The O antigen enables Bordetella parapertussis to avoid Bordetella pertussis-induced immunity

Infection and Immunity

Volumn 75, Issue 10, 2007, Pages 4972-4979

  Wolfe, Daniel N ^a   Goebel, Elizabeth M ^b   Bjornstad, Ottar N ^a   Restif, Olivier ^c   Harvill, Eric T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

O ANTIGEN; PERTUSSIS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CONTROLLED STUDY; ENDEMIC DISEASE; MOUSE; NONHUMAN; PERTUSSIS; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, BACTERIAL; BORDETELLA INFECTIONS; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; COLONY COUNT, MICROBIAL; CROSS REACTIONS; INTERFERON TYPE II; LUNG; LYMPHOCYTES; MICE; MICE, INBRED C57BL; NASAL CAVITY; O ANTIGENS; TRACHEA; WHOOPING COUGH;

EID: 34848889597     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00763-07     Document Type: Article

References (62)

1. Anderson, R. M. 1995. Evolutionary pressures in the spread and persistence of infectious agents in vertebrate populations. Parasitology 111(Suppl.):S15-S31.
2. Arico, B., R. Gross, J. Smida, and R. Rappuoli. 1987. Evolutionary relationships in the genus Bordetella. Mol. Microbiol. 1:301-308.
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. Bjornstad, O. N., and E. T. Harvill. 2005. Evolution and emergence of Bordetella in humans. Trends Microbiol. 13:355-359.
5. Burns, V. C., E. J. Pishko, A. Preston, D. J. Maskell, and E. T. Harvill. 2003. Role of Bordetella O antigen in respiratory tract infection. Infect. Immun. 71:86-94.
6. Carbonetti, N. H., G. V. Artamonova, C. Andreason, E. Dudley, R. M. Mays, and Z. E. Worthington. 2004. Suppression of serum antibody responses by pertussis toxin after respiratory tract colonization by Bordetella pertussis and identification of an immunodominant lipoprotein. Infect. Immun. 72:3350-3358.
7. Celentano, L. P., M. Massari, D. Paramatti, S. Salmaso, A. E. Tozzi, and the EUVAC-NET Group. 2005. Resurgence of pertussis in Europe. Pediatr. Infect. Dis. J. 24:761-765.
8. Centers for Disease Control and Prevention. 2002. Pertussis - United States, 1997-2000. JAMA 287:977-979.
9. Cherry, J. D. 1984. The epidemiology of pertussis and pertussis immunization in the United Kingdom and the United States: a comparative study. Curr. Probl. Pediatr. 14:1-78.
10. Crowcroft, N. S., C. Stein, P. Duclos, and M. Birmingham. 2003. How best to estimate the global burden of pertussis? Lancet Infect. Dis. 3:413-418.
11. 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 22:1892-1898.
12. 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.
13. Diavatopoulos, D. A., C. A. Cummings, L. M. Schouls, M. M. Brinig, D. A. Relman, and F. R. Mooi. 2005. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 1:e45.
14. Ferguson, N. M., A. P. Galvani, and R. M. Bush. 2003. Ecological and immunological determinants of influenza evolution. Nature 422:428-433.
15. Gupta, S., M. C. Maiden, I. M. Feavers, S. Snee, R. M. May, and R. M. Anderson. 1996. The maintenance of strain structure in populations of recombining infectious agents. Nat. Med. 2:437-442.
16. Gupta, S., and M. C. J. Maiden. 2001. Exploring the evolution of diversity in pathogen populations. Trends Microbiol. 9:181-185.
17. Harvill, E. T., P. A. Cotter, and J. F. Miller. 1999. Pregenomic comparative analysis between Bordetella bronchiseptica RB50 and Bordetella pertussis Tohama I in murine models of respiratory tract infection. Infect. Immun. 67:6109-6118.
18. 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.
19. Heininger, U., J. D. Cherry, K. Stehr, S. Schmitt-Grohe, M. Uberall, S. Laussucq, T. Eckhardt, M. Meyer, J. Gornbein, et al. 1998. Comparative efficacy of the Lederle/Takeda acellular pertussis component DTP (DTaP) vaccine and Lederle whole-cell component DTP vaccine in German children after household exposure. Pediatrics 102:546-553.
20. Heininger, U., P. A. Cotter, H. W. Fescemyer, G. Martinez de Tejada, M. H. Yuk, J. F. Miller, and E. T. Harvill. 2002. Comparative phenotypic analysis of the Bordetella parapertussis isolate chosen for genomic sequencing. Infect. Immun. 70:3777-3784.
21. Heininger, U., K. Stehr, S. Schmitt-Grohe, C. Lorenz, R. Rost, P. D. Christensen, 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.
22. Kawai, H., T. Aoyama, Y. Murase, C. Tamura, and A. Imaizumi. 1996. A causal relationship between Bordetella pertussis and Bordetella parapertussis infections. Scand. J. Infect. Dis. 28:377-381.
23. Kingsley, R. A., and A. J. Baumler. 2000. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36:1006-1014.
24. Kirimanjeswara, G. S., L. 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.
25. Kirimanjeswara, G. S., P. B. Mann, and E. T. Harvill. 2003. Role of antibodies in immunity to Bordetella infections. Infect. Immun. 71:1719-1724.
26. Lautrop, H. 1971. Epidemics of parapertussis. 20 years' observations in Denmark. Lancet i:1195-1198.
27. + T cells for key functions other than specific antibody production. J. Exp. Med. 191:1841-1852.
28. 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.
29. 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.
30. Lipsitch, M. 1999. Bacterial vaccines and serotype replacement: lessons from Haemophilus influenzae and prospects for Streptococcus pneumoniae. Emcrg. Infect. Dis. 5:336-345.
31. Mahon, B. P., B. J. Sheahan, F. Griffin, G. Murphy, and K. H. Mills. 1997. Atypical disease after Bordetella pertussis respiratory infection of mice with targeted disruptions of interferon-gamma receptor or immunoglobulin mu chain genes. J. Exp. Med. 186:1843-1851.
32. Mahon, B. P., and K. H. Mills. 1999. Interferon-gamma mediated immune effector mechanisms against Bordetella pertussis. Immunol. Lett. 68:213-217.
33. Maixnerova, M. 2003. The 2001 serological survey in the Czech Republic - parapertussis. Cent. Eur. J. Public Health 11(Suppl.):S23-S24.
34. Maixnerova, M. 2003. The 2001 serological survey in the Czech Republic - pertussis. Cent. Eur. J. Public Health 11(Suppl.):S17-S22.
35. Makinen, J., J. Mertsola, H. Soini, H. Arvilomni, M. K. Viljanen, N. Guiso, and Q. He. 2003. PFGE and pertactin gene sequencing suggest limited genetic variability within the Finnish Bordetella parapertussis population. J. Med. Microbiol. 52:1059-1063.
36. 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.
37. Mattoo, S., and J. 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.
38. Mielcarek, N., A. S. Debrie, D. Raze, J. Bertout, C. Rouanet, A. B. Younes, C. Creusy, J. Engle, W. E. Goldman, and C. Locht. 2006. Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog. 2:e65.
39. Morona, R., and L. Van den Bosch. 2003. Lipopolysaccharide O antigen chains mask IcsA (VirG) in Shigella flexneri. FEMS Microbiol. Lett. 221: 173-180.
40. Musser, J. M., E. L. Hewlett, M. S. Peppler, and R. K. Selander. 1986. Genetic diversity and relationships in populations of Bordetella spp. J. Bacteriol. 166:230-237.
41. Olson, L. 1975. Pertussis. Medicine (Baltimore) 54:427-469.
42. 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. Atkins, 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. Noberczak, S. O'Neil, D. Osmond, 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.
43. Pennington, J. E., G. J. Small, M. E. Lostrom, and G. B. Pier. 1986. Polyclonal and monoclonal antibody therapy for experimental Pseudomonas aeruginosa pneumonia. Infect. Immun. 54:239-244.
44. 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.
45. Restif, O., and B. T. Grenfell. 2006. Integrating life history and cross-immunity into the evolutionary dynamics of pathogens. Proc. R. Soc. B 273:409-416.
46. Robbins, J. B., C. Chu, and R. Schneerson. 1992. Hypothesis for vaccine development: protective immunity to enteric diseases caused by nontyphoidal salmonellac and shigellae may be conferred by serum IgG antibodies to the O-specific polysaccharide of their lipopolysaccharides. Clin. Infect. Dis. 15:346-361.
47. Rohani, P., D. J. Earn, and B. T. Grenfell. 1999. Opposite patterns of synchrony in sympatric disease metapopulations. Science 286:968-971.
48. Rohani, P., C. J. Green, N. B. Mantilla-Beniers, and B. T. Grenfell. 2003. Ecological interference between fatal diseases. Nature 422:885-888.
49. Skowronski, D. M., G. De Serres, D. MacDonald, W. Wu, C. Shaw, J. Macnabb, S. Champagne, D. M. Patrick, and S. A. Halperin. 2002. The changing age and seasonal profile of pertussis in Canada. J. Infect. Dis. 185:1448-1453.
50. Stehr, K., J. Cherry, U. Heininger, S. Schmitt-Grohe, M. Uberall, S. Laussucq, T. Eckhardt, M. Meyer, R. Englehardt, and P. Christensen. 1998. A comparative efficacy trial in Germany in infants who received either the Lederle/Takeda acellular pertussis component DTP (DTaP) vaccine, the Lederle whole-cell component DTP vaccine, or DT vaccine. Pediatrics 101: 1-11.
51. 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.
52. Sun, K., S. L. Salmon, S. A. Lotz, and D. W. Metzger. 2007. Interleukin-12 promotes gamma interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect. Immun. 75:1196-1202.
53. van der Ley, P., P. de Graaff, and J. Tommassen. 1986. Shielding of Escherichia coli outer membrane proteins as receptors for bacteriophages and colicins by O-antigenic chains of lipopolysaccharide. J. Bacteriol. 168:449-451.
54. van der Ley, P., O. Kuipers, J. Tommassen, and B. Lugtenberg. 1986. O-antigenic chains of lipopolysaccharide prevent binding of antibody molecules to an outer membrane pore protein in Enterobacteriaceae. Microb. Pathog. 1:43-49.
55. 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.
56. von Konig, C. H., S. Halperin, M. Riffelmann, and N. Guiso. 2002. Pertussis of adults and infants. Lancet Infect. Dis. 2:744-750.
57. Voorhis, D. L., S. Dillon, S. B. Formal, and R. R. Isberg. 1991. An O antigen can interfere with the function of the Yersinia pseudotuberculosis invasin protein. Mol. Microbiol. 5:317-325.
58. Watanabe, M., and M. Nagai. 2001. Reciprocal protective immunity against Bordetella pertussis and Bordetella parapertussis in a murine model of respiratory infection. Infect. Immun. 69:6981-6986.
59. Watanabe, M., and M. Nagai. 2004. Whooping cough due to Bordetella parapertussis: an unresolved problem. Expert Rev. Anti-Infect. Ther. 2:447-454.
60. Wendelboe, A. M., A. Van Rie, S. Salmaso, and J. A. Englund. 2005. Duration of immunity against pertussis after natural infection or vaccination. Pediatr. Infect. Dis. J. 24(5S):S58-S61.
61. 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.
62. Wolfe, D. N., G. 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.