The O antigen is a critical antigen for the development of a protective immune response to Bordetella parapertussis

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 5050-5058

  Zhang, Xuqing ^a   Goebel, Elizabeth M ^a   Rodríguez, Maria Eugenia ^b   Preston, Andrew ^c   Harvill, Eric T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Universidad Nacional de La Plata   (Argentina)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA PERTUSSIS TETANUS VACCINE; GAMMA INTERFERON; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; O ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BORDETELLA PARAPERTUSSIS; BORDETELLA PARAPERTUSSIS INFECTION; CONTROLLED STUDY; DRUG EFFICACY; IMMUNE RESPONSE; IMMUNIZATION; LOWER RESPIRATORY TRACT; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; BLOTTING, WESTERN; BORDETELLA INFECTIONS; BORDETELLA PARAPERTUSSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICE; MICE, INBRED C57BL; O ANTIGENS;

EID: 70350435097     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00667-09     Document Type: Article

References (59)

1. Allen, A., and D. Maskell. 1996. The identification, cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordetella pertussis. Mol. Microbiol. 19:37-52.
2. Allen, A. G., R. M. Thomas, J. T. Cadisch, and D. J. Maskell. 1998. Molecular and functional analysis of the lipopolysaccharide biosynthesis locus wlb from Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Mol. Microbiol. 29:27-38.
3. Bergfors, E., B. Trollfors, J. Taranger, T. Lagergard, V. Sundh, and G. Zackrisson. 1999. Parapertussis and pertussis: differences and similarities in incidence, clinical course, and antibody responses. Int. J. Infect. Dis. 3:140-146.
4. Borska, K., and M. Simkovicová. 1972. Studies on the circulation of Bordetella pertussis and Bordetella parapertussis in populations of children. J. Hyg. Epidemiol. Microbiol. Immunol. 16:159-172.
5. CDC. 2002. Pertussis-United States, 1997-2000. JAMA 287:977-979.
6. Cherry, J. D., D. X. Xing, P. Newland, K. Patel, U. Heininger, and M. J. Corbel. 2004. Determination of serum antibody to Bordetella pertussis adenylate cyclase toxin in vaccinated and unvaccinated children and in children and adults with pertussis. Clin. Infect. Dis. 38:502-507.
7. Circolo, A., G. Garnier, W. Fukuda, X. Wang, T. Hidvegi, A. J. Szalai, D. E. Briles, J. E. Volanakis, R. A. Wetsel, and H. R. Colten. 1999. Genetic disruption of the murine complement C3 promoter region generates deficient mice with extrahepatic expression of C3 mRNA. Immunopharmacology 42:135-149. (Pubitemid 29322296)
8. Cummings, C. A., M. M. Brinig, P. W. Lepp, S. van de Pas, and D. A. Relman. 2004. Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J. Bacteriol. 186:1484-1492.
9. David, S., R. van Furth, and F. R. Mooi. 2004. Efficacies of whole cell and acellular pertussis vaccines against Bordetella parapertussis in a mouse model. Vaccine 22:1892. (Pubitemid 38581058)
10. de Melker, H. E., J. F. Schellekens, S. E. Neppelenbroek, F. R. Mooi, H. C. Rumke, and M. A. Conyn-van Spaendonck. 2000. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg. Infect. Dis. 6:348-357.
11. Goebel, E. M., D. N. Wolfe, K. Elder, S. Stibitz, and E. T. Harvill. 2008. O antigen protects Bordetella parapertussis from complement. Infect. Immun. 76:1774-1780.
12. Gopinathan, L., G. S. Kirimanjeswara, D. N. Wolfe, M. L. Kelley, and E. T. Harvill. 2007. Different mechanisms of vaccine-induced and infection-induced immunity to Bordetella bronchiseptica. Microbes Infect. 9:442-448. (Pubitemid 46436541)
13. Harvill, E. T., A. Preston, P. A. Cotter, A. G. Allen, D. J. Maskell, and J. F. Miller. 2000. Multiple roles for Bordetella lipopolysaccharide molecules during respiratory tract infection. Infect. Immun. 68:6720-6728.
14. He, Q., M. K. Viljanen, H. Arvilommi, B. Aittanen, and J. Mertsola. 1998. Whooping cough caused by Bordetella pertussis and Bordetella parapertussis in an immunized population. JAMA 280:635-637. (Pubitemid 28502641)
15. Heininger, U., K. Stehr, P. Christenson, and J. D. Cherry. 1999. Evidence of efficacy of the Lederle/Takeda acellular pertussis component diphtheria and tetanus toxoids and pertussis vaccine but not the Lederle whole-cell component diphtheria and tetanus toxoids and pertussis vaccine against Bordetella parapertussis infection. Clin. Infect. Dis. 28:602-604.
16. 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.
17. Khelef, N., B. Danve, M. J. Quentin-Millet, and N. Guiso. 1993. Bordetella pertussis and Bordetella parapertussis: two immunologically distinct species. Infect. Immun. 61:486-490.
18. Kirimanjeswara, G. S., L. M. Agosto, M. J. Kennett, O. N. Bjornstad, and E. T. Harvill. 2005. Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis. J. Clin. Investig. 115: 3594-3601.
19. Kirimanjeswara, G. S., P. B. Mann, and E. T. Harvill. 2003. Role of antibodies in immunity to Bordetella infections. Infect. Immun. 71:1719-1724.
20. Kubler-Kielb, J., E. Vinogradov, G. Ben-Menachem, V. Pozsgay, J. B. Robbins, and R. Schneerson. 2008. Saccharide/protein conjugate vaccines for Bordetella species: preparation of saccharide, development of new conjugation procedures, and physico-chemical and immunological characterization of the conjugates. Vaccine 26:3587-3593.
21. Letowska, I., and W. Hryniewicz. 2004. Epidemiology and characterization of Bordetella parapertussis strains isolated between 1995 and 2002 in and around Warsaw, Poland. Eur. J. Clin. Microbiol. Infect. Dis. 23:499-501.
22. Li, J., C. Ryder, M. Mandal, F. Ahmed, P. Azadi, D. S. Snyder, R. D. Pechous, T. Zahrt, and T. J. Inzana. 2007. Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS. Microbiology 153:3141-3153. (Pubitemid 47517074)
23. Liese, J. G., C. Renner, S. Stojanov, B. H. Belohradsky, and the Munich Vaccine Study Group. 2003. Clinical and epidemiological picture of B pertussis and B parapertussis infections after introduction of acellular pertussis vaccines. Arch. Dis. Child. 88:684-687.
24. Maixnerova, M. 2003. The 2001 serological survey in the Czech Republic- parapertussis. Cent. Eur. J. Public Health 11(Suppl.):S23-S24.
25. Mann, P., E. Goebel, J. Barbarich, M. Pilione, M. Kennett, and E. Harvill. 2007. Use of a genetically defined double mutant strain of Bordetella bronchiseptica lacking adenylate cyclase and type III secretion as a live vaccine. Infect. Immun. 75:3665-3672.
26. Mann, P. B., D. Wolfe, E. Latz, D. Golenbock, A. Preston, and E. T. Harvill. 2005. Comparative Toll-like receptor 4-mediated innate host defense to Bordetella infection. Infect. Immun. 73:8144-8152.
27. Mastrantonio, P., P. Stefanelli, M. Giuliano, Y. Herrera Rojas, M. Ciofi degli Atti, A. Anemona, and A. E. Tozzi. 1998. Bordetella parapertussis infection in children: epidemiology, clinical symptoms, and molecular characteristics of isolates. J. Clin. Microbiol. 36:999-1002.
28. Mattoo, S., and J. D. Cherry. 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18:326-382. (Pubitemid 40548297)
29. Mills, K. H. 2001. Immunity to Bordetella pertussis. Microbes Infect. 3:655-677.
30. Mills, K. H., A. Barnard, J. Watkins, and K. Redhead. 1993. Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect. Immun. 61:399-410.
31. Mooi, F. R., H. G. van der Heide, A. R. ter Avest, K. G. Welinder, I. Livey, B. A. van der Zeijst, and W. Gaastra. 1987. Characterization of fimbrial subunits from Bordetella species. Microb. Pathog. 2:473-484.
32. Munford, R. S., and A. W. Varley. 2006. Shield as signal: lipopolysaccharides and the evolution of immunity to gram-negative bacteria. PLoS Pathog. 2:e67.
33. Nicosia, A., A. Bartoloni, M. Perugini, and R. Rappuoli. 1987. Expression and immunological properties of the five subunits of pertussis toxin. Infect. Immun. 55:963-967.
34. Nicosia, A., and R. Rappuoli. 1987. Promoter of the pertussis toxin operon and production of pertussis toxin. J. Bacteriol. 169:2843-2846. (Pubitemid 17104354)
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. Phalipon, A., C. Costachel, C. Grandjean, A. Thuizat, C. Guerreiro, M. Tanguy, F. Nato, B. Vulliez-Le Normand, F. Belot, K. Wright, V. Marcel- Peyre, P. J. Sansonetti, and L. A. Mulard. 2006. Characterization of functional oligosaccharide mimics of the Shigella flexneri serotype 2a O-antigen: implications for the development of a chemically defined glycoconjugate vaccine. J. Immunol. 176:1686-1694. (Pubitemid 43134313)
37. Pilione, M. R., and E. T. Harvill. 2006. The Bordetella bronchiseptica type III secretion system inhibits gamma interferon production that is required for efficient antibody-mediated bacterial clearance. Infect. Immun. 74:1043-1049.
38. Pishko, E. J., G. S. Kirimanjeswara, M. R. Pilione, L. Gopinathan, M. J. Kennett, and E. T. Harvill. 2004. Antibody-mediated bacterial clearance from the lower respiratory tract of mice requires complement component C3. Eur. J. Immunol. 34:184-193.
39. Preston, A., A. G. Allen, J. Cadisch, R. Thomas, K. Stevens, C. M. Churcher, K. L. Badcock, J. Parkhill, B. Barrell, and D. J. Maskell. 1999. Genetic basis for lipopolysaccharide O-antigen biosynthesis in bordetellae. Infect. Immun. 67:3763-3767.
40. Preston, A., B. O. Petersen, J. O. Duus, J. Kubler-Kielb, G. Ben-Menachem, J. Li, and E. Vinogradov. 2006. Complete structures of Bordetella bronchiseptica and Bordetella parapertussis lipopolysaccharides. J. Biol. Chem. 281: 18135-18144.
41. Repp, R., T. Valerius, A. Sendler, M. Gramatzki, H. Iro, J. R. Kalden, and E. Platzer. 1991. Neutrophils express the high affinity receptor for IgG (Fc gamma RI, CD64) after in vivo application of recombinant human granulocyte colony-stimulating factor. Blood 78:885-889.
42. Rodriguez, M. E., S. M. Hellwig, D. F. Hozbor, J. Leusen, W. L. van der Pol, and J. G. van de Winkel. 2001. Fc receptor-mediated immunity against Bordetella pertussis. J. Immunol. 167:6545-6551.
43. Rodriguez, M. E., W. L. Van der Pol, and J. G. Van de Winkel. 2001. Flow cytometry-based phagocytosis assay for sensitive detection of opsonic activity of pneumococcal capsular polysaccharide antibodies in human sera. J. Immunol. Methods 252:33-44.
44. 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.
45. Stanislavsky, E. S., T. A. Makarenko, and T. E. Kozhenova. 1992. Specific and non-specific mouse protection induced by different chemotypes of the Pseudomonas aeruginosa lipopolysaccharides. FEMS Microbiol. Immunol. 5:181-189.
46. Stibitz, S., and M. S. Yang. 1991. Subcellular localization and immunological detection of proteins encoded by the vir locus of Bordetella pertussis. J. Bacteriol. 173:4288-4296.
47. van den Akker, W. M. 1998. Lipopolysaccharide expression within the genus Bordetella: influence of temperature and phase variation. Microbiology 144: 1527-1535.
48. van der Zee, A., F. Mooi, J. Van Embden, and J. Musser. 1997. Molecular evolution and host adaptation of Bordetella spp.: phylogenetic analysis using multilocus enzyme electrophoresis and typing with three insertion sequences. J. Bacteriol. 179:6609-6617.
49. von Koenig, C. H., A. Tacken, and H. Finger. 1988. Use of supplemented Stainer-Scholte broth for the isolation of Bordetella pertussis from clinical material. J. Clin. Microbiol. 26:2558-2560.
50. Watanabe, M., and M. Nagai. 2004. Whooping cough due to Bordetella parapertussis: an unresolved problem. Expert Rev. Anti-Infect. Ther. 2:447-454.
51. Weingart, C. L., G. Broitman-Maduro, G. Dean, S. Newman, M. Peppler, and A. A. Weiss. 1999. Fluorescent labels influence phagocytosis of Bordetella pertussis by human neutrophils. Infect. Immun. 67:4264-4267.
52. Willems, R. J., J. Kamerbeek, C. A. Geuijen, J. Top, H. Gielen, W. Gaastra, and F. R. Mooi. 1998. The efficacy of a whole cell pertussis vaccine and fimbriae against Bordetella pertussis and Bordetella parapertussis infections in a respiratory mouse model. Vaccine 16:410-416. (Pubitemid 28010778)
53. Wirsing von Konig, C. H., D. Gounis, S. Laukamp, H. Bogaerts, and H. J. Schmitt. 1999. Evaluation of a single-sample serological technique for diagnosing pertussis in unvaccinated children. Eur. J. Clin. Microbiol. Infect. Dis. 18:341-345.
54. Wirsing von Konig, C. H., and H. J. Schmitt. 1996. Epidemiologic aspects and diagnostic criteria for a protective efficacy field trial of a pertussis vaccine. J. Infect. Dis. 174(Suppl. 3):S281-S286.
55. Wolfe, D. N., A. M. Buboltz, and E. T. Harvill. 2009. Inefficient Toll-like receptor-4 stimulation enables Bordetella parapertussis to avoid host immunity. PLoS ONE 4:e4280.
56. Wolfe, D. N., E. M. Goebel, O. N. Bjornstad, O. Restif, and E. T. Harvill. 2007. The O antigen enables Bordetella parapertussis to avoid Bordetella pertussis-induced immunity. Infect. Immun. 75:4972-4979.
57. Wolfe, D. N., G. S. Kirimanjeswara, E. M. Goebel, and E. T. Harvill. 2007. Comparative role of immunoglobulin A in protective immunity against the bordetellae. Infect. Immun. 75:4416-4422.
58. Wolfe, D. N., G. S. Kirimanjeswara, and E. T. Harvill. 2005. Clearance of Bordetella parapertussis from the lower respiratory tract requires humoral and cellular immunity. Infect. Immun. 73:6508-6513.
59. Zhang, X., M. E. Rodriguez, and E. T. Harvill. 2009. O antigen allows B. parapertussis vaccine-induced immunity by blocking binding and functions of cross-reactive antibodies. PLoS One 4:e6989.