Protective immunity to Bordetella pertussis requires both B cells and CD4+ T cells for key functions other than specific antibody production

Journal of Experimental Medicine

Volumn 191, Issue 11, 2000, Pages 1841-1852

  Leef, Mary ^a   Elkins, Karen L ^b   Barbic, Jerko ^a,c   Shahin, Roberta D ^a  

^a Center for Biologics Evaluation/Res   (United States)

^b Ctr Biologics Eval Res Food D   (United States)

^c University Hospital   (Croatia)

Author keywords

B cell; Immunization; Pertussis; Protective immunity; T cell

Indexed keywords

ANTIBODY; GAMMA INTERFERON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; B LYMPHOCYTE; BORDETELLA PERTUSSIS; CONTROLLED STUDY; IMMUNITY; IMMUNIZATION; IMMUNOREGULATION; INFECTION CONTROL; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PERTUSSIS; PRIORITY JOURNAL; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, BACTERIAL; B-LYMPHOCYTES; BORDETELLA PERTUSSIS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; VACCINATION; WHOOPING COUGH;

EID: 0034608713     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.11.1841     Document Type: Article

References (37)

1. Cherry, J.D., P.A. Brunell, G.S. Golden, and D.T. Karzon. 1988. Report of the task force on pertussis and pertussis immunization. Pediatrics. 81:939-984.
2. Cherry, J.D. 1999. Epidemiological, clinical, and laboratory aspects of pertussis in adults. Clin. Infect. Dis. 28(Suppl. 2): S112-S117.
3. Lambert, H.J. 1965. Epidemiology of a small pertussis outbreak in Kent County, Michigan. Public Health Rep. 80:365-369.
4. Cherry, J.D. 1996. Historical review of pertussis and the classical vaccine. J. Infect. Dis. 174(Suppl. 3):S259-S263.
5. Schmitt-Grohé, S., J.D. Cherry, U. Heininger, M.A. Überall, E. Pineda, and K. Stehr. 1995. Pertussis in German adults. Clin. Infect. Dis. 21:860-866.
6. Gustafsson, L., H.O. Hallander, P. Olin, E. Reizenstein, and J. Storsaeter. 1996. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N. Engl. J. Med. 334:349-355.
7. Greco, D., S. Salmaso, P. Mastrantonio, M. Giuliano, A.E. Tozzi, A. Anemona, M.L. Ciofi degli Atti, A. Giammanco, P. Panei, W.C. Blackwelder, et al. 1996. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse Working Group. N. Engl. J. Med. 334:341-348.
8. Cherry, J.D., J. Gornbein, U. Heininger, and K. Stehr. 1998. A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine. 16:1901-1906.
9. Storsaeter, J., H.O. Hallander, L. Gustafsson, and P. Olin. 1998. Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine. 16: 1907-1916.
10. Shahin, R.D., M.J. Brennan, Z.M. Li, B.D. Meade, and C.R. Manclark. 1990. Characterization of the protective capacity and immunogenicity of the 69-kD outer membrane protein of Bordetella pertussis. J. Exp. Med. 171:63-73.
11. Shahin, R.D., J. Hamel, M.F. Leef, and B.R. Brodeur. 1994. Analysis of protective and nonprotective monoclonal antibodies specific for Bordetella pertusis lipooligosaccharide. Infect. Immun. 62:722-725.
12. Mountzouros, K.T., A. Kimura, and J.L. Cowell. 1992. A bactericidal monoclonal antibody specific for the lipooligosaccharide of Bordetella pertussis reduces colonization of the respiratory tract of mice after aerosol intection with B. pertussis. Infect. Immun. 60:5316-5318.
13. Sato, H., A. Ito, J. Chiba, and Y. Sato. 1984. Monoclonal antibody against pertussis toxin: effect on toxin activity and pertussis infections. Infect. Immun. 46:422-428.
14. Halperin, S.A., T.B. Issekutz, and A. Kasina. 1991. Modulation of Bordetella pertussis infection with monoclonal antibodies to pertussis toxin. J. Infect. Dis. 163:355-361.
15. 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-γ receptor or immunoglobulin μ chain genes. J. Exp. Med. 186:1843-1851.
16. Ryan, M., G. Murphy, L. Gothefors, L. Nilsson, J. Storsaeter, and K.H. Mills. 1997. Bordetella pertussis respiratory infection in children is associated with preferential activation of type 1 T helper cells. J. Infect. Dis. 175:1246-1250.
17. 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.
18. Redhead, K., J. Watkins, A. Barnard, and K.H. Mills. 1993. Effective immunization against Bordetella pertusis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect. Immun. 61:3190-3198.
19. Barbic, J., M.F. Leef, D.L. Burns, and R.D. Shahin. 1997. Role of gamma interferon in natural clearance of Bordetella pertussis infection. Infect. Immun. 65:4904-4908.
20. Cheers, C., and D.F. Gray. 1969. Macrophage behaviour during the complaisant phase of murine pertussis. Immunology. 17:875-887.
21. Saukkonen, K., C. Cabellos, M. Burroughs, S. Prasad, and E. Tuomanen. 1991. Integrin-mediated localization of Bordetella pertussis within macrophages: role in pulmonary colonization. J. Exp. Med. 173:1143-1149.
22. Shahin, R.D., and J.L. Cowell. 1994. Mouse respiratory infection models for pertussis. Methods Enzymol. 235:47-58.
23. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 350:423-426.
24. Chen, J., M. Trounstine, F.W. Alt, F. Young, C. Kurahara, J.F. Loring, and D. Huszar. 1993. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the Jh locus. Int. Immunol. 5:647-656.
25. Shahin, R., M. Leef, J. Eldridge, M. Hudson, and R. Gilley. 1995. Adjuvanticity and protective immunity elicited by Bordetella pertussis antigens encapsulated in poly(DL-lactide-coglycolide) microspheres. Infect. Immun. 63:1195-1200.
26. Shahin, R.D., D.F. Amsbaugh, and M.F. Leef. 1992. Mucosal immunization with filamentous hemagglutinin protects against Bordetella pertussis respiratory infection. Infect. Immun. 60:1482-1488.
27. Arico, B., R. Gross, J. Smida, and R. Rappuoli. 1987. Evolutionary relationships in the genus Bordetella. Mol. Microbiol. 1: 301-308.
28. Petersen, J.W., P.H. Ibsen, K. Haslov, and I. Heron. 1992. Proliferative responses and gamma interferon and tumor necrosis factor production by lymphocytes isolated from tracheobroncheal lymph nodes and spleen of mice aerosol infected with Bordetella pertussis. Infect. Immun. 60:4563-4570.
29. 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.
30. Berstad, A.K., J. Holst, B. Mogster, I.L. Haugen, and B. Haneberg. 1997. A nasal whole-cell pertussis vaccine can induce strong systemic and mucosal antibody responses which are not enhanced by cholera toxin. Vaccine. 15:1473-1478.
31. Mills, K.H., M. Ryan, E. Ryan, and B.P. Mahon. 1998. A murine model in which protection correlates with pertussis vaccine efficacy in children reveals complementary roles for humoral and cell-mediated immunity in protection against Bordetella pertussis. Infect. Immun. 66:594-602.
32. Golovkine, T.V., M. Shlomchik, L. Hannum, and A. Chervonsky. 1999. Organogenic role of B lymphocytes in mucosal immunity. Science. 286:1965-1968.
33. Elkins, K.L., CM. Bosio, and T.R. Rhinehart-Jones. 1999. Importance of B cells, but not specific antibodies, in primary and secondary protective immunity to the model intracellular bacterium, Francisella tularensis live vaccine strain. Infect. Immun. 67:6002-6007.
34. Elkins, K.L., P.W. Stashak, and P.J. Baker. 1987. Cell-associated IgM, but not IgD or I-A/E, is important in the activation of suppressor T cells by antigen-primed B cells. J. Immunol. 139:695-701.
35. Roth, R., and M.J. Mamula. 1997. Trafficking of adoptively transferred B lymphocytes in B-lymphocyte-deficient mice. J. Exp. Biol. 200:2057-2062.
36. Bosio, C.M., D. Gardner, and K.L. Elkins. 2000. Infection of B cell-deficient mice with CDC 1551, a clinical isolate of Mycobacterium tuberculosis: delay in dissemination and development of lung pathology. J. Immunol. In press.
37. Ewanowich, C.A., A.R. Melton, A.A. Weiss, R.K. Sherburne, and M.S. Peppler. 1989. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect. Immun. 57:2698-2704.