1887

Abstract

The fimbriae of are required for colonization of the human respiratory tract. Two serologically distinct fimbrial subunits, Fim2 and Fim3, considered important vaccine components for many years, are included in the Sanofi Pasteur 5-component acellular pertussis vaccine, and the World Health Organization recommends the inclusion of strains expressing both fimbrial serotypes in whole-cell pertussis vaccines. Each of the fimbrial major subunit genes, , , and , has a promoter poly(C) tract upstream of its −10 box. Such monotonic DNA elements are susceptible to changes in length via slipped-strand mispairing and , which potentially causes on/off switching of genes at every cell division. Here, we have described intra-culture variability in poly(C) tract lengths and the resulting fimbrial phenotypes in 22 recent UK isolates. Owing to the highly plastic nature of fimbrial promoters, we used the same cultures for both genome sequencing and flow cytometry. Individual cultures of contained multiple fimbrial serotypes and multiple different fimbrial promoter poly(C) tract lengths, which supports earlier serological evidence that expresses both serotypes during infection.

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2014-09-01
2019-11-22
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References

  1. Aho A. V., Kernighan B. W., Weinberger P. J.. ( 1988;). The AWK Programming Language. Reading, MA:: Addison-Wesley;.
    [Google Scholar]
  2. Alexander F., Matheson M., Fry N. K., Labram B., Gorringe A. R.. ( 2012;). Antibody responses to individual Bordetella pertussis fimbrial antigen Fim2 or Fim3 following immunization with the five-component acellular pertussis vaccine or to pertussis disease. . Clin Vaccine Immunol 19:, 1776–1783. [CrossRef][PubMed]
    [Google Scholar]
  3. Beese L. S., Derbyshire V., Steitz T. A.. ( 1993;). Structure of DNA polymerase I Klenow fragment bound to duplex DNA. . Science 260:, 352–355. [CrossRef][PubMed]
    [Google Scholar]
  4. 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. [CrossRef][PubMed]
    [Google Scholar]
  5. Cherry J. D., Gornbein J., Heininger U., Stehr K.. ( 1998;). A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. . Vaccine 16:, 1901–1906. [CrossRef][PubMed]
    [Google Scholar]
  6. Coenye T., Vandamme P.. ( 2005;). Characterization of mononucleotide repeats in sequenced prokaryotic genomes. . DNA Res 12:, 221–233. [CrossRef][PubMed]
    [Google Scholar]
  7. 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. [CrossRef][PubMed]
    [Google Scholar]
  8. Decker K. B., James T. D., Stibitz S., Hinton D. M.. ( 2012;). The Bordetella pertussis model of exquisite gene control by the global transcription factor BvgA. . Microbiology 158:, 1665–1676. [CrossRef][PubMed]
    [Google Scholar]
  9. Eom S. H., Wang J., Steitz T. A.. ( 1996;). Structure of Taq polymerase with DNA at the polymerase active site. . Nature 382:, 278–281. [CrossRef][PubMed]
    [Google Scholar]
  10. Fazekas A., Steeves R., Newmaster S.. ( 2010;). Improving sequencing quality from PCR products containing long mononucleotide repeats. . Biotechniques 48:, 277–285. [CrossRef][PubMed]
    [Google Scholar]
  11. Fresco J. R., Alberts B. M.. ( 1960;). The accommodation of noncomplementary bases in helical polyribouncleotides and deoxyribonucleic acids. . Proc Natl Acad Sci USA 46:, 311–321. [CrossRef][PubMed]
    [Google Scholar]
  12. Fry N. K., Neal S., Harrison T. G., Miller E., Matthews R., George R. C.. ( 2001;). Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. . Infect Immun 69:, 5520–5528. [CrossRef][PubMed]
    [Google Scholar]
  13. Gustafsson L., Hallander H. O., Olin P., Reizenstein E., Storsaeter J.. ( 1996;). A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. . N Engl J Med 334:, 349–355. [CrossRef][PubMed]
    [Google Scholar]
  14. Hallander H. O., Advani A., Donnelly D., Gustafsson L., Carlsson R.-M.. ( 2005;). Shifts of Bordetella pertussis variants in Sweden from 1970 to 2003, during three periods marked by different vaccination programs. . J Clin Microbiol 43:, 2856–2865. [CrossRef][PubMed]
    [Google Scholar]
  15. Hallander H., Advani A., Alexander F., Gustafsson L., Ljungman M., Pratt C., Hall I., Gorringe A. R.. ( 2014;). Antibody responses to Bordetella pertussis Fim2 or Fim3 following immunization with a whole-cell, two-component, or five-component acellular pertussis vaccine and following pertussis disease in children in Sweden in 1997 and 2007. . Clin Vaccine Immunol 21:, 165–173. [CrossRef][PubMed]
    [Google Scholar]
  16. Heck D. V., Trus B. L., Steven A. C.. ( 1996;). Three-dimensional structure of Bordetella pertussis fimbriae. . J Struct Biol 116:, 264–269. [CrossRef][PubMed]
    [Google Scholar]
  17. 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. [CrossRef][PubMed]
    [Google Scholar]
  18. Heininger U., Stehr K., Cherry J. D.. ( 1998;). The efficacy of a whole cell pertussis vaccine and fimbriae against Bordetella pertussis and Bordetella parapertussis infections in respiratory mouse model. . Vaccine 16:, 1255. [CrossRef][PubMed]
    [Google Scholar]
  19. Knuth D. E.. ( 1997;). The Art of Computer Programming, Volume 2 (3rd ed.) Seminumerical Algorithms, p. 232. Boston, MA:: Addison-Wesley Longman;.
    [Google Scholar]
  20. Litt D. J., Neal S. E., Fry N. K.. ( 2009;). Changes in genetic diversity of the Bordetella pertussis population in the United Kingdom between 1920 and 2006 reflect vaccination coverage and emergence of a single dominant clonal type. . J Clin Microbiol 47:, 680–688. [CrossRef][PubMed]
    [Google Scholar]
  21. Ma L., Jensen J. S., Mancuso M., Hamasuna R., Jia Q., McGowin C. L., Martin D. H.. ( 2012;). Variability of trinucleotide tandem repeats in the MgPa operon and its repetitive chromosomal elements in Mycoplasma genitalium.. J Med Microbiol 61:, 191–197. [CrossRef][PubMed]
    [Google Scholar]
  22. Martin P., van de Ven T., Mouchel N., Jeffries A. C., Hood D. W., Moxon E. R.. ( 2003;). Experimentally revised repertoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. . Mol Microbiol 50:, 245–257. [CrossRef][PubMed]
    [Google Scholar]
  23. Mattoo S., Cherry J. D.. ( 2005;). Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. . Clin Microbiol Rev 18:, 326–382. [CrossRef][PubMed]
    [Google Scholar]
  24. Mooi F. R., Van Der Maas N. A., De Melker H. E.. ( 2014;). Pertussis resurgence: waning immunity and pathogen adaptation – two sides of the same coin. . Epidemiol Infect 142:, 685–694. [CrossRef][PubMed]
    [Google Scholar]
  25. Murphy G. L., Connell T. D., Barritt D. S., Koomey M., Cannon J. G.. ( 1989;). Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. . Cell 56:, 539–547. [CrossRef][PubMed]
    [Google Scholar]
  26. Myers R. H., MacDonald M. E., Koroshetz W. J., Duyao M. P., Ambrose C. M., Taylor S. A., Barnes G., Srinidhi J., Lin C. S.. & other authors ( 1993;). De novo expansion of a (CAG)n repeat in sporadic Huntington’s disease. . Nat Genet 5:, 168–173. [CrossRef][PubMed]
    [Google Scholar]
  27. Olin P.. ( 1997;). Efficacy trial of acellular pertussis vaccines; trial I. . Dev Biol Stand 89:, 52–54.[PubMed]
    [Google Scholar]
  28. Packard E. R., Parton R., Coote J. G., Fry N. K.. ( 2004;). Sequence variation and conservation in virulence-related genes of Bordetella pertussis isolates from the UK. . J Med Microbiol 53:, 355–365. [CrossRef][PubMed]
    [Google Scholar]
  29. Parkhill J., Sebaihia M., Preston A., Murphy L. D., Thomson N., Harris D. E., Holden M. T., Churcher C. M., Bentley S. D.. & other authors ( 2003;). Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. . Nat Genet 35:, 32–40. [CrossRef][PubMed]
    [Google Scholar]
  30. Poolman J. T., Hallander H. O.. ( 2007;). Acellular pertussis vaccines and the role of pertactin and fimbriae. . Expert Rev Vaccines 6:, 47–56. [CrossRef][PubMed]
    [Google Scholar]
  31. Rice P., Longden I., Bleasby A.. ( 2000;). EMBOSS: the European Molecular Biology Open Software Suite. . Trends Genet 16:, 276–277. [CrossRef][PubMed]
    [Google Scholar]
  32. Robinson A., Gorringe A. R., Funnell S. G., Fernandez M.. ( 1989a;). Serospecific protection of mice against intranasal infection with Bordetella pertussis. . Vaccine 7:, 321–324. [CrossRef][PubMed]
    [Google Scholar]
  33. Robinson A., Ashworth L. A., Irons L. I.. ( 1989b;). Serotyping Bordetella pertussis strains. . Vaccine 7:, 491–494. [CrossRef][PubMed]
    [Google Scholar]
  34. Sarkari J., Pandit N., Moxon E. R., Achtman M.. ( 1994;). Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. . Mol Microbiol 13:, 207–217. [CrossRef][PubMed]
    [Google Scholar]
  35. 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. [CrossRef][PubMed]
    [Google Scholar]
  36. Storsaeter J., Hallander H. O., Gustafsson L., Olin P.. ( 1998;). Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. . Vaccine 16:, 1907–1916. [CrossRef][PubMed]
    [Google Scholar]
  37. Tartof S. Y., Lewis M., Kenyon C., White K., Osborn A., Liko J., Zell E., Martin S., Messonnier N. E.. & other authors ( 2013;). Waning immunity to pertussis following 5 doses of DTaP. . Pediatrics 131:, e1047–e1052. [CrossRef][PubMed]
    [Google Scholar]
  38. Tauseef I., Ali Y. M., Bayliss C. D.. ( 2013;). Phase variation of PorA, a major outer membrane protein, mediates escape of bactericidal antibodies by Neisseria meningitides. . Infect Immun 81:, 1374–1380. [CrossRef][PubMed]
    [Google Scholar]
  39. Tefon B. E., Maass S., Özcengiz E., Becher D., Hecker M., Özcengiz G.. ( 2011;). A comprehensive analysis of Bordetella pertussis surface proteome and identification of new immunogenic proteins. . Vaccine 29:, 3583–3595. [CrossRef][PubMed]
    [Google Scholar]
  40. Thompson K., Ritchie D. M.. ( 1971;). UNIX Programmers Manual. New York:: Bell Laboratories;.
    [Google Scholar]
  41. Tsang R. S., Lau A. K., 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. [CrossRef][PubMed]
    [Google Scholar]
  42. Van Buynder P. G., Owen D., Vurdien J. E., Andrews N. J., Matthews R. C., Miller E.. ( 1999;). Bordetella pertussis surveillance in England and Wales: 1995-7. . Epidemiol Infect 123:, 403–411. [CrossRef][PubMed]
    [Google Scholar]
  43. van der Ende A., Hopman C. T., Zaat S., Essink B. B., Berkhout B., Dankert J.. ( 1995;). Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the -10 and -35 regions of the promoter. . J Bacteriol 177:, 2475–2480.[PubMed]
    [Google Scholar]
  44. van der Woude M. W., Bäumler A. J.. ( 2004;). Phase and antigenic variation in bacteria. . Clin Microbiol Rev 17:, 581–611. [CrossRef][PubMed]
    [Google Scholar]
  45. Walker F. O.. ( 2007;). Huntington’s disease. . Lancet 369:, 218–228. [CrossRef][PubMed]
    [Google Scholar]
  46. Warfel J. M., Zimmerman L. I., Merkel T. J.. ( 2014;). Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. . Proc Natl Acad Sci U S A 111:, 787–792. [CrossRef][PubMed]
    [Google Scholar]
  47. Welford B. P.. ( 1962;). Note on a method for calculating corrected sums of squares and products. . Technometrics 4:, 419–420. [CrossRef]
    [Google Scholar]
  48. 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]
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