Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1992 Jun;60(6):2380–2385. doi: 10.1128/iai.60.6.2380-2385.1992

Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin.

E Leininger 1, C A Ewanowich 1, A Bhargava 1, M S Peppler 1, J G Kenimer 1, M J Brennan 1
PMCID: PMC257169  PMID: 1587605

Abstract

Pertactin and filamentous hemagglutinin (FHA), proteins present on the surface of the gram-negative organism Bordetella pertussis, have been shown to contain the putative cell-binding sequence arginine-glycine-aspartic acid (RGD) and to promote eukaryotic cell attachment. The attachment of epithelial cells to purified pertactin and the entry of B. pertussis into human HeLa cells are both inhibited by an RGD-containing peptide derived from the pertactin sequence. In contrast, an RGD-containing peptide derived from the FHA sequence has no effect on either the attachment of epithelial cells to purified FHA or the entry of B. pertussis into HeLa cells. Staphylococcus aureus organisms coated with pertactin or FHA, purified from B. pertussis, enter HeLa cells more efficiently than S. aureus cells coated with bovine serum albumin. The pertactin-enhanced entry of S. aureus is inhibited by 75% in the presence of the RGD peptide from pertactin, whereas the RGD peptide derived from FHA has no effect on the increased entry promoted by the pertactin-coated or by the FHA-coated S. aureus. These results indicate that the active uptake of B. pertussis by certain mammalian cells may be mediated by the interaction of the RGD site found in pertactin with eukaryotic cell surface receptors.

Full text

PDF
2380

Images in this article

Selected References

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

  1. Aricó B., Miller J. F., Roy C., Stibitz S., Monack D., Falkow S., Gross R., Rappuoli R. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671–6675. doi: 10.1073/pnas.86.17.6671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Charles I. G., Li J. L., Roberts M., Beesley K., Romanos M., Pickard D. J., Francis M., Campbell D., Dougan G., Brennan M. J. Identification and characterization of a protective immunodominant B cell epitope of pertactin (P.69) from Bordetella pertussis. Eur J Immunol. 1991 May;21(5):1147–1153. doi: 10.1002/eji.1830210509. [DOI] [PubMed] [Google Scholar]
  6. Delisse-Gathoye A. M., Locht C., Jacob F., Raaschou-Nielsen M., Heron I., Ruelle J. L., de Wilde M., Cabezon T. Cloning, partial sequence, expression, and antigenic analysis of the filamentous hemagglutinin gene of Bordetella pertussis. Infect Immun. 1990 Sep;58(9):2895–2905. doi: 10.1128/iai.58.9.2895-2905.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ewanowich C. A., Melton A. R., Weiss A. A., Sherburne R. K., Peppler M. S. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. doi: 10.1128/iai.57.9.2698-2704.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ewanowich C. A., Sherburne R. K., Man S. F., Peppler M. S. Bordetella parapertussis invasion of HeLa 229 cells and human respiratory epithelial cells in primary culture. Infect Immun. 1989 Apr;57(4):1240–1247. doi: 10.1128/iai.57.4.1240-1247.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Griffin F. M., Jr, Griffin J. A., Leider J. E., Silverstein S. C. Studies on the mechanism of phagocytosis. I. Requirements for circumferential attachment of particle-bound ligands to specific receptors on the macrophage plasma membrane. J Exp Med. 1975 Nov 1;142(5):1263–1282. doi: 10.1084/jem.142.5.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Isberg R. R. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science. 1991 May 17;252(5008):934–938. doi: 10.1126/science.1674624. [DOI] [PubMed] [Google Scholar]
  11. Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
  12. Lee C. K., Roberts A. L., Finn T. M., Knapp S., Mekalanos J. J. A new assay for invasion of HeLa 229 cells by Bordetella pertussis: effects of inhibitors, phenotypic modulation, and genetic alterations. Infect Immun. 1990 Aug;58(8):2516–2522. doi: 10.1128/iai.58.8.2516-2522.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leininger E., Roberts M., Kenimer J. G., Charles I. G., Fairweather N., Novotny P., Brennan M. J. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):345–349. doi: 10.1073/pnas.88.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pierschbacher M. D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 1984 May 3;309(5963):30–33. doi: 10.1038/309030a0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Roberts M., Fairweather N. F., Leininger E., Pickard D., Hewlett E. L., Robinson A., Hayward C., Dougan G., Charles I. G. Construction and characterization of Bordetella pertussis mutants lacking the vir-regulated P.69 outer membrane protein. Mol Microbiol. 1991 Jun;5(6):1393–1404. doi: 10.1111/j.1365-2958.1991.tb00786.x. [DOI] [PubMed] [Google Scholar]
  18. Ruoslahti E., Pierschbacher M. D. Arg-Gly-Asp: a versatile cell recognition signal. Cell. 1986 Feb 28;44(4):517–518. doi: 10.1016/0092-8674(86)90259-x. [DOI] [PubMed] [Google Scholar]
  19. Stibitz S., Aaronson W., Monack D., Falkow S. Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature. 1989 Mar 16;338(6212):266–269. doi: 10.1038/338266a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Tuomanen E., Weiss A. Characterization of two adhesins of Bordetella pertussis for human ciliated respiratory-epithelial cells. J Infect Dis. 1985 Jul;152(1):118–125. doi: 10.1093/infdis/152.1.118. [DOI] [PubMed] [Google Scholar]
  22. Urisu A., Cowell J. L., Manclark C. R. Filamentous hemagglutinin has a major role in mediating adherence of Bordetella pertussis to human WiDr cells. Infect Immun. 1986 Jun;52(3):695–701. doi: 10.1128/iai.52.3.695-701.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Weiss A. A., Hewlett E. L. Virulence factors of Bordetella pertussis. Annu Rev Microbiol. 1986;40:661–686. doi: 10.1146/annurev.mi.40.100186.003305. [DOI] [PubMed] [Google Scholar]

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

RESOURCES