Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Oct;65(10):4222–4228. doi: 10.1128/iai.65.10.4222-4228.1997

Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract.

C A Geuijen 1, R J Willems 1, M Bongaerts 1, J Top 1, H Gielen 1, F R Mooi 1
PMCID: PMC175606  PMID: 9317030

Abstract

Bordetella pertussis fimbriae are composed of a major subunit, Fim2 or Fim3, and the minor subunit FimD. Using immunoelectron microscopy, we provide evidence that FimD is located at the fimbrial tip. The role of FimD in colonization of the mouse respiratory tract was studied by using two fimbrial mutants: a mutant completely devoid of fimbriae (designated FimD-) and a mutant devoid of the major fimbrial subunits but still producing the minor subunit (designated FimD+). The ability of the two fimbrial mutants to colonize the nasopharynx, trachea, and lungs was compared with those of the wild type parental strain and a filamentous hemagglutinin (FHA) mutant. Of the three mutants studied, the FimD- mutant showed the greatest defect, colonizing less well in the nasopharynx, trachea, and lungs. The most pronounced defect in colonizing ability of the three mutants was observed in the trachea. However, the colonizing defect of the FHA and FimD+ mutants in the trachea was observed only during the first 3 days of infection. After 10 days, the colonization level was nearly restored to wild-type levels. The FHA and FimD+ mutants showed a slight colonization defect in the nasopharynx but no defect in the lungs. A maltose binding protein-FimD fusion protein and a peptide derived from FimD were able to bind to heparin, a member of a class of sulfated sugars which are ubiquitous in the respiratory tract. Recently it was shown (W. L. W. Hazenbos, C. A. W. Geuijen, B. M. van den Berg, F. R. Mooi, and R. van Furth, J. Infect. Dis. 171:924-929, 1995) that FimD also binds to the integrin VLA-5, and our results suggest that the binding of B. pertussis to these two molecules plays an important role in colonization of the respiratory tract of the mouse.

Full Text

The Full Text of this article is available as a PDF (527.7 KB).

Selected References

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

  1. Abraham S. N., Goguen J. D., Sun D., Klemm P., Beachey E. H. Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products. J Bacteriol. 1987 Dec;169(12):5530–5536. doi: 10.1128/jb.169.12.5530-5536.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bakker D., Vader C. E., Roosendaal B., Mooi F. R., Oudega B., de Graaf F. K. Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enterotoxigenic Escherichia coli. Mol Microbiol. 1991 Apr;5(4):875–886. doi: 10.1111/j.1365-2958.1991.tb00761.x. [DOI] [PubMed] [Google Scholar]
  3. Brennan M. J., Hannah J. H., Leininger E. Adhesion of Bordetella pertussis to sulfatides and to the GalNAc beta 4Gal sequence found in glycosphingolipids. J Biol Chem. 1991 Oct 5;266(28):18827–18831. [PubMed] [Google Scholar]
  4. Cao J., Khan A. S., Bayer M. E., Schifferli D. M. Ordered translocation of 987P fimbrial subunits through the outer membrane of Escherichia coli. J Bacteriol. 1995 Jul;177(13):3704–3713. doi: 10.1128/jb.177.13.3704-3713.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cardin A. D., Weintraub H. J. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 1989 Jan-Feb;9(1):21–32. doi: 10.1161/01.atv.9.1.21. [DOI] [PubMed] [Google Scholar]
  6. Friedman R. L., Nordensson K., Wilson L., Akporiaye E. T., Yocum D. E. Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect Immun. 1992 Nov;60(11):4578–4585. doi: 10.1128/iai.60.11.4578-4585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Geuijen C. A., Willems R. J., Mooi F. R. The major fimbrial subunit of Bordetella pertussis binds to sulfated sugars. Infect Immun. 1996 Jul;64(7):2657–2665. doi: 10.1128/iai.64.7.2657-2665.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hazenbos W. L., Geuijen C. A., van den Berg B. M., Mooi F. R., van Furth R. Bordetella pertussis fimbriae bind to human monocytes via the minor fimbrial subunit FimD. J Infect Dis. 1995 Apr;171(4):924–929. doi: 10.1093/infdis/171.4.924. [DOI] [PubMed] [Google Scholar]
  9. Hazenbos W. L., van den Berg B. M., Geuijen C. W., Mooi F. R., van Furth R. Binding of FimD on Bordetella pertussis to very late antigen-5 on monocytes activates complement receptor type 3 via protein tyrosine kinases. J Immunol. 1995 Oct 15;155(8):3972–3978. [PubMed] [Google Scholar]
  10. Lindberg F., Lund B., Johansson L., Normark S. Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature. 1987 Jul 2;328(6125):84–87. doi: 10.1038/328084a0. [DOI] [PubMed] [Google Scholar]
  11. Locht C., Bertin P., Menozzi F. D., Renauld G. The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol. 1993 Aug;9(4):653–660. doi: 10.1111/j.1365-2958.1993.tb01725.x. [DOI] [PubMed] [Google Scholar]
  12. McDonald J. A. Extracellular matrix assembly. Annu Rev Cell Biol. 1988;4:183–207. doi: 10.1146/annurev.cb.04.110188.001151. [DOI] [PubMed] [Google Scholar]
  13. Menozzi F. D., Gantiez C., Locht C. Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol Lett. 1991 Feb;62(1):59–64. doi: 10.1111/j.1574-6968.1991.tb04417.x. [DOI] [PubMed] [Google Scholar]
  14. Menozzi F. D., Mutombo R., Renauld G., Gantiez C., Hannah J. H., Leininger E., Brennan M. J., Locht C. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect Immun. 1994 Mar;62(3):769–778. doi: 10.1128/iai.62.3.769-778.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moch T., Hoschützky H., Hacker J., Kröncke K. D., Jann K. Isolation and characterization of the alpha-sialyl-beta-2,3-galactosyl-specific adhesin from fimbriated Escherichia coli. Proc Natl Acad Sci U S A. 1987 May;84(10):3462–3466. doi: 10.1073/pnas.84.10.3462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mooi F. R., Jansen W. H., Brunings H., Gielen H., van der Heide H. G., Walvoort H. C., Guinee P. A. Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb Pathog. 1992 Feb;12(2):127–135. doi: 10.1016/0882-4010(92)90115-5. [DOI] [PubMed] [Google Scholar]
  17. Mooi F. R., Wijfjes A., de Graaf F. K. Identification and characterization of precursors in the biosynthesis of the K88ab fimbria of Escherichia coli. J Bacteriol. 1983 Apr;154(1):41–49. doi: 10.1128/jb.154.1.41-49.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mooi F. R., van der Heide H. G., ter Avest A. R., Welinder K. G., Livey I., van der Zeijst B. A., Gaastra W. Characterization of fimbrial subunits from Bordetella species. Microb Pathog. 1987 Jun;2(6):473–484. doi: 10.1016/0882-4010(87)90054-4. [DOI] [PubMed] [Google Scholar]
  19. Ortega-Barria E., Pereira M. E. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 1991 Oct 18;67(2):411–421. doi: 10.1016/0092-8674(91)90192-2. [DOI] [PubMed] [Google Scholar]
  20. Poolman J. T., Kuipers B., Vogel M. L., Hamstra H. J., Nagel J. Description of a hybridoma bank towards Bordetella pertussis toxin and surface antigens. Microb Pathog. 1990 Jun;8(6):377–382. doi: 10.1016/0882-4010(90)90024-k. [DOI] [PubMed] [Google Scholar]
  21. Relman D. A., Domenighini M., Tuomanen E., Rappuoli R., Falkow S. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2637–2641. doi: 10.1073/pnas.86.8.2637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Relman D., Tuomanen E., Falkow S., Golenbock D. T., Saukkonen K., Wright S. D. Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell. 1990 Jun 29;61(7):1375–1382. doi: 10.1016/0092-8674(90)90701-f. [DOI] [PubMed] [Google Scholar]
  23. Riegman N., Hoschützky H., van Die I., Hoekstra W., Jann K., Bergmans H. Immunocytochemical analysis of P-fimbrial structure: localization of minor subunits and the influence of the minor subunit FsoE on the biogenesis of the adhesin. Mol Microbiol. 1990 Jul;4(7):1193–1198. doi: 10.1111/j.1365-2958.1990.tb00694.x. [DOI] [PubMed] [Google Scholar]
  24. Robinson A., Ashworth L. A., Irons L. I. Serotyping Bordetella pertussis strains. Vaccine. 1989 Dec;7(6):491–494. doi: 10.1016/0264-410x(89)90270-3. [DOI] [PubMed] [Google Scholar]
  25. Rudel T., Scheurerpflug I., Meyer T. F. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature. 1995 Jan 26;373(6512):357–359. doi: 10.1038/373357a0. [DOI] [PubMed] [Google Scholar]
  26. Saukkonen K., Cabellos C., Burroughs M., Prasad S., Tuomanen E. Integrin-mediated localization of Bordetella pertussis within macrophages: role in pulmonary colonization. J Exp Med. 1991 May 1;173(5):1143–1149. doi: 10.1084/jem.173.5.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stibitz S., Black W., Falkow S. The construction of a cloning vector designed for gene replacement in Bordetella pertussis. Gene. 1986;50(1-3):133–140. doi: 10.1016/0378-1119(86)90318-5. [DOI] [PubMed] [Google Scholar]
  28. Stibitz S., Garletts T. L. Derivation of a physical map of the chromosome of Bordetella pertussis Tohama I. J Bacteriol. 1992 Dec;174(23):7770–7777. doi: 10.1128/jb.174.23.7770-7777.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stibitz S., Yang M. S. Subcellular localization and immunological detection of proteins encoded by the vir locus of Bordetella pertussis. J Bacteriol. 1991 Jul;173(14):4288–4296. doi: 10.1128/jb.173.14.4288-4296.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tuomanen E., Towbin H., Rosenfelder G., Braun D., Larson G., Hansson G. C., Hill R. Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J Exp Med. 1988 Jul 1;168(1):267–277. doi: 10.1084/jem.168.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Verwey W. F., Thiele E. H., Sage D. N., Schuchardt L. F. A SIMPLIFIED LIQUID CULTURE MEDIUM FOR THE GROWTH OF HEMOPHILUS PERTUSSIS. J Bacteriol. 1949 Aug;58(2):127–134. [PMC free article] [PubMed] [Google Scholar]
  32. Willems R. J., Geuijen C., van der Heide H. G., Matheson M., Robinson A., Versluis L. F., Ebberink R., Theelen J., Mooi F. R. Isolation of a putative fimbrial adhesin from Bordetella pertussis and the identification of its gene. Mol Microbiol. 1993 Aug;9(3):623–634. doi: 10.1111/j.1365-2958.1993.tb01722.x. [DOI] [PubMed] [Google Scholar]
  33. Willems R. J., Geuijen C., van der Heide H. G., Renauld G., Bertin P., van den Akker W. M., Locht C., Mooi F. R. Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol. 1994 Jan;11(2):337–347. doi: 10.1111/j.1365-2958.1994.tb00314.x. [DOI] [PubMed] [Google Scholar]
  34. Willems R. J., van der Heide H. G., Mooi F. R. Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous haemagglutinin gene. Mol Microbiol. 1992 Sep;6(18):2661–2671. doi: 10.1111/j.1365-2958.1992.tb01443.x. [DOI] [PubMed] [Google Scholar]
  35. Willems R., Paul A., van der Heide H. G., ter Avest A. R., Mooi F. R. Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J. 1990 Sep;9(9):2803–2809. doi: 10.1002/j.1460-2075.1990.tb07468.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. van der Ley P., Heckels J. E., Virji M., Hoogerhout P., Poolman J. T. Topology of outer membrane porins in pathogenic Neisseria spp. Infect Immun. 1991 Sep;59(9):2963–2971. doi: 10.1128/iai.59.9.2963-2971.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES