1887

Abstract

causes whooping cough, an infectious disease that is reemerging despite widespread vaccination. A more complete understanding of pathogenic mechanisms will involve unravelling the regulation of its impressive arsenal of virulence factors. Here we review the action of the response regulator BvgA in the context of what is known about bacterial RNA polymerase and various modes of transcription activation. At most virulence gene promoters, multiple dimers of phosphorylated BvgA (BvgA~P) bind upstream of the core promoter sequence, using a combination of high- and low-affinity sites that fill through cooperativity. Activation by BvgA~P is typically mediated by a novel form of class I/II mechanisms, but two virulence genes, and , which encode serologically distinct fimbrial subunits, are regulated using a previously unrecognized RNA polymerase/activator architecture. In addition, the genes undergo phase variation because of an extended cytosine (C) tract within the promoter sequences that is subject to slipped-strand mispairing during replication. These sophisticated systems of regulation demonstrate one aspect whereby , which is highly clonal and lacks the extensive genetic diversity observed in many other bacterial pathogens, has been highly successful as an obligate human pathogen.

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2012-07-01
2024-12-07
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References

  1. Akerley B. J., Cotter P. A., Miller J. F. ( 1995). Ectopic expression of the flagellar regulon alters development of the Bordetella–host interaction. Cell 80:611–620 [View Article][PubMed]
    [Google Scholar]
  2. Barnard A., Wolfe A., Busby S. ( 2004). Regulation at complex bacterial promoters: how bacteria use different promoter organizations to produce different regulatory outcomes. Curr Opin Microbiol 7:102–108 [View Article][PubMed]
    [Google Scholar]
  3. Baxter K., Lee J., Minakhin L., Severinov K., Hinton D. M. ( 2006). Mutational analysis of sigma70 region 4 needed for appropriation by the bacteriophage T4 transcription factors AsiA and MotA. J Mol Biol 363:931–944 [View Article][PubMed]
    [Google Scholar]
  4. Benoff B., Yang H., Lawson C. L., Parkinson G., Liu J., Blatter E., Ebright Y. W., Berman H. M., Ebright R. H. ( 2002). Structural basis of transcription activation: the CAP-alpha CTD-DNA complex. Science 297:1562–1566 [View Article][PubMed]
    [Google Scholar]
  5. Blanco A. G., Canals A., Bernués J., Solà M., Coll M. ( 2011). The structure of a transcription activation subcomplex reveals how σ70 is recruited to PhoB promoters. EMBO J 30:3776–3785 [View Article][PubMed]
    [Google Scholar]
  6. Bonocora R. P., Caignan G., Woodrell C., Werner M. H., Hinton D. M. ( 2008). A basic/hydrophobic cleft of the T4 activator MotA interacts with the C-terminus of E. coli sigma70 to activate middle gene transcription. Mol Microbiol 69:331–343 [View Article][PubMed]
    [Google Scholar]
  7. Bootsma H. J., Cummings C. A., Relman D. A., Miller J. F. ( 2002).National Meeting of the American Society for Microbiology
  8. Bordet J., Gengou O. ( 1906). Le microbe de la coqueluche. Ann Inst Pasteur (Paris) 20:731–741
    [Google Scholar]
  9. Boucher P. E., Stibitz S. ( 1995). Synergistic binding of RNA polymerase and BvgA phosphate to the pertussis toxin promoter of Bordetella pertussis . J Bacteriol 177:6486–6491[PubMed]
    [Google Scholar]
  10. Boucher P. E., Menozzi F. D., Locht C. ( 1994). The modular architecture of bacterial response regulators. Insights into the activation mechanism of the BvgA transactivator of Bordetella pertussis . J Mol Biol 241:363–377 [View Article][PubMed]
    [Google Scholar]
  11. Boucher P. E., Murakami K., Ishihama A., Stibitz S. ( 1997). Nature of DNA binding and RNA polymerase interaction of the Bordetella pertussis BvgA transcriptional activator at the fha promoter. J Bacteriol 179:1755–1763[PubMed]
    [Google Scholar]
  12. Boucher P. E., Yang M. S., Schmidt D. M., Stibitz S. ( 2001). Genetic and biochemical analyses of BvgA interaction with the secondary binding region of the fha promoter of Bordetella pertussis . J Bacteriol 183:536–544 [View Article][PubMed]
    [Google Scholar]
  13. Boucher P. E., Maris A. E., Yang M. S., Stibitz S. ( 2003). The response regulator BvgA and RNA polymerase alpha subunit C-terminal domain bind simultaneously to different faces of the same segment of promoter DNA. Mol Cell 11:163–173 [View Article][PubMed]
    [Google Scholar]
  14. Bouchez V., Caro V., Levillain E., Guigon G., Guiso N. ( 2008). Genomic content of Bordetella pertussis clinical isolates circulating in areas of intensive children vaccination. PLoS ONE 3:e2437 [View Article][PubMed]
    [Google Scholar]
  15. Bouchez V., Brun D., Cantinelli T., Dore G., Njamkepo E., Guiso N. ( 2009). First report and detailed characterization of B. pertussis isolates not expressing Pertussis Toxin or Pertactin. Vaccine 27:6034–6041 [View Article][PubMed]
    [Google Scholar]
  16. Brinig M. M., Cummings C. A., Sanden G. N., Stefanelli P., Lawrence A., Relman D. A. ( 2006). Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J Bacteriol 188:2375–2382 [View Article][PubMed]
    [Google Scholar]
  17. Browning D. F., Busby S. J. ( 2004). The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57–65 [View Article][PubMed]
    [Google Scholar]
  18. Campbell E. A., Muzzin O., Chlenov M., Sun J. L., Olson C. A., Weinman O., Trester-Zedlitz M. L., Darst S. A. ( 2002). Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell 9:527–539 [View Article][PubMed]
    [Google Scholar]
  19. Caro V., Hot D., Guigon G., Hubans C., Arrivé M., Soubigou G., Renauld-Mongénie G., Antoine R., Locht C. et al. ( 2006). Temporal analysis of French Bordetella pertussis isolates by comparative whole-genome hybridization. Microbes Infect 8:2228–2235 [View Article][PubMed]
    [Google Scholar]
  20. CDC ( 1995). Pertussis–United States, January 1992–June 1995. MMWR Morb Mortal Wkly Rep 44:525–529[PubMed]
    [Google Scholar]
  21. CDC ( 2011). Pertussis (Whooping Cough) www.cdc.gov/vaccines/pubs/pinkbook/pert.html
    [Google Scholar]
  22. Chen Q., Decker K. B., Boucher P. E., Hinton D., Stibitz S. ( 2010). Novel architectural features of Bordetella pertussis fimbrial subunit promoters and their activation by the global virulence regulator BvgA. Mol Microbiol 77:1326–1340 [View Article][PubMed]
    [Google Scholar]
  23. Cotter P. A., DiRita V. J. ( 2000). Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54:519–565 [View Article][PubMed]
    [Google Scholar]
  24. Cotter P. A., Jones A. M. ( 2003). Phosphorelay control of virulence gene expression in Bordetella . Trends Microbiol 11:367–373 [View Article][PubMed]
    [Google Scholar]
  25. Cotter P. A., Miller J. F. ( 1994). BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62:3381–3390[PubMed]
    [Google Scholar]
  26. de Melker H. E., Schellekens J. F. P., Neppelenbroek S. E., Mooi F. R., Rümke H. C., Conyn-van Spaendonck M. A. E. ( 2000). Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis 6:348–357 [View Article][PubMed]
    [Google Scholar]
  27. Decker K. B., Chen Q., Hsieh M. L., Boucher P., Stibitz S., Hinton D. M. ( 2011). Different requirements for σ Region 4 in BvgA activation of the Bordetella pertussis promoters P(fim3) and P(fhaB). J Mol Biol 409:692–709 [View Article][PubMed]
    [Google Scholar]
  28. Diavatopoulos D. A., Cummings C. A., Schouls L. M., Brinig M. M., Relman D. A., Mooi F. R. ( 2005). Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica . PLoS Pathog 1:e45 [View Article][PubMed]
    [Google Scholar]
  29. Dorman C. J. ( 1995). 1995 Fleming Lecture. DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology 141:1271–1280 [View Article][PubMed]
    [Google Scholar]
  30. Dove S. L., Darst S. A., Hochschild A. ( 2003). Region 4 of sigma as a target for transcription regulation. Mol Microbiol 48:863–874 [View Article][PubMed]
    [Google Scholar]
  31. Dybvig K. ( 1993). DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10:465–471 [View Article][PubMed]
    [Google Scholar]
  32. Galperin M. Y. ( 2010). Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13:150–159 [View Article][PubMed]
    [Google Scholar]
  33. Gangarosa E. J., Galazka A. M., Wolfe C. R., Phillips L. M., Gangarosa R. E., Miller E., Chen R. T. ( 1998). Impact of anti-vaccine movements on pertussis control: the untold story. Lancet 351:356–361 [View Article][PubMed]
    [Google Scholar]
  34. García San Miguel L., Quereda C., Martínez M., Martín-Dávila P., Cobo J., Guerrero A. ( 1998). Bordetella bronchiseptica cavitary pneumonia in a patient with AIDS. Eur J Clin Microbiol Infect Dis 17:675–676[PubMed] [CrossRef]
    [Google Scholar]
  35. Geier D., Geier M. ( 2002). The true story of pertussis vaccination: a sordid legacy?. J Hist Med Allied Sci 57:249–284 [View Article][PubMed]
    [Google Scholar]
  36. Gerlach G., von Wintzingerode F., Middendorf B., Gross R. ( 2001). Evolutionary trends in the genus Bordetella . Microbes Infect 3:61–72 [View Article][PubMed]
    [Google Scholar]
  37. Geuijen C. A., Willems R. J., Bongaerts M., Top J., Gielen H., Mooi F. R. ( 1997). Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun 65:4222–4228[PubMed]
    [Google Scholar]
  38. Gogol E. B., Cummings C. A., Burns R. C., Relman D. A. ( 2007). Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis . BMC Genomics 8:122 [View Article][PubMed]
    [Google Scholar]
  39. 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 [View Article][PubMed]
    [Google Scholar]
  40. Gries T. J., Kontur W. S., Capp M. W., Saecker R. M., Record M. T. Jr ( 2010). One-step DNA melting in the RNA polymerase cleft opens the initiation bubble to form an unstable open complex. Proc Natl Acad Sci U S A 107:10418–10423 [View Article][PubMed]
    [Google Scholar]
  41. Gruber T. M., Gross C. A. ( 2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466 [View Article][PubMed]
    [Google Scholar]
  42. Halperin S. A. ( 2007). The control of pertussis–2007 and beyond. N Engl J Med 356:110–113 [View Article][PubMed]
    [Google Scholar]
  43. Heck D. V., Trus B. L., Steven A. C. ( 1996). Three-dimensional structure of Bordetella pertussis fimbriae. J Struct Biol 116:264–269 [View Article][PubMed]
    [Google Scholar]
  44. Heikkinen E., Kallonen T., Saarinen L., Sara R., King A. J., Mooi F. R., Soini J. T., Mertsola J., He Q. S. ( 2007). Comparative genomics of Bordetella pertussis reveals progressive gene loss in Finnish strains. PLoS ONE 2:e904 [View Article][PubMed]
    [Google Scholar]
  45. Heikkinen E., Xing D. K., Olander R. M., Hytönen J., Viljanen M. K., Mertsola J., He Q. ( 2008). Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol 8:162 [View Article][PubMed]
    [Google Scholar]
  46. Henderson I. R., Owen P., Nataro J. P. ( 1999). Molecular switches – the ON and OFF of bacterial phase variation. Mol Microbiol 33:919–932 [View Article][PubMed]
    [Google Scholar]
  47. Herrou J., Debrie A. S., Willery E., Renauld-Mongénie G., Locht C., Mooi F., Jacob-Dubuisson F., Antoine R. ( 2009). Molecular evolution of the two-component system BvgAS involved in virulence regulation in Bordetella . PLoS ONE 4:e6996 [View Article][PubMed]
    [Google Scholar]
  48. Hinton D. M. ( 2010). Transcriptional control in the prereplicative phase of T4 development. Virol J 7:289 [View Article][PubMed]
    [Google Scholar]
  49. Hobman J. L., Wilkie J., Brown N. L. ( 2005). A design for life: prokaryotic metal-binding MerR family regulators. Biometals 18:429–436 [View Article][PubMed]
    [Google Scholar]
  50. Hook-Barnard I. G., Hinton D. M. ( 2007). Transcription initiation by mix and match elements: flexibility for polymerase binding to bacterial promoters. Gene Regul Syst Bio 1:275–293[PubMed]
    [Google Scholar]
  51. Jain D., Kim Y., Maxwell K. L., Beasley S., Zhang R., Gussin G. N., Edwards A. M., Darst S. A. ( 2005). Crystal structure of bacteriophage lambda cII and its DNA complex. Mol Cell 19:259–269 [View Article][PubMed]
    [Google Scholar]
  52. Karimova G., Ullmann A. ( 1997). Characterization of DNA binding sites for the BvgA protein of Bordetella pertussis . J Bacteriol 179:3790–3792[PubMed]
    [Google Scholar]
  53. Karimova G., Bellalou J., Ullmann A. ( 1996). Phosphorylation-dependent binding of BvgA to the upstream region of the cyaA gene of Bordetella pertussis . Mol Microbiol 20:489–496 [View Article][PubMed]
    [Google Scholar]
  54. Kerr J. R., Matthews R. C. ( 2000). Bordetella pertussis infection: pathogenesis, diagnosis, management, and the role of protective immunity. Eur J Clin Microbiol Infect Dis 19:77–88 [View Article][PubMed]
    [Google Scholar]
  55. Kinnear S. M., Boucher P. E., Stibitz S., Carbonetti N. H. ( 1999). Analysis of BvgA activation of the pertactin gene promoter in Bordetella pertussis . J Bacteriol 181:5234–5241[PubMed]
    [Google Scholar]
  56. Kinnear S. M., Marques R. R., Carbonetti N. H. ( 2001). Differential regulation of Bvg-activated virulence factors plays a role in Bordetella pertussis pathogenicity. Infect Immun 69:1983–1993 [View Article][PubMed]
    [Google Scholar]
  57. Kontur W. S., Saecker R. M., Capp M. W., Record M. T. Jr ( 2008). Late steps in the formation of E. coli RNA polymerase-λPR promoter open complexes: characterization of conformational changes by rapid [perturbant] upshift experiments. J Mol Biol 376:1034–1047 [View Article][PubMed]
    [Google Scholar]
  58. Lacey B. W. ( 1960). Antigenic modulation of Bordetella pertussis . J Hyg (Lond) 58:57–93 [View Article][PubMed]
    [Google Scholar]
  59. Lambert L. J., Wei Y., Schirf V., Demeler B., Werner M. H. ( 2004). T4 AsiA blocks DNA recognition by remodeling sigma70 region 4. EMBO J 23:2952–2962 [View Article][PubMed]
    [Google Scholar]
  60. Lawson C. L., Swigon D., Murakami K. S., Darst S. A., Berman H. M., Ebright R. H. ( 2004). Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 14:10–20 [View Article][PubMed]
    [Google Scholar]
  61. Levinson G., Gutman G. A. ( 1987). Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221[PubMed]
    [Google Scholar]
  62. Locht C., Antoine R., Jacob-Dubuisson F. ( 2001). Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 4:82–89 [View Article][PubMed]
    [Google Scholar]
  63. Marques R. R., Carbonetti N. H. ( 1997). Genetic analysis of pertussis toxin promoter activation in Bordetella pertussis . Mol Microbiol 24:1215–1224 [View Article][PubMed]
    [Google Scholar]
  64. Marteyn B., West N. P., Browning D. F., Cole J. A., Shaw J. G., Palm F., Mounier J., Prévost M. C., Sansonetti P., Tang C. M. ( 2010). Modulation of Shigella virulence in response to available oxygen in vivo . Nature 465:355–358 [View Article][PubMed]
    [Google Scholar]
  65. Mattoo S., Foreman-Wykert A. K., Cotter P. A., Miller J. F. ( 2001). Mechanisms of Bordetella pathogenesis . Front Biosci 6:e168–e186 [View Article][PubMed]
    [Google Scholar]
  66. Merkel T. J., Stibitz S., Keith J. M., Leef M., Shahin R. ( 1998). Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis . Infect Immun 66:4367–4373[PubMed]
    [Google Scholar]
  67. Merkel T. J., Boucher P. E., Stibitz S., Grippe V. K. ( 2003). Analysis of bvgR expression in Bordetella pertussis . J Bacteriol 185:6902–6912 [View Article][PubMed]
    [Google Scholar]
  68. Mooi F. R., van der Heide H. G. J., ter Avest A. R., Welinder K. G., Livey I., van der Zeijst B. A. M., Gaastra W. ( 1987). Characterization of fimbrial subunits from Bordetella species. Microb Pathog 2:473–484 [View Article][PubMed]
    [Google Scholar]
  69. Mooi F. R., Jansen W. H., Brunings H., Gielen H., van der Heide H. G. J., Walvoort H. C., Guinee P. A. M. ( 1992). Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb Pathog 12:127–135 [View Article][PubMed]
    [Google Scholar]
  70. Mooi F. R., van Loo I. H. M., van Gent M., He Q., Bart M. J., Heuvelman K. J., de Greeff S. C., Diavatopoulos D., Teunis P. et al. ( 2009). Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis 15:1206–1213 [View Article][PubMed]
    [Google Scholar]
  71. Parkhill J., Sebaihia M., Preston A., Murphy L. D., Thomson N., Harris D. E., Holden M. T., Churcher C. M., Bentley S. D. et al. ( 2003). Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica . Nat Genet 35:32–40 [View Article][PubMed]
    [Google Scholar]
  72. Proulx F., Toledano B., Phan V., Clermont M. J., Mariscalco M. M., Seidman E. G. ( 2002). Circulating granulocyte colony-stimulating factor, C-X-C, and C-C chemokines in children with Escherichia coli O157:H7 associated hemolytic uremic syndrome. Pediatr Res 52:928–934[PubMed] [CrossRef]
    [Google Scholar]
  73. Rhen M., Dorman C. J. ( 2005). Hierarchical gene regulators adapt Salmonella enterica to its host milieus. Int J Med Microbiol 294:487–502 [View Article][PubMed]
    [Google Scholar]
  74. Riboli B., Pedroni P., Cuzzoni A., Grandi G., de Ferra F. ( 1991). Expression of Bordetella pertussis fimbrial (fim) genes in Bordetella bronchiseptica: fimX is expressed at a low level and vir-regulated. Microb Pathog 10:393–403 [View Article][PubMed]
    [Google Scholar]
  75. Roy C. R., Falkow S. ( 1991). Identification of Bordetella pertussis regulatory sequences required for transcriptional activation of the fhaB gene and autoregulation of the bvgAS operon. J Bacteriol 173:2385–2392[PubMed]
    [Google Scholar]
  76. Saecker R. M., Tsodikov O. V., McQuade K. L., Schlax P. E. Jr, Capp M. W., Record M. T. Jr ( 2002). Kinetic studies and structural models of the association of E. coli sigma(70) RNA polymerase with the lambdaP(R) promoter: large scale conformational changes in forming the kinetically significant intermediates. J Mol Biol 319:649–671 [View Article][PubMed]
    [Google Scholar]
  77. Scarlato V., Aricò B., Prugnola A., Rappuoli R. ( 1991). Sequential activation and environmental regulation of virulence genes in Bordetella pertussis . EMBO J 10:3971–3975[PubMed]
    [Google Scholar]
  78. Seifert H. S., So M. ( 1988). Genetic mechanisms of bacterial antigenic variation. Microbiol Rev 52:327–336[PubMed]
    [Google Scholar]
  79. Steffen P., Ullmann A. ( 1998). Hybrid Bordetella pertussisEscherichia coli RNA polymerases: selectivity of promoter activation. J Bacteriol 180:1567–1569[PubMed]
    [Google Scholar]
  80. Steffen P., Goyard S., Ullmann A. ( 1996). Phosphorylated BvgA is sufficient for transcriptional activation of virulence-regulated genes in Bordetella pertussis . EMBO J 15:102–109[PubMed]
    [Google Scholar]
  81. Stibitz S., Aaronson W., Monack D., Falkow S. ( 1989). Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338:266–269 [View Article][PubMed]
    [Google Scholar]
  82. Stock A. M., Robinson V. L., Goudreau P. N. ( 2000). Two-component signal transduction. Annu Rev Biochem 69:183–215 [View Article][PubMed]
    [Google Scholar]
  83. Streisinger G., Owen J. ( 1985). Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4. Genetics 109:633–659[PubMed]
    [Google Scholar]
  84. Swanson M. S., Hammer B. K. ( 2000). Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54:567–613 [View Article][PubMed]
    [Google Scholar]
  85. Tsang R. S. W., Lau A. K. H., Sill M. L., Halperin S. A., Van Caeseele P., Jamieson F., Martin I. E. ( 2004). Polymorphisms of the fimbria fim3 gene of Bordetella pertussis strains isolated in Canada. J Clin Microbiol 42:5364–5367 [View Article][PubMed]
    [Google Scholar]
  86. Uhl M. A., Miller J. F. ( 1996). Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J 15:1028–1036[PubMed]
    [Google Scholar]
  87. van Loo I. H. M., Heuvelman K. J., King A. J., Mooi F. R. ( 2002). Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J Clin Microbiol 40:1994–2001 [View Article][PubMed]
    [Google Scholar]
  88. von Wintzingerode F., Schattke A., Siddiqui R. A., Rösick U., Göbel U. B., Gross R. ( 2001). Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella . Int J Syst Evol Microbiol 51:1257–1265[PubMed] [CrossRef]
    [Google Scholar]
  89. Watanabe S., Kita A., Kobayashi K., Miki K. ( 2008). Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc Natl Acad Sci U S A 105:4121–4126 [View Article][PubMed]
    [Google Scholar]
  90. Willems R., Paul A., van der Heide H. G., ter Avest A. R., Mooi F. R. ( 1990). Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J 9:2803–2809[PubMed]
    [Google Scholar]
  91. Williams C. L., Boucher P. E., Stibitz S., Cotter P. A. ( 2005). BvgA functions as both an activator and a repressor to control Bvg phase expression of bipA in Bordetella pertussis . Mol Microbiol 56:175–188 [View Article][PubMed]
    [Google Scholar]
  92. Yang Z. X., Zhou Y. N., Yang Y., Jin D. J. ( 2010). Polyphosphate binds to the principal sigma factor of RNA polymerase during starvation response in Helicobacter pylori . Mol Microbiol 77:618–627 [View Article][PubMed]
    [Google Scholar]
  93. Zu T., Manetti R., Rappuoli R., Scarlato V. ( 1996). Differential binding of BvgA to two classes of virulence genes of Bordetella pertussis directs promoter selectivity by RNA polymerase. Mol Microbiol 21:557–565 [View Article][PubMed]
    [Google Scholar]
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