Direct anti-inflammatory effect of a bacterial virulence factor: IL-10-dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella peptussis

European Journal of Immunology

Volumn 30, Issue 2, 2000, Pages 415-422

  McGuirk, Peter ^a   Mills, Kingston H G ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Bordetella pertussis; CR3 integrin; IL 10; IL 12; Immune subversion

Indexed keywords

ANTIBODY; BACTERIUM LIPOPOLYSACCHARIDE; GAMMA INTERFERON; HEMAGGLUTININ; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD LEVEL; BORDETELLA PERTUSSIS; CYTOKINE PRODUCTION; ESCHERICHIA COLI; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK;

ANIMALS; BORDETELLA PERTUSSIS; HEMAGGLUTININS; IMMUNITY; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-12; MICE; MICE, INBRED BALB C; WHOOPING COUGH;

EID: 0033952395     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-4141(200002)30:2<415::AID-IMMU415>3.0.CO;2-X     Document Type: Article

References (32)

1. Trinchieri, G., Interleukin-12: A proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 1995. 13: 251-276.
2. Trembleau, S., Penna, G., Bosi, E., Mortara, A., Gately, M. K. and Adorini, L., Interleukin-12 administration induces T helper type cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 1995. 18: 817-821.
3. Skeen, M. J., Miller, M. A., Shinnick, T. M. and Ziegler, H. K., Regulation of macrophage IL-12 production. Activation of macrophages in vivo, restimulation in vitro, and modulation by other cytokines. J. Immunol 1996. 156: 1196-1206.
4. D'Andrea, A., Ma, X., Aste-Amezaga, M., Paganin, C. and Trinchieri, G., Stimulatory and inhibitory effects of interleukin (IL)-4 and IL-13 on production of cytokines by human peripheral blood mononuclear cells: priming for IL-1 and tumour necrosis factor-α production. J. Exp. Med. 1995. 181: 537-546.
5. Marth, T. and Kelsall, B. L., Regulation of interleukin-12 by complement receptor 3 signalling. J. Exp. Med. 1997. 11: 1987-1995.
6. Sutterwala, F. S., Noel, G. J., Clynes, R. and Mosser, D. M., Selective suppression of interleukin-12 induction after macrophage receptor ligation. J. Exp. Med. 1997. 185: 1977-1985.
7. Sutterwala, F. S., Noel, G. J., Salgame, P. and Mosser, D. M., Reversal of proinflammatory responses by ligating the macrophage Fcγ receptor type 1. J. Exp. Med. 1998. 188: 217-222.
8. Kishimoto, T. K., Larson, R. S., Corbi, A. L., Dustin, M. L., Staunton, D. E. and Springer, T. A., The leukocyte integrins. Adv. Immunol. 1989. 46: 149-182.
9. Relman, D., Tuomanen, E., Falkow, S., Golenbock, D. T., Saukkonen, K. and Wright, S. D., Recognition of a bacterial adhesion by an integrin: macrophage CR3 (CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 1990. 61: 1375-1382.
10. Ross, G. D. and Vetvicka, V., CR3 (CD11b/CD18): a phagocyte and NK cell membrane receptor with multiple ligand specificities and function. Clin. Exp. Immunol. 1993. 92: 181-184.
11. Goodrum, K. J., McCormick, L. L. and Schneider, B., Group B streptococcus nitric oxide production in murine macrophages is CR3 (CD11b/CD18) dependent. Infect. Immun. 1994. 62: 3102-310.
12. Johnson, L. L., Gibson, G. W. and Sayles, P. C., CR3-dependent resistance to acute Toxoplasma gondii infection in mice. Infect. Immun. 1996. 64: 1998-2003.
13. Rosen, H., Gordon, S. and North, R. J., Exacerbation of murine listeriosis by a monoclonal antibody specific for the type 3 complement receptor of myelomonocytic cells. J. Exp. Med. 1989. 170: 27-38.
14. Saukkonen, E., Cabellos, C., Burroughs, M., Parsad, S. and Tuomanen, E., Integrin-mediated localization of Bordetella pertussis within macrophages: Role in pulmonary colonization. J. Exp. Med. 1991. 173: 1143-1149.
15. Friedman, R. L., Nordensson, K., Wilson, L., Akporiaye, E. T. and Yocum, D. E., Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect. Immun. 1992. 60: 4578-4585.
16. Mills, K. H. G., Barnard, A., Watkins, J. and Redhead, K., Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect. Immun. 1993. 61: 399-410.
17. Mahon, B. P., Sheahan, B. J., Griffin, F., Murphy, G. and Mills, K. H. G., Atypical disease after Bordetella pertussis respiratory infection of mice with targeted disruptions of interferon-γ receptor or immunoglobulin μ chain genes. J. Exp. Med. 1997. 186: 184-1851.
18. Mahon, B. P., Ryan, M. S., Griffin, F. and Mills, K. H. G., Interleukin-12 is produced by macrophages in response to live or killed Bordetella pertussis and enhances the efficacy of an acellular pertussis vaccine by promoting induction of Th1 cells. Infect. Immun. 1996. 64: 5295-5301.
19. McGuirk, P., Mahon, B. P., Griffin, F. and Mills, K. H. G., Comparmentalization of T cell responses following respiratory infection with Bordetella pertussis: hyporesponsiveness of lung T cells is associaed with modulated expression of the co-stimulatory molecule CD28. Eur. J. Immunol. 1998. 28: 153-163.
20. Mattner, F., Fischer, S., Guckes, S., Jin, S., Kaulen, H., Schmitt, E., Rude, E. and Germann, T., The interleukin-12 sub-unit p40 specifically inhibits effects of the interleukin heterodimer. Eur. J. Immunol. 1993. 23: 2202-2208.
21. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P. and Mills, K. H. G., Pertussis Toxin potentiates Th1 and Th2 responses to co-injected antigen: adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7-1, B7-2 and CD28. Int. Immunol. 1998. 10: 651-662.
22. Redhead, K., Watkins, J., Barnard, A. and Mills, K. H. G., Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infect. Immun. 1993. 61: 3190-3198.
23. Ryan, M., Murphy, G., Ryan, E., Nilsson, L., Shackley, F., Gothefors, L., Oymar, K., Miller, E., Storsaeter, J. and Mills, K. H. G., Distinct Th cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 1998. 93: 1-10.
24. Ausiello, C. M., Urbani, F., la Sala, A., Lande, R. and Cassone, A., Vaccine- and antigen-dependent type 1 and type 2 cytokine induction after primary vaccination of infants with whole-cell or acellular pertussis vaccines. Infect. Immun. 1997. 65: 2168-2174.
25. Karp, C. L., Wysocka, M., Wahl, L. M., Ahearn, J. M., Cuomo, P. J., Sherry, B., Trinchieri, G. and Griffin, D. E., Mechanism of suppression of cell-mediated immunity by measles virus. Science 1996. 273: 228-231.
26. Chougnet, C., Wynn, T. A., Clerici, M., Landay, A. L., Kessler, H. A., Rusnak, J., Melcher, G. P., Sher, A. and Shearer, G. M., Molecular analysis of decreased interleukin-12 production in persons infected with human immunodeficiency virus. J. Infect. Dis. 1996. 174: 46-53.
27. Carrera, L., Gazzinelli, R. T., Badolato, R., Hieny, S., Muller, W., Kuhn, R. and Sacks, D. L., Leishmania promastigotes selectively inhibit interleukin-12 induction in bone marrow-derived macrophages from susceptible and resistance mice. J. Exp. Med. 1996. 183: 515-526.
28. Locht, C., Bertin, P., Menozzi, F. D. and Renauld, G., The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetalla spp. Mol. Microbiol. 1993. 9: 653-660.
29. Heinzel, F. P., Rerko, R. M., Ling, P., Hakimi, J. and Schoenhaut, D. S., Interleukin 12 is produced in vivo during endotoxemia and stimulates synthesis of gamma Interferon. Infect. Immun. 1994. 62: 4244-4249.
30. Everest, P., Li, J., Douce, G., Charles, I., De Azavedo, J., Chatfield, S., Dougan, G. and Roberts, M., Role of Bordetella pertussis P.69/pertactin protein and the P.69/pertactin RGD motif in the adherance to and invasion of mammalian cells. Microbiology 1996. 142: 3261-3268.
31. Gustafsson, L., Hallander, H. O., Olin, P., Reizenstein, E. and Storsaeter, J., A controlled trial of a two-component acellular a five-component acellular and a whole cell Pertussis vaccine. N. Engl. J. Med. 1996. 334: 349-355.
32. Torre, D., Speranza, F., Pugliese, A., Perversi, L., Marone, P. and Ferrario, G., Effects of recombinant murine (rm) interleukin-12 and rm interferon-gamma in mice infected with Bordetella pertussis. J. Infect. Dis 1996. 174: 786-789.