1887

Abstract

Bordetella pertussis, a human pathogenic bacterium, produces either one or two types of serologically distinct fimbriae, Fim2 and Fim3, as virulence factors. The expression of fim2 and fim3 is regulated by the BvgAS two-component system and the length of poly(C) stretches in Pfim promoters. In the Bvg phase, B. pertussis virulence-activated genes (vags) are up-regulated and virulence-repressed genes (vrgs) are down-regulated. Previous studies have shown that fim2 is a vag, but there is no consensus on fim3 regulation. We examined the regulation of fimbrial expression in B. pertussis clinical isolates. Our findings indicate that fim2 is a vag, while fim3 is a vag when Pfim3 poly(C)>13C, and a vrg when poly(C)≤13C. Although increased fim3 expression was observed in the Bvg phase in isolates with Pfim3 poly(C)≤13C, Fim3 production was not detected, suggesting post-transcriptional regulation of fim3 expression. These findings provide an insight into the regulation of fimbrial expression in B. pertussis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000514
2017-08-15
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/9/1364.html?itemId=/content/journal/micro/10.1099/mic.0.000514&mimeType=html&fmt=ahah

References

  1. Locht C, Antoine R, Jacob-Dubuisson F. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 2001;4:82–89 [CrossRef][PubMed]
    [Google Scholar]
  2. Mattoo S, Cherry JD. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 2005;18:326–382 [CrossRef][PubMed]
    [Google Scholar]
  3. Willems RJ, van der Heide HG, Mooi FR. Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous haemagglutinin gene. Mol Microbiol 1992;6:2661–2671 [CrossRef][PubMed]
    [Google Scholar]
  4. Willems R, Paul A, van der Heide HG, Ter Avest AR, Mooi FR. Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. Embo J 1990;9:2803–2809[PubMed]
    [Google Scholar]
  5. Chen Q, Boulanger A, Hinton DM, Stibitz S. Strong inhibition of fimbrial 3 subunit gene transcription by a novel downstream repressive element in Bordetella pertussis. Mol Microbiol 2014;93:748–758 [CrossRef][PubMed]
    [Google Scholar]
  6. Locht C, Geoffroy MC, Renauld G. Common accessory genes for the Bordetella pertussis filamentous hemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. Embo J 1992;11:3175–3183[PubMed]
    [Google Scholar]
  7. Cummings CA, Bootsma HJ, Relman DA, Miller JF. Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J Bacteriol 2006;188:1775–1785 [CrossRef][PubMed]
    [Google Scholar]
  8. Gorringe AR, Vaughan TE. Bordetella pertussis fimbriae (Fim): relevance for vaccines. Expert Rev Vaccines 2014;13:1205–1214 [CrossRef][PubMed]
    [Google Scholar]
  9. Hot D, Antoine R, Renauld-Mongénie G, Caro V, Hennuy B et al. Differential modulation of Bordetella pertussis virulence genes as evidenced by DNA microarray analysis. Mol Genet Genomics 2003;269:475–486 [CrossRef][PubMed]
    [Google Scholar]
  10. Chen Q, Decker KB, Boucher PE, Hinton D, Stibitz S. Novel architectural features of Bordetella pertussis fimbrial subunit promoters and their activation by the global virulence regulator BvgA. Mol Microbiol 2010;77:1326–1340 [CrossRef][PubMed]
    [Google Scholar]
  11. Vaughan TE, Pratt CB, Sealey K, Preston A, Fry NK et al. Plasticity of fimbrial genotype and serotype within populations of Bordetella pertussis: analysis by paired flow cytometry and genome sequencing. Microbiology 2014;160:2030–2044 [CrossRef][PubMed]
    [Google Scholar]
  12. Yuan JS, Reed A, Chen F, Stewart CN. Statistical analysis of real-time PCR data. BMC Bioinformatics 2006;7:85 [CrossRef][PubMed]
    [Google Scholar]
  13. Beattie DT, Knapp S, Mekalanos JJ. Evidence that modulation requires sequences downstream of the promoters of two vir-repressed genes of Bordetella pertussis. J Bacteriol 1990;172:6997–7004 [CrossRef][PubMed]
    [Google Scholar]
  14. Beattie DT, Mahan MJ, Mekalanos JJ. Repressor binding to a regulatory site in the DNA coding sequence is sufficient to confer transcriptional regulation of the vir-repressed genes (vrg genes) in Bordetella pertussis. J Bacteriol 1993;175:519–527 [CrossRef][PubMed]
    [Google Scholar]
  15. Cróinín TO, Grippe VK, Merkel TJ. Activation of the vrg6 promoter of Bordetella pertussis by RisA. J Bacteriol 2005;187:1648–1658 [CrossRef][PubMed]
    [Google Scholar]
  16. Merkel TJ, Stibitz S. Identification of a locus required for the regulation of bvg-repressed genes in Bordetella pertussis. J Bacteriol 1995;177:2727–2736 [CrossRef][PubMed]
    [Google Scholar]
  17. Guiso N, von Konig CH, Becker C, Hallander H. Fimbrial typing of Bordetello pertussis isolates: agglutination with polyclonal and monoclonal antisera. J Clin Microbiol 2001;39:1684–1685 [CrossRef][PubMed]
    [Google Scholar]
  18. Mooi FR, Hallander H, Wirsing von König CH, Hoet B, Guiso N. Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur J Clin Microbiol Infect Dis 2000;19:174–181 [CrossRef][PubMed]
    [Google Scholar]
  19. Li ZM, Brennan MJ, David JL, Carter PH, Cowell JL et al. Comparison of type 2 and type 6 fimbriae of Bordetella pertussis by using agglutinating monoclonal antibodies. Infect Immun 1988;56:3184–3188[PubMed]
    [Google Scholar]
  20. de Gouw D, Hermans PW, Bootsma HJ, Zomer A, Heuvelman K et al. Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One 2014;9:e84523 [CrossRef][PubMed]
    [Google Scholar]
  21. Coutte L, Huot L, Antoine R, Slupek S, Merkel TJ et al. The multifaceted RisA regulon of Bordetella pertussis. Sci Rep 2016;6:32774 [CrossRef][PubMed]
    [Google Scholar]
  22. Xing D, Corbel MJ, Newland P. Evaluation of Purified Monoclonal Antibodies to Bordetella Pertussis Fimbriae Type 2 and 3: Study Report and Proposal to Establish WHO Reference Reagents Who/bs/04/1998 Geneva: World Health Organization; 2004
    [Google Scholar]
  23. Tizolova A, Guiso N, Guillot S. Insertion sequences shared by Bordetella species and implications for the biological diagnosis of pertussis syndrome. Eur J Clin Microbiol Infect Dis 2013;32:89–96 [CrossRef][PubMed]
    [Google Scholar]
  24. Bouchez V, Caro V, Levillain E, Guigon G, Guiso N. Genomic content of Bordetella pertussis clinical isolates circulating in areas of intensive children vaccination. PLoS One 2008;3:e2437 [CrossRef][PubMed]
    [Google Scholar]
  25. Bouchez V, Hegerle N, Strati F, Njamkepo E, Guiso N. New Data on Vaccine antigen deficient Bordetella pertussis Isolates. Vaccines 2015;3:751–770 [CrossRef][PubMed]
    [Google Scholar]
  26. Hegerle N, Guiso N. Antibody-mediated inhibition of Bordetella pertussis adenylate cyclase-haemolysin-induced macrophage cytotoxicity is influenced by variations in the bacterial population. Microbiology 2014;160:962–969 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000514
Loading
/content/journal/micro/10.1099/mic.0.000514
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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