oswald E., Repoila F. 2006; Concert of regulators to switch on LEE expression in enterohemorrhagic Escherichia coli O157 : H7: interplay between Ler, GrlA, HNS and RpoS. Int J Med Microbiol 296:197–210
     [Google Scholar]
  64. Lang B., Blot N., Bouffartigues E., Buckle M., Geertz M., Gualerzi C. O., Mavathur R., Muskhelishvili G., Pon C. L. other authors 2007; High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35:6330–6337
     [Google Scholar]
  65. Le Gall T., Mavris M., Martino M. C., Bernardini M. L., Denamur E., Parsot C. 2005; Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri . Microbiology 151:951–962
     [Google Scholar]
  66. Lease R. A., Cusick M. E., Belfort M. 1998; Riboregulation in Escherichia coli : DsrA RNA acts by RNA : RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95:12456–12461
     [Google Scholar]
  67. Lee S. H., Hava D. L., Waldor M. K., Camilli A. 1999; Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99:625–634
     [Google Scholar]
  68. Libby S. J., Goebel W., Ludwig A., Buchmeier N., Bowe F., Fang F. C., Guiney D. G., Songer J. G., Heffron F. 1994; A cytolysin encoded by Salmonella is required for survival within macrophages. Proc Natl Acad Sci U S A 91:489–493
     [Google Scholar]
  69. Lithgow J. K., Haider F., Roberts I. S., Green J. 2007; Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol Microbiol 66:685–698
     [Google Scholar]
  70. Liu Q., Richardson C. C. 1993; Gene 5.5 protein of bacteriophage T7 inhibits the nucleoid protein H-NS of Escherichia coli . Proc Natl Acad Sci U S A 90:1761–1765
     [Google Scholar]
  71. 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]
  72. Madhusudan S., Paukner A., Klingen Y., Schnetz K. 2005; Independent regulation of H-NS-mediated silencing of the bgl operon at two levels: upstream by BglJ and LeuO and downstream by DnaKJ. Microbiology 151:3349–3359
     [Google Scholar]
  73. Majdalani N., Cunning C., Sledjeski D., Elliott T., Gottesman S. 1998; DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci U S A 95:12462–12467
     [Google Scholar]
  74. 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]
  75. Mayer O., Rajkowitsch L., Lorenz C., Konrat R., Schroeder R. 2007; RNA chaperone activity and RNA-binding properties of the E. coli protein StpA. Nucleic Acids Res 35:1257–1269
     [Google Scholar]
  76. McFeeters R. L., Altieri A. S., Cherry S., Tropea J. E., Waugh D. S., Byrd R. A. 2007; The high-precision solution structure of Yersinia modulating protein YmoA provides insight into interaction with H-NS. Biochemistry 46:13975–13982
     [Google Scholar]
  77. McGovern V., Higgins N. P., Chiz R. S., Jaworski A. 1994; H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie 76:1019–1029
     [Google Scholar]
  78. McKenna S., Beloin C., Dorman C. J. 2003; In vitro DNA binding properties of VirB, the Shigella flexneri virulence regulatory protein. FEBS Lett 545:183–187
     [Google Scholar]
  79. McLeod S. M., Kimsey H. H., Davis B. M., Waldor M. K. 2005; CTXphi and Vibrio cholerae : exploring a newly recognized type of phage–host cell relationship. Mol Microbiol 57:347–356
     [Google Scholar]
  80. Mikulskis A. V., Cornelis G. R. 1994; A new class of proteins regulating gene expression in enterobacteria. Mol Microbiol 11:77–86
     [Google Scholar]
  81. Morse R. H. 2007; Transcription factor access to promoter elements. J Cell Biochem 102:560–567
     [Google Scholar]
  82. Müller C. M., Dobrindt U., Nagy G., Emödy L., Uhlin B. E., Hacker J. 2006; Role of histone-like proteins H-NS and StpA in expression of virulence determinants of uropathogenic Escherichia coli . J Bacteriol 188:5428–5438
     [Google Scholar]
  83. Murphree D., Froehlich B., Scott J. R. 1997; Transcriptional control of genes encoding CS1 pili: negative regulation by a silencer and positive regulation by Rns. J Bacteriol 179:5736–5743
     [Google Scholar]
  84. Murphy R. A., Boyd E. F. 2008; Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates. J Bacteriol 190:636–647
     [Google Scholar]
  85. Nasser W., Reverchon S. 2002; H-NS-dependent activation of pectate lyases synthesis in the phytopathogenic bacterium Erwinia chrysanthemi is mediated by the PecT repressor. Mol Microbiol 43:733–748
     [Google Scholar]
  86. Navarre W. W., Halsey T. A., Walthers D., Frye J., McClelland M., Potter J. L., Kenney L. J., Gunn J. S., Fang F. C., Libby S. J. 2005; Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 56:492–508
     [Google Scholar]
  87. 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]
  88. Navarre W. W., McClelland M., Libby S. J., Fang F. C. 2007; Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21:1456–1471
     [Google Scholar]
  89. Nickerson C. A., Achberger E. C. 1995; Role of curved DNA in binding of Escherichia coli RNA polymerase to promoters. J Bacteriol 177:5756–5761
     [Google Scholar]
  90. Nieto J. M., Madrid C., Prenafeta A., Miquelay E., Balsalobre C., Carrascal M., Juárez A. 2000; Expression of the hemolysin operon in Escherichia coli is modulated by a nucleoid–protein complex that includes the proteins Hha and H-NS. Mol Gen Genet 263:349–358
     [Google Scholar]
  91. Nieto J. M., Madrid C., Miquelay E., Parra J. L., Rodríguez S., Juárez 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
     [Google Scholar]
  92. Noom M. C., Navarre W. W., Oshima T., Wuite G. J., Dame R. T. 2007; H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17:R913–R914
     [Google Scholar]
  93. Norte V. A., Stapleton M. R., Green J. 2003; PhoP-responsive expression of the Salmonella enterica serovar typhimurium slyA gene. J Bacteriol 185:3508–3514
     [Google Scholar]
  94. Nye M. B., Pfau J. D., Skorupski K., Taylor R. K. 2000; Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. J Bacteriol 182:4295–4303
     [Google Scholar]
  95. O'Byrne C. P., Dorman C. J. 1994; Transcription of the Salmonella typhimurium spv virulence locus is regulated negatively by the nucleoid-associated protein H-NS. FEMS Microbiol Lett 121:99–105
     [Google Scholar]
  96. Olekhnovich I. N., Kadner R. J. 2007; Role of nucleoid-associated proteins Hha and H-NS in expression of Salmonella enterica activators HilD, HilC, and RtsA required for cell invasion. J Bacteriol 189:6882–6890
     [Google Scholar]
  97. Oshima T., Ishikawa S., Kurokawa K., Aiba H., Ogasawara N. 2006; Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13:141–153
     [Google Scholar]
  98. Paytubi S., Madrid C., Forns N., Nieto J. M., Balsalobre C., Uhlin B. E., Juárez A. 2004; YdgT, the Hha paralogue in Escherichia coli , forms heteromeric complexes with H-NS and StpA. Mol Microbiol 54:251–263
     [Google Scholar]
  99. Perez J. C., Latifi T., Groisman E. A. 2008; Overcoming H-NS-mediated transcriptional silencing of horizontally-acquired genes by the PhoP and SlyA proteins in Salmonella enterica . J Biol Chem 283:10773–10783
     [Google Scholar]
  100. Petersen C., Møller L. B., Valentin-Hansen P. 2002; The cryptic adenine deaminase gene of Escherichia coli . Silencing by the nucleoid-associated DNA-binding protein, H-NS, and activation by insertion elements. J Biol Chem 277:31373–31380
     [Google Scholar]
  101. Poore C. A., Mobley H. L. 2003; Differential regulation of the Proteus mirabilis urease gene cluster by UreR and H-NS. Microbiology 149:3383–3394
     [Google Scholar]
  102. Porter M. E., Dorman C. J. 2002; In vivo DNA-binding and oligomerization properties of the Shigella flexneri AraC-like transcriptional regulator VirF as identified by random and site-specific mutagenesis. J Bacteriol 184:531–539
     [Google Scholar]
  103. Porter M. E., Mitchell P., Roe A. J., Free A., Smith D. G., Gally D. L. 2004; Direct and indirect transcriptional activation of virulence genes by an AraC-like protein, PerA from enteropathogenic Escherichia coli . Mol Microbiol 54:1117–1133
     [Google Scholar]
  104. 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]
  105. Revell P. A., Miller V. L. 2000; A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence. Mol Microbiol 35:677–685
     [Google Scholar]
  106. Reverchon S., Nasser W., Robert-Baudouy J. 1994; pecS : a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi . Mol Microbiol 11:1127–1139
     [Google Scholar]
  107. Rhen M., Dorman C. J. 2005; Hierarchical gene regulators adapt Salmonella enterica to its host milieus. Int J Med Microbiol 294:487–502
     [Google Scholar]
  108. Rimsky S. 2004; Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. Curr Opin Microbiol 7:109–114
     [Google Scholar]
  109. Rimsky S., Zuber F., Buckle M., Buc H. 2001; A molecular mechanism for the repression of transcription by the H-NS protein. Mol Microbiol 42:1311–1323
     [Google Scholar]
  110. Rine J. 1999; On the mechanism of silencing in Escherichia coli . Proc Natl Acad Sci U S A 96:8309–8311
     [Google Scholar]
  111. Rodionov O., Yarmolinsky M. 2004; Plasmid partitioning and the spreading of P1 partition protein ParB. Mol Microbiol 52:1215–1223
     [Google Scholar]
  112. Rodionov O., Lobocka M., Yarmolinsky M. 1999; Silencing of genes flanking the P1 plasmid centromere. Science 283:546–549
     [Google Scholar]
  113. Schild S., Tamayo R., Nelson E. J., Qadri F., Calderwood S. B., Camilli A. 2007; Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2:264–277
     [Google Scholar]
  114. Schneider D. A., Ross W., Gourse R. L. 2003; Control of rRNA expression in Escherichia coli . Curr Opin Microbiol 6:151–156
     [Google Scholar]
  115. Schröder O., Wagner R. 2000; The bacterial DNA-binding protein H-NS represses ribosomal RNA transcription by trapping RNA polymerase in the initiation complex. J Mol Biol 298:737–748
     [Google Scholar]
  116. Shi Y., Latifi T., Cromie M. J., Groisman E. A. 2004; Transcriptional control of the antimicrobial peptide resistance ugtL gene by the Salmonellas PhoP and SlyA regulatory proteins. J Biol Chem 279:38618–38625
     [Google Scholar]
  117. Shin M., Song M., Rhee J. H., Hong Y., Kim Y. J., Seok Y. J., Ha K. S., Jung S. H., Choy H. E. 2005; DNA looping-mediated repression by histonelike protein H-NS: specific requirement of E σ 70 as a cofactor for looping. Genes Dev 19:2388–2398
     [Google Scholar]
  118. Silphaduang U., Mascarenhas M., Karmali M., Coombes B. K. 2007; Repression of intracellular virulence factors in Salmonella by the Hha and YdgT nucleoid-associated proteins. J Bacteriol 189:3669–3673
     [Google Scholar]
  119. Sinden R. R., Pearson C. E., Potaman V. N., Ussery D. W. 1998; DNA: structure and function. Adv Genome Biol 5A:1–141
     [Google Scholar]
  120. Skorupski K., Taylor R. K. 1997; Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol Microbiol 25:1003–1009
     [Google Scholar]
  121. Sledjeski D., Gottesman S. 1995; A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli . Proc Natl Acad Sci U S A 92:2003–2007
     [Google Scholar]
  122. Spory A., Bosserhoff A., von Rhein C., Goebel W., Ludwig A. 2002; Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. J Bacteriol 184:3549–3559
     [Google Scholar]
  123. Stapleton M. R., Norte V. A., Read R. C., Green J. 2002; Interaction of the Salmonella typhimurium transcription and virulence factor SlyA with target DNA and identification of members of the SlyA regulon. J Biol Chem 277:17630–17637
     [Google Scholar]
  124. Stoebel D. M., Dean A. M., Dykhuizen D. E. 2008; The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178:1653–1660
     [Google Scholar]
  125. Stratmann T., Madhusudan S., Schnetz K. 2008; Regulation of the yjjQ-bglJ operon, encoding LuxR-type transcription factors, and the divergent yjjP gene by H-NS and LeuO. J Bacteriol 190:926–935
     [Google Scholar]
  126. Taniya T., Mitobe J., Nakayama S., Mingshan Q., Okuda K., Watanabe H. 2003; Determination of the InvE binding site required for expression of IpaB of the Shigella sonnei virulence plasmid: involvement of a ParB BoxA-like sequence. J Bacteriol 185:5158–5165
     [Google Scholar]
  127. Tendeng C., Bertin P. N. 2003; H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11:511–518
     [Google Scholar]
  128. Tobe T., Yoshikawa M., Sasakawa C. 1995; Thermoregulation of virB transcription in Shigella flexneri by sensing of changes in local DNA superhelicity. J Bacteriol 177:1094–1097
     [Google Scholar]
  129. Tolstorukov M. Y., Virnik K. M., Adhya S., Zhurkin V. B. 2005; A-tract clusters may facilitate DNA packaging in bacterial nucleoid. Nucleic Acids Res 33:3907–3918
     [Google Scholar]
  130. Torres A. G., López-Sánchez G. N., Milflores-Flores L., Patel S. D., Rojas-López M., Martínez de la Peña C. F., Arenas-Hernández M. M., Martínez-Laguna Y. 2007; Ler and H-NS, regulators controlling expression of the long polar fimbriae of Escherichia coli O157 : H7. J Bacteriol 189:5916–5928
     [Google Scholar]
  131. Tramonti A., De Canio M., Delany I., Scarlato V., De Biase D. 2006; Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli . J Bacteriol 188:8118–8127
     [Google Scholar]
  132. Turner E. C., Dorman C. J. 2007; H-NS antagonism in Shigella flexneri by VirB, a virulence gene transcription regulator that is closely related to plasmid partition factors. J Bacteriol 189:3403–3413
     [Google Scholar]
  133. Ueguchi C., Ohta T., Seto C., Suzuki T., Mizuno T. 1998; The leuO gene product has a latent ability to relieve bgl silencing in Escherichia coli . J Bacteriol 180:190–193
     [Google Scholar]
  134. Umanski T., Rosenshine I., Friedberg D. 2002; Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli . Microbiology 148:2735–2744
     [Google Scholar]
  135. van Noort J., Verbrugge S., Goosen N., Dekker C., Dame R. T. 2004; Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci U S A 101:6969–6974
     [Google Scholar]
  136. Vivero A., Baños R. C., Mariscotti J. F., Oliveros J. C., García-del Portillo F., Juárez A., Madrid C. 2008; Modulation of horizontally acquired genes by the Hha-YdgT proteins in Salmonella enterica serovar Typhimurium. J Bacteriol 190:1152–1156
     [Google Scholar]
  137. Wade J. T., Struhl K., Busby S. J. W., Grainger D. C. 2007; Genomic analysis of protein–DNA interactions in bacteria: insights into transcription and chromosome organization. Mol Microbiol 65:21–26
     [Google Scholar]
  138. Wagner R. 2000 Transcription Regulation in Prokaryotes Oxford, UK: Oxford University Press;
     [Google Scholar]
  139. Walthers D., Carroll R. K., Navarre W. W., Libby S. J., Fang F. C., Kenney L. J. 2007; The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid-associated protein H-NS. Mol Microbiol 65:477–493
     [Google Scholar]
  140. Westermark M., Oscarsson J., Mizunoe Y., Urbonaviciene J., Uhlin B. E. 2000; Silencing and activation of ClyA cytotoxin expression in Escherichia coli . J Bacteriol 182:6347–6357
     [Google Scholar]
  141. Wilkinson S. P., Grove A. 2006; Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr Issues Mol Biol 8:51–62
     [Google Scholar]
  142. Will W. R., Lu J., Frost L. S. 2004; The role of H-NS in silencing F transfer gene expression during entry into stationary phase. Mol Microbiol 54:769–782
     [Google Scholar]
  143. 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]
  144. Williamson H. S., Free A. 2005; A truncated H-NS-like protein from enteropathogenic Escherichia coli acts as an H-NS antagonist. Mol Microbiol 55:808–827
     [Google Scholar]
  145. Wolf T., Janzen W., Blum C., Schnetz K. 2006; Differential dependence of StpA on H-NS in autoregulation of stpA and in regulation of bgl . J Bacteriol 188:6728–6738
     [Google Scholar]
  146. Yamada H., Muramatsu S., Mizuno T. 1990; An Escherichia coli protein that preferentially binds to sharply curved DNA. J Biochem 108:420–425
     [Google Scholar]
  147. Yang J., Hart E., Tauschek M., Price G. D., Hartland E. L., Strugnell R. A., Robins-Browne R. M. 2008; Bicarbonate-mediated transcriptional activation of divergent operons by the virulence regulatory protein, RegA, from Citrobacter rodentium . Mol Microbiol 68:314–327
     [Google Scholar]
  148. Yarmolinsky M. 2000; Transcriptional silencing in bacteria. Curr Opin Microbiol 3:138–143
     [Google Scholar]
  149. Yu R. R., DiRita V. J. 2002; Regulation of gene expression in Vibrio cholerae by ToxT involves both antirepression and RNA polymerase stimulation. Mol Microbiol 43:119–134
     [Google Scholar]
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Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria
Microbiology 154, 2533 (2008); https://doi.org/10.1099/mic.0.2008/020693-0
/content/journal/micro/10.1099/mic.0.2008/020693-0
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