Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Research Article
  • Published:

Homologous and heterologous protection after single intranasal administration of live attenuated recombinant Bordetella pertussis

Nature Biotechnology volume 16, pages 454–457 (1998)Cite this article

Abstract

While single-dose mucosal immunization is best achieved by the use of attenuated live microorganisms, attenuation generally results in decreased immunogenicity. We attenuated Bordetella pertussis by the deletion of the pertussis toxin gene. A single intranasal administration of this strain protected against subsequent challenge as well as did the parent strain and better than immunization with commercial vaccine. Unexpectedly, this attenuation resulted in increased immunogenicity against the protective antigen filamentous hemagglutinin (FHA). In addition, immunogenicity was also enhanced against the Schistosoma mansoni Sm28GST genetically fused to FHA, resulting in protection against the parasite, as characterized by a reduction in worm burden and egg charge, after a single intranasal administration. Thus, attenuated recombinant B. pertussis strains are promising vectors for the simultaneous protection against pertussis and heterologous diseases by a single intranasal administration.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Hormaeche, C. and Khan, C.M.A. 1996. Recombinant bacteria as vaccine carriers of heterologous antigens, pp. 327–359 in Concepts in vaccine development. Kaufmann, S.H.E. (ed.). Walter de Gruyter, Berlin.

    Google Scholar 

  2. Wu, H.-Y. and Russell, M.W. 1997. Nasal lymphoid tissue, intranasal immunization, and compartmentalization of the common mucosal immune system. Immunol. Res. 16: 187–201.

    Article  CAS  Google Scholar 

  3. Hirabayashi, Y., Kurata, H., Funato, H., Nagamine, T., Aizawa, C., and Kurata, T. 1990. Comparison of intranasal inoculation of influenza HA vaccine combined with cholera toxin B subunit with oral or parenteral vaccination. Vaccine 8: 243–248.

    Article  CAS  Google Scholar 

  4. Robinson, K., Chamberlain, L.M., Schofield, K.M., Wells, J.M., and Le Page, R.W.F. 1997. Oral vaccination of mice against tetanus with recombinant Lactococcus lactis. Nature Biotechnology 15: 653–657

    Article  CAS  Google Scholar 

  5. Bass, J.W. and Stephenson, S.R. 1987. The return of pertussis. Pediatr. Infect. Dis.J. 6: 141–144.

    Article  CAS  Google Scholar 

  6. Jenkinson, D. 1988. Duration of effectiveness of pertussis vaccine: evidence from a 10 year community study. Br. Med. J. 296: 612–614.

    Article  CAS  Google Scholar 

  7. Lambert, H.J. 1965. Epidemiology of a small pertussis outbreak in Kent County, Michigan. Public Health Rep. 80: 365.

    Article  CAS  Google Scholar 

  8. Renauld-Mongénie, G., Mielcarek, N., Cornette, J., Schacht, A.-M., Capron, A., Riveau, G. and Locht, C. 1996. Induction of mucosal immune responses against a heterologous antigen fused to filamentous hemagglutinin after intranasal immunization with recombinant Bordetella pertussis. Proc. Natl Acad. Sci. USA 93: 7944–7949.

    Article  Google Scholar 

  9. Mielcarek, N., Cornette, J., Schacht, A.-M., Pierce, R., Locht, C., Capron, A., and Riveau, G. 1997. Intranasal priming with recombinant Bordetella pertussis for the induction of a systemic immune response against a heterologous antigen. Infect. Immun. 65: 544–550.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Locht, C., Berlin, P., Menozzi, F.D. and Renauld, G. 1993. The filamentous hemagglutinin, a multifaceted adhesln produced by virulent Bordetella spp. Mol. Microbiol. 9: 653–660.

    Article  CAS  Google Scholar 

  11. Black, W.J., Munoz, J.J., Peacock, M.G., Schad, P.A., Cowell, J.L., Burchall, J.J. et al. 1988. ADP-ribosyltransferase activity of pertussis toxin and immunomodu-lation by Bordetella pertussis. Science 240: 656–659.

    Article  CAS  Google Scholar 

  12. Khelef, N., Bachelet, C.-M., Vargaftig, B.B., and Guiso, N. 1994. Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect. Immun. 62: 2893–2900.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Antoine, R. and Locht, C. 1990. Roles of the disulfide bond and the carboxy-ter-minal region of the S1 subunit in the assembly and biosynthesis of pertussis toxin. Infect. Immun. 58: 1518–1526.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ad hoc group for the study of pertussis vaccines.1988. Placebo-controlled trial of two acellular pertussis vaccines in Sweden—protective efficacy and adverse events. Lancet 331:955–960 (Published erratum appears in Lancet. 1988. 331: 1238).

  15. Greco, D., Salmaso, S., Mastrantonio, P., Giuliano, M., Tozzi, A.E., Anemona, A. et al. 1996. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. N. Engl. J. Med. 334: 341–348.

    Article  CAS  Google Scholar 

  16. Gustafsson, L., Hallander, H.O., Olin, P., Reizenstein, E. and 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.

    Article  CAS  Google Scholar 

  17. Sato, Y., Kimura, M., and Fukumi, H. 1984.Development of a pertussis component in Japan. Lancet 324: 122–126.

    Article  Google Scholar 

  18. Weiss, A.A., Hewlett, E.L., Myers, G.A. and Falkow, S. 1983. Tn5-induced mutations affecting virulence factors of Bordetella pertussis. Infect. Immun. 42: 33–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Locht, C. and Keith, J.M. 1986. Pertussis toxin gene: nucleotide sequence and genetic organization. Science 232: 1258–1264.

    Article  CAS  Google Scholar 

  20. Warren, K.S. 1982. The secret of the immunopathogenesis of schistosomiasis: in vivo models. Immunol. Rev. 61: 189–213.

    Article  CAS  Google Scholar 

  21. Capron, A., Dessaint, J.P., Capron, M., Ouma, J.H., and Butterworth, A.E. 1987. Immunity to schistosomes: Progress toward vaccine. Science 238: 1065–1072.

    Article  CAS  Google Scholar 

  22. Shahin, R.D., Amsbaugh, D.F., and Leef, M.F. 1992. Mucosal immunization with filamentous hemagglutinin protects against Bordetella pertussis respiratory infection. Infect. Immun. 60: 1482–1488.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Greenberg, L. and Fleming, D.S. 1947. Increased efficiency of diphtheria toxoid when combined with pertussis vaccine. Can. J. Public Health 38: 279–282.

    CAS  PubMed  Google Scholar 

  24. Lehrer, S.B., Vaughan, J.H., and Tan, E.M. 1975. Immunological and biochemical properties of the histamine-sensitizing factor of Bordetella pertussis. J. Immunol. 114: 34–39.

    CAS  PubMed  Google Scholar 

  25. Vogel, F.R., Klein, T.W., Stewart II, W.E., Igarashi, T. and Friedman, H. 1985. Immune suppression and induction of gamma interferon by pertussis toxin. Infect. Immun. 49: 90–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Lobet, Y., Feron, C., Dequesne, G., Simoen, E., Hauser, P., and Locht, C. 1993. Site-specific alterations in the B oligomer that affect receptor-binding activities and mitogenicity of pertussis toxin. J. Exp. Med. 177: 79–87.

    Article  CAS  Google Scholar 

  27. Menozzi, F.D., Mutombo, R., Renauld, G., Gantiez, C., Hannah, J.H., Leininger, E. et al. 1994. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect. Immun. 62: 769–778.

  28. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NY.

    Google Scholar 

  29. Menozzi, F.D., Gantiez, C., and Locht, C. 1991. Interaction of the Bordetella pertussis filamentous haemagglutinin with heparin. FEMS Microbiol. Lett. 78: 59–64.

    Article  CAS  Google Scholar 

  30. Hoiset, S.K. and Stocker, B.A.D. 1981. Aromatic-dependentSalmonella typhimurium are non virulent and effective as live vaccines. Nature 291: 238–239.

    Article  Google Scholar 

Download references

Author information

Author notes

  1. Camille Locht: Corresponding author e-mail: camille.locht@pasteur-lille.fr

Authors and Affiliations

  1. INSERM U167, Pasteur Institute of Lille, 1 rue du Prof. Calmette, F-59019, Lille Cedex, France

    Nathalie Mielcarek, Gilles Riveau, Franck Remoué, Rudy Antoine & André Capron

  2. INSERM U447, Pasteur Institute of Lille, 1 rue du Prof. Calmette, F-59019, Lille Cedex, France

    Camille Locht

Authors
  1. Nathalie Mielcarek
    View author publications

    Search author on:PubMed Google Scholar

  2. Gilles Riveau
    View author publications

    Search author on:PubMed Google Scholar

  3. Franck Remoué
    View author publications

    Search author on:PubMed Google Scholar

  4. Rudy Antoine
    View author publications

    Search author on:PubMed Google Scholar

  5. André Capron
    View author publications

    Search author on:PubMed Google Scholar

  6. Camille Locht
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mielcarek, N., Riveau, G., Remoué, F. et al. Homologous and heterologous protection after single intranasal administration of live attenuated recombinant Bordetella pertussis. Nat Biotechnol 16, 454–457 (1998). https://doi.org/10.1038/nbt0598-454

Download citation

  • Received:

  • Accepted:

  • Issue date:

  • DOI: https://doi.org/10.1038/nbt0598-454

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing