Bordetella bronchiseptica adherence to cilia is mediated by multiple adhesin factors and blocked by surfactant protein A

Infection and Immunity

Volumn 73, Issue 6, 2005, Pages 3618-3626

  Edwards, Jessica A ^a   Groathouse, Nathan A ^b   Boitano, Scott ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADHESIN; HEMAGGLUTININ; HEMOLYSIN; PERTACTIN; SURFACTANT PROTEIN A; TOXIN;

ANIMAL CELL; ARTICLE; BACTERIUM ADHERENCE; BINDING AFFINITY; BORDETELLA BRONCHISEPTICA; CELL CULTURE; EUKARYOTIC FLAGELLUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; RABBIT; SCANNING ELECTRON MICROSCOPY; TRACHEA MUCOSA;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BORDETELLA BRONCHISEPTICA; CILIA; HEMAGGLUTININS; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; RABBITS;

EID: 19744370931     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.6.3618-3626.2005     Document Type: Article

References (53)

1. Akerley, B. J., P. A. Cotter, and J. F. Miller. 1995. Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80:611-620.
2. Brockmeier, S. L., K. B. Register, T. Magyar, A. J. Lax, G. D. Pullinger, and R. A. Kunkle. 2002. Role of the dermonecrotic toxin of Bordetella bronchiseptica in the pathogenesis of respiratory disease in swine. Infect. Immun. 70:481-490.
3. Cherry, J. D. 1999. Epidemiological, clinical, and laboratory aspects of pertussis in adults. Clin. Infect. Dis. 28(Suppl. 2):S112-S117.
4. Cotter, P. A., and J. F. Miller. 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62:3381-3390.
5. Cotter, P. A., M. H. Yuk, S. Mattoo, B. J. Akerley, J. Boschwitz, D. A. Relman, and J. F. Miller. 1998. Filamentous hemagglutinin of Bordetella bronchiseptica is required for efficient establishment of tracheal colonization. Infect. Immun. 66:5921-5929.
6. Crouch, E., and J. R. Wright. 2001. Surfactant proteins A and D and pulmonary host defense. Annu. Rev. Physiol. 63:521-554.
7. Diamond, G., D. Legarda, and L. K. Ryan. 2000. The innate immune response of the respiratory epithelium. Immunol. Rev. 173:27-38.
8. Dirksen, E. R., J. A. Felix, and M. J. Sanderson. 1995. Preparation of explant and organ cultures and single cells from airway epithelium. Methods Cell Biol. 47:65-74.
9. Eggleton, P., and K. B. Reid. 1999. Lung surfactant proteins involved in innate immunity. Curr. Opin. Immunol. 11:28-33.
10. Emsley, P., I. G. Charles, N. F. Fairweather, and N. W. Isaacs. 1996. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381:90-92.
11. Geuijen, C. A., R. J. Willems, and F. R. Mooi. 1996. The major fimbrial subunit of Bordetella pertussis binds to sulfated sugars. Infect. Immun. 64: 2657-2665.
12. Goodnow, R. A. 1980. Biology of Bordetella bronchiseptica. Microbiol. Rev. 44:722-738.
13. Gray, M. C., W. Ross, K. Kim, and E. L. Hewlett. 1999. Characterization of binding of adenylate cyclase toxin to target cells by flow cytometry. Infect. Immun. 67:4393-4399.
14. 2+ transients in ciliated tracheal epithelial cells. Infect. Immun. 71:7208-7210.
15. Hannah, J. H., F. D. Menozzi, G. Renauld, C. Locht, and M. J. Brennan. 1994. Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect. Immun. 62:5010-5019.
16. Harvill, E. T., P. A. Cotter, M. H. Yuk, and J. F. Miller. 1999. Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect. Immun. 67:1493-1500.
17. Hastie, A. T., M. J. Krantz, and F. P. Colizzo. 1990. Identification of surface components of mammalian respiratory tract cilia. Cell Motil. Cytoskelet. 17:317-328.
18. Hazenbos, W. L., C. A. Geuijen, B. M. van den Berg, F. R. Mooi, and R. van Furth. 1995. Bordetella pertussis fimbriae bind to human monocytes via the minor fimbrial subunit FimD. J. Infect. Dis. 171:924-929.
19. Hazenbos, W. L., B. M. van den Berg, C. W. Geuijen, F. R. Mooi, and R. van Furth. 1995. Binding of FimD on Bordetella pertussis to very late antigen-5 on monocytes activates complement receptor type 3 via protein tyrosine kinases. J. Immunol. 155:3972-3978.
20. Heininger, U., K. Stehr, S. Schmitt-Grohe, C. Lorenz, R. Rost, P. D. Christenson, M. Uberall, and J. D. Cherry. 1994. Clinical characteristics of illness caused by Bordetella parapertussis compared with illness caused by Bordetella pertussis. Pediatr. Infect. Dis. J. 13:306-309.
21. Jacob-Dubuisson, F., B. Kehoe, E. Willery, N. Reveneau, C. Locht, and D. A. Relman. 2000. Molecular characterization of Bordetella bronchiseptica filamentous haemagglutinin and its secretion machinery. Microbiology 146: 1211-1221.
22. Khubchandani, K. R., K. L. Goss, J. F. Engelhardt, and J. M. Snyder. 2001. In situ hybridization of SP-A mRNA in adult human conducting airways. Pediatr. Pathol. Mol. Med. 20:349-366.
23. Kuehn, M. J. 1997. Establishing communication via gram-negative bacterial pili. Trends Microbiol. 5:130-132.
24. Ladant, D., and A. Ullmann. 1999. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 7:172-176.
25. Leininger, E., M. Roberts, J. G. Kenimer, I. G. Charles, N. Fairweather, P. Novotny, and M. J. Brennan. 1991. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. USA 88:345-349.
26. LeVine, A. M., M. D. Bruno, K. M. Huelsman, G. F. Ross, J. A. Whitsett, and T. R. Korfhagen. 1997. Surfactant protein A-deficient mice are susceptible to group B streptococcal infection. J. Immunol. 158:4336-4340.
27. Locht, C., R. Antoine, and F. Jacob-Dubuisson. 2001. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4:82-89.
28. - phase nor the vrg6 locus of Bordetella pertussis is required for respiratory infection in mice. Infect. Immun. 66:2762-2768.
29. Mattoo, S., J. F. Miller, and P. A. Cotter. 2000. Role of Bordetella bronchiseptica fimbriae in tracheal colonization and development of a humoral immune response. Infect. Immun. 68:2024-2033.
30. McCormack, F. X., and J. A. Whitsett. 2002. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J. Clin. Investig. 109: 707-712.
31. Menozzi, F. D., R. Mutombo, G. Renauld, C. Gantiez, J. H. Hannah, E. Leininger, M. J. Brennan, and C. Locht. 1994. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect. Immun. 62:769-778.
32. Merkel, T. J., S. Stibitz, J. M. Keith, M. Leef, and R. Shahin. 1998. Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis. Infect. Immun. 66:4367-4373.
33. Miller, J. F., S. A. Johnson, W. J. Black, D. T. Beattie, J. J. Mekalanos, and S. Falkow. 1992. Constitutive sensory transduction mutations in the Bordetella pertussis bvgS gene. J. Bacteriol. 174:970-979.
34. Reference deleted.
35. Parkhill, J., M. Sebaihia, A. Preston, L. D. Murphy, N. Thomson, D. E. Harris, M. T. Holden, C. M. Churcher, S. D. Bentley, K. L. Mungall, A. M. Cerdeno-Tarraga, L. Temple, K. James, B. Harris, M. A. Quail, M. Achtman, R. Atkin, S. Baker, D. Basham, N. Bason, I. Cherevach, T. Chillingworth, M. Collins, A. Cronin, P. Davis, J. Doggett, T. Feltwell, A. Goble, N. Hamlin, H. Hauser, S. Holroyd, K. Jagels, S. Leather, S. Moule, H. Norberczak, S. O'Neil, D. Ormond, C. Price, E. Rabbinowitsch, S. Rutter, M. Sanders, D. Saunders, K. Seeger, S. Sharp, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, L. Unwin, S. Whitehead, B. G. Barrell, and D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:32-40.
36. Porter, J. F., K. Connor, and W. Donachie. 1994. Isolation and characterization of Bordetella parapertussis-like bacteria from ovine lungs. Microbiology 140:255-261.
37. Prasad, S. M., Y. Yin, E. Rodzinski, E. I. Tuomanen, and H. R. Masure. 1993. Identification of a carbohydrate recognition domain in filamentous hemagglutinin from Bordetella pertussis. Infect. Immun. 61:2780-2785.
38. Relman, D., E. Tuomanen, S. Falkow, D. T. Golenbock, K. Saukkonen, and S. D. Wright. 1990. Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61:1375-1382.
39. Relman, D. A., M. Domenighini, E. Tuomanen, R. Rappuoli, and S. Falkow. 1989. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc. Natl. Acad. Sci. USA 86:2637-2641.
40. Reynolds, H. Y. 2002. Modulating airway defenses against microbes. Curr. Opin. Pulm. Med. 8:154-165.
41. Roberts, M., N. F. Fairweather, E. Leininger, D. Pickard, E. L. Hewlett, A. Robinson, C. Hayward, G. Dougan, and I. G. Charles. 1991. Construction and characterization of Bordetella pertussis mutants lacking the vir-regulated P.69 outer membrane protein. Mol. Microbiol. 5:1393-1404.
42. Saitoh, H., H. Okayama, S. Shimura, T. Fushimi, T. Masuda, and K. Shirato. 1998. Surfactant protein A2 gene expression by human airway submucosal gland cells. Am. J. Respir. Cell. Mol. Biol. 19:202-209.
43. Sakurai, Y., H. Suzuki, and E. Terada. 1993. Purification and characterisation of haemagglutinin from Bordetella bronchiseptica. J. Med. Microbiol. 39:388-392.
44. Schaeffer, L. M., F. X. McCormack, H. Wu, and A. A. Weiss. 2004. Bordetella pertussis lipopolysaccharide resists the bactericidal effects of pulmonary surfactant protein A. J. Immunol. 173:1959-1965.
45. Soane, M. C., A. Jackson, D. Maskell, A. Allen, P. Keig, A. Dewar, G. Dougan, and R. Wilson. 2000. Interaction of Bordetella pertussis with human respiratory mucosa in vitro. Respir. Med. 94:791-799.
46. Stainer, D. W., and M. J. Scholte. 1970. A simple chemically defined medium for the production of phase I Bordetella pertussis. J. Gen. Microbiol. 63:211-220.
47. Temple, L. M., A. A. Weiss, K. E. Walker, H. J. Barnes, V. L. Christensen, D. M. Miyamoto, C. B. Shelton, and P. E. Orndorff. 1998. Bordetella avium virulence measured in vivo and in vitro. Infect. Immun. 66:5244-5251.
48. Tuomanen, E., H. Towbin, G. Rosenfelder, D. Braun, G. Larson, G. C. Hansson, and R. Hill. 1988. Receptor analogs and monoclonal antibodies that inhibit adherence of Bordetella pertussis to human ciliated respiratory epithelial cells. J. Exp. Med. 168:267-277.
49. Tuomanen, E., and A. Weiss. 1985. Characterization of two adhesins of Bordetella pertussis for human ciliated respiratory-epithelial cells. J. Infect. Dis. 152:118-125.
50. van den Berg, B. M., H. Beekhuizen, R. J. L. Willems, F. R. Mooi, and R. van Furth. 1999. Role of Bordetella pertussis virulence factors in adherence to epithelial cell lines derived from the human respiratory tract. Infect. Immun. 67:1056-1062.
51. Weiss, A. A., and S. Falkow. 1984. Genetic analysis of phase change in Bordetella pertussis. Infect. Immun. 43:263-269.
52. Wu, H., A. Kuzmenko, S. Wan, L. Schaffer, A. Weiss, J. H. Fisher, K. S. Kim, and F. X. McCormack. 2003. Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability. J. Clin. Investig. 111:1589-1602.
53. Zaretzky, F. R., M. C. Gray, and E. L. Hewlett 2002. Mechanism of association of adenylate cyclase toxin with the surface of Bordetella pertussis: a role for toxin-filamentous haemagglutinin interaction. Mol. Microbiol. 45:1589-1598.