Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1993 Feb;61(2):486–490. doi: 10.1128/iai.61.2.486-490.1993

Bordetella pertussis and Bordetella parapertussis: two immunologically distinct species.

N Khelef 1, B Danve 1, M J Quentin-Millet 1, N Guiso 1
PMCID: PMC302754  PMID: 8423077

Abstract

Bordetella pertussis and Bordetella parapertussis are closely related species. Both are responsible for outbreaks of whooping cough in humans and produce similar virulence factors, with the exception of pertussis toxin, specific to B. pertussis. Current pertussis whole-cell vaccine will soon be replaced by acellular vaccines containing major adhesins (filamentous hemagglutinin and pertactin) and major toxin (pertussis toxin). All of these factors are antigens that stimulate a protective immune response in the murine respiratory model and in clinical assays. In the present study, we examined the protective efficacies of these factors, and that of adenylate cyclase-hemolysin, another B. pertussis toxin, against B. parapertussis infection in a murine respiratory model. As expected, pertussis toxin did not protect against B. parapertussis infection, since this bacterium did not express this protein, but the surprising result was that none of the other factors were protective against B. parapertussis infection. Furthermore, B. parapertussis adenylate cyclase-hemolysin, although it protected against B. parapertussis infection, did not protect against B. pertussis infection. Despite a high degree of homology between both B. pertussis and B. parapertussis species, no cross-protection was observed. Our results outline the fact that, as in other gram-negative bacteria, Bordetella surface proteins vary immunologically.

Full text

PDF
486

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aricò B., Gross R., Smida J., Rappuoli R. Evolutionary relationships in the genus Bordetella. Mol Microbiol. 1987 Nov;1(3):301–308. doi: 10.1111/j.1365-2958.1987.tb01936.x. [DOI] [PubMed] [Google Scholar]
  2. Aricò B., Rappuoli R. Bordetella parapertussis and Bordetella bronchiseptica contain transcriptionally silent pertussis toxin genes. J Bacteriol. 1987 Jun;169(6):2847–2853. doi: 10.1128/jb.169.6.2847-2853.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barry E. M., Weiss A. A., Ehrmann I. E., Gray M. C., Hewlett E. L., Goodwin M. S. Bordetella pertussis adenylate cyclase toxin and hemolytic activities require a second gene, cyaC, for activation. J Bacteriol. 1991 Jan;173(2):720–726. doi: 10.1128/jb.173.2.720-726.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bellalou J., Ladant D., Sakamoto H. Synthesis and secretion of Bordetella pertussis adenylate cyclase as a 200-kilodalton protein. Infect Immun. 1990 May;58(5):1195–1200. doi: 10.1128/iai.58.5.1195-1200.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Borská K., Simkovicová M. Studies on the circulation of bordetella pertussis and bordetella parapertussis in populations of children. J Hyg Epidemiol Microbiol Immunol. 1972;16(2):159–172. [PubMed] [Google Scholar]
  6. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  7. Brennan M. J., Li Z. M., Cowell J. L., Bisher M. E., Steven A. C., Novotny P., Manclark C. R. Identification of a 69-kilodalton nonfimbrial protein as an agglutinogen of Bordetella pertussis. Infect Immun. 1988 Dec;56(12):3189–3195. doi: 10.1128/iai.56.12.3189-3195.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charles I. G., Dougan G., Pickard D., Chatfield S., Smith M., Novotny P., Morrissey P., Fairweather N. F. Molecular cloning and characterization of protective outer membrane protein P.69 from Bordetella pertussis. Proc Natl Acad Sci U S A. 1989 May;86(10):3554–3558. doi: 10.1073/pnas.86.10.3554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DONCHEV D., STOYANOVA M. The epidemiological significance of the differentiation of pertussis and parapertussis. J Hyg Epidemiol Microbiol Immunol. 1961;5:294–297. [PubMed] [Google Scholar]
  10. Endoh M., Nagai M., Ueda T., Yoshida Y., Nakase Y. Cytopathic effect of heat-labile toxin of Bordetella parapertussis on aortic smooth muscle cells from pigs or guinea pigs. Microbiol Immunol. 1988;32(4):423–428. doi: 10.1111/j.1348-0421.1988.tb01401.x. [DOI] [PubMed] [Google Scholar]
  11. Endoh M., Takezawa T., Nakase Y. Adenylate cyclase activity of Bordetella organisms. I. Its production in liquid medium. Microbiol Immunol. 1980;24(2):95–104. doi: 10.1111/j.1348-0421.1980.tb00567.x. [DOI] [PubMed] [Google Scholar]
  12. Guiso N., Szatanik M., Rocancourt M. Protective activity of Bordetella adenylate cyclase-hemolysin against bacterial colonization. Microb Pathog. 1991 Dec;11(6):423–431. doi: 10.1016/0882-4010(91)90038-c. [DOI] [PubMed] [Google Scholar]
  13. Ladant D., Brezin C., Alonso J. M., Crenon I., Guiso N. Bordetella pertussis adenylate cyclase. Purification, characterization, and radioimmunoassay. J Biol Chem. 1986 Dec 5;261(34):16264–16269. [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Li L. J., Dougan G., Novotny P., Charles I. G. P.70 pertactin, an outer-membrane protein from Bordetella parapertussis: cloning, nucleotide sequence and surface expression in Escherichia coli. Mol Microbiol. 1991 Feb;5(2):409–417. doi: 10.1111/j.1365-2958.1991.tb02123.x. [DOI] [PubMed] [Google Scholar]
  16. Linnemann C. C., Perry E. B. Bordetella parapertussis. Recent experience and a review of the literature. Am J Dis Child. 1977 May;131(5):560–563. doi: 10.1001/archpedi.1977.02120180074014. [DOI] [PubMed] [Google Scholar]
  17. Marchitto K. S., Smith S. G., Locht C., Keith J. M. Nucleotide sequence homology to pertussis toxin gene in Bordetella bronchiseptica and Bordetella parapertussis. Infect Immun. 1987 Mar;55(3):497–501. doi: 10.1128/iai.55.3.497-501.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Monack D., Munoz J. J., Peacock M. G., Black W. J., Falkow S. Expression of pertussis toxin correlates with pathogenesis in Bordetella species. J Infect Dis. 1989 Feb;159(2):205–210. doi: 10.1093/infdis/159.2.205. [DOI] [PubMed] [Google Scholar]
  19. Musser J. M., Hewlett E. L., Peppler M. S., Selander R. K. Genetic diversity and relationships in populations of Bordetella spp. J Bacteriol. 1986 Apr;166(1):230–237. doi: 10.1128/jb.166.1.230-237.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Novotny P. Pathogenesis in Bordetella species. J Infect Dis. 1990 Mar;161(3):581–583. doi: 10.1093/infdis/161.3.581. [DOI] [PubMed] [Google Scholar]
  21. Sato Y., Cowell J. L., Sato H., Burstyn D. G., Manclark C. R. Separation and purification of the hemagglutinins from Bordetella pertussis. Infect Immun. 1983 Jul;41(1):313–320. doi: 10.1128/iai.41.1.313-320.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sekura R. D., Fish F., Manclark C. R., Meade B., Zhang Y. L. Pertussis toxin. Affinity purification of a new ADP-ribosyltransferase. J Biol Chem. 1983 Dec 10;258(23):14647–14651. [PubMed] [Google Scholar]
  23. Shahin R. D., Brennan M. J., Li Z. M., Meade B. D., Manclark C. R. Characterization of the protective capacity and immunogenicity of the 69-kD outer membrane protein of Bordetella pertussis. J Exp Med. 1990 Jan 1;171(1):63–73. doi: 10.1084/jem.171.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stainer D. W., Scholte M. J. A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol. 1970 Oct;63(2):211–220. doi: 10.1099/00221287-63-2-211. [DOI] [PubMed] [Google Scholar]
  25. Storsaeter J., Hallander H., Farrington C. P., Olin P., Möllby R., Miller E. Secondary analyses of the efficacy of two acellular pertussis vaccines evaluated in a Swedish phase III trial. Vaccine. 1990 Oct;8(5):457–461. doi: 10.1016/0264-410x(90)90246-i. [DOI] [PubMed] [Google Scholar]
  26. VYSOKA BURIANOVA B. CONTEMPORARY PROBLEMS IN THE EPIDEMIOLOGY OF WHOOPING COUGH. J Hyg Epidemiol Microbiol Immunol. 1963;7:472–481. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES