Bordetella bronchiseptica persists in the nasal cavities of mice and triggers early delivery of dendritic cells in the lymph nodes draining the lower and upper respiratory tract

Infection and Immunity

Volumn 71, Issue 7, 2003, Pages 4137-4143

  Gueirard, Pascale ^a   Ave, Patrick ^a   Balazuc, Anne Marie ^a   Thiberge, Sabine ^a   Huerre, Michel ^a   Milon, Genevieve ^a   Guiso, Nicole ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BORDETELLA BRONCHISEPTICA; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HISTOPATHOLOGY; IMMUNOREACTIVITY; INFECTION RESISTANCE; LUNG LAVAGE; LUNG PARENCHYMA; LYMPH NODE; MOUSE; NONHUMAN; NOSE CAVITY; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD11C; BORDETELLA BRONCHISEPTICA; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; LEUKOCYTES; LUNG; LYMPH NODES; LYMPHOID TISSUE; MICE; MICE, INBRED BALB C; NASAL CAVITY;

EID: 0038309663     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.7.4137-4143.2003     Document Type: Article

References (42)

1. Arico, B., R. Gross, J. Smida, and R. Rappuoli. 1987. Evolutionary relationships in the genus Bordetella. Mol. Microbiol. 1:301-308.
2. Dworkin, M. S., P. S. Sullivan, S. E. Buskin, R. D. Harrington, J. Oliffe, R. D. MacArthur, and C. E. Lopez. 1999. Bordetella bronchiseptica infection in human immunodeficiency virus-infected patients. Clin. Infect. Dis. 28:1095-1099.
3. Ferry, N. S. 1912. A preliminary report of the bacterial findings in canine distemper. Am. Vet. Rev. 37:449-504.
4. Fukuyama, S., T. Hiroi, Y. Yokota, P. D. Rennert, M. Yanagita, N. Kinoshita, S. Terawaki, T. Shikina, M. Yamamoto, Y. Kurono, and H. Kiyono. 2002. Initiation of NALT organogenesis is independent of the IL-7R, LTβR, and NIK signaling pathways but requires the Id2 gene and CD3-CD4+CD45+ cells. Immunity 17:31-40.
5. Garcia, S. M., C. Quereda, M. Martinez, P. Martin-Davila, J. Cobo, and A. Guerrero. 1998. Bordetella bronchiseptica cavitary pneumonia in a patient with AIDS. Eur. J. Clin. Microbiol. Infect. Dis. 17:675-676.
6. Gong, J. L., K. M. McCarthy, J. Telford, T. Tamatani, M. Miyasaka, and E. Schneeberger. 1992. Intraepithelial airway dendritic cells: a distinct subset of pulmonary dendritic cells obtained by microdissection. J. Exp. Med. 175:797-807.
7. Goodnow, R. A. 1980. Biology of Bordetella bronchiseptica. Microbiol. Rev. 44:722-738.
8. Gueirard, P., and N. Guiso. 1993. Virulence of Bordetella bronchiseptica: role of adenylate cyclase-hemolysin. Infect. Immun. 61:4072-4078.
9. Gueirard, P., P. Minoprio, and N. Guiso. 1996. Intranasal inoculation of Bordetella bronchiseptica in mice induces long-lasting antibody and T-cell mediated immune responses. Scand. J. Immunol. 43:181-192.
10. Gueirard, P., C. Weber, A. Le Coustumier, and N. Guiso. 1995. Human Bordetella bronchiseptica infection related to contact with infected animals: persistence of bacteria in host. J. Clin. Microbiol. 33:2002-2006.
11. Guiso, N., M. Szatanik, and M. Rocancourt. 1991. Protective activity of Bordetella adenylate cyclase-hemolysin against bacterial colonization. Microb. Pathog. 11:423-431.
12. 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.
13. Heritage, P. L., B. J. Underdown, A. L. Arsenault, D. P. Snider, and M. R. McDermott. 1997. Comparison of murine nasal-associated lymphoid tissue and Peyer's patches. Am. J. Respir. Crit. Care Med. 156:1256-1262.
14. Holt, P. G., M. A. Schon-Hegrad, and J. Oliver. 1988. MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat: regulation of antigen presentation activity by endogenous macrophage population. J. Exp. Med. 167:262-274.
15. Hou, Y., W. G. Hu, T. Hirano, and X. X. Gu. 2002. A new intra-NALT route elicits mucosal and systemic immunity against Moraxella catarrhalis in a mouse challenge model. Vaccine 20:2375-2381.
16. Jungnitz, H., N. P. West, M. J. Walker, G. S. Chhatwal, and C. A. Guzman. 1998. A second two-component regulatory system of Bordetella bronchiseptica required for bacterial resistance to oxidative stress, production of acid phosphatase, and in vivo persistence. Infect. Immun. 66:4640-4650.
17. Kraal, G. Nasal associated lymphoid tissue. In J. Mestecki et al. (ed.), Mucosal immunology, 2nd ed., in press.
18. Lagranderie, M., M. A. Nahori, A. M. Balazuc, H. Kieffer-Biasizzo, J. R. Lapa E Silva, G. Milon, G. Marchal, and B. B. Vargaftig. 2003. Dendritic cells recruited to the lung shortly after intranasal delivery of Mycobacterium bovis BCG drive the primary immune response towards a type 1 cytokine production. Immunology 108:352-364.
19. Lambrecht, B. N., H. C. Hoogsteden, and R. A. Pauwels. 2001. Dendritic cells as regulators of the immune response to inhaled allergen: recent findings in animal models of asthma. Int. Arch. Allergy Immunol. 124:432-436.
20. Lang, T., P. Ave, M. Huerre, G. Milon, and J. C. Antoine. 2000. Macrophage subsets harbouring Leishmania donovani in spleens of infected BALB/c mice; localization and characterization. Cell. Microbiol. 2:415-430.
21. Lipscomb, M. F., and B. J. Masten. 2002. Dendritic cells: immune regulators in health and disease. Physiol. Rev. 82:97-130.
22. Lopez, A. F., M. Strath, and C. J. Sanderson. 1984. Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies. Br. J. Haematol. 57:489-494.
23. Masten, B. J., J. L. Yates, A. M. Pollard Koga, and M. F. Lipscomb. 1997. Characterization of accessory molecules in murine lung dendritic cell function: roles for CD80, CD86, CD54, and CD40L. Am. J. Respir. Cell Mol. Biol. 16:335-342.
24. Mattoo, S., A. K. Foreman-Wykert, P. A. Cotter, and J. F. Miller. 2001. Mechanisms of Bordetella pathogenesis. Front. Biosci. 6: E168-E186.
25. McLellan, A., M. Heldmann, G. Terbeck, F. Weih, C. Linden, E. B. Bröcker, M. Leverkus, and E. Kämpgen. 2000. MHC class II and CD40 play opposing roles in dendritic cell survival. Eur. J. Immunol. 30:2612-2619.
26. McWilliam, A. S., S. Napoli, A. M. Marsh, F. L. Pemper, D. J. Nelson, C. L. Pimm, P. A. Stumbles, T. N. C. Wells, and P. G. Holt. 1996. Dendritic cells are recruited into the airway epithelium during the inflammatory response to a broad spectrum of stimuli. J. Exp. Med. 184:2429-2432.
27. McWilliam, A. S., D. Nelson, J. A. Thomas, and P. G. Holt. 1994. Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces. J. Exp. Med. 179:1331-1336.
28. McWilliam, A. S., P. A. Stumbles, and P. G. Holt. 1999. Dendritic cells in the lung, p. 123-140. In M. T. Loyze and A. W. Thomson (ed.), Dendritic cells: biology and clinical applications. Academic Press, Inc., New York, N.Y.P.A.
29. Nelson, D. J., C. McMenamin, A. S. McWilliam, M. Brenan, and P. G. Holt. 1994. Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J. Exp. Med. 179:203-212.
30. Pajak, B., T. De Smedt, V. Moulin, C. De Trez, R. Maldonado-Lopez, G. Vansanten, E. Briend, J. Urbain, O. Leo, and M. Moser. 2000. Immunohistowax processing, a new fixation and embedding method for light microscopy, which preserves antigen immunoreactivity and morphological structures: visualisation of dendritic cells in peripheral organs. J. Clin. Pathol. 53:518-524.
31. Porgador, A., H. F. Staats, Y. Itoh, and B. L. Kelsall. 1998. Intranasal immunization with cytotoxic T-lymphocyte epitope peptide and mucosal adjuvant cholera toxin: selective augmentation of peptide-presenting dendritic cells in nasal mucosa-associated lymphoid tissue. Infect. Immun. 66: 5876-5881.
32. Randolph, G. J., K. Inaba, D. F. Robbiani, R. M. Steinman, and W. A. Muller. 1999. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11:753-761.
33. Rao, A. S., J. A. Roake, C. P. Larsen, D. F. Hankins, P. J. Morris, and J. M. Austyn. 1993. Isolation of dendritic leukocytes from non-lymphoid organs. Adv. Exp. Med. Biol. 329:507-512.
34. Sekiya, K., M. Kawahira, and Y. Nakase. 1983. Protection against experimental Bordetella bronchiseptica infection in mice by active immunization with killed vaccine. Infect. Immun. 41:598-603.
35. Sertl, K., T. Takemura, E. Tschachler, V. J. Ferrans, M. A. Kaliner, and E. M. Shevach. 1986. Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J. Exp. Med. 163:436-451.
36. Steinman, R. M., and M. C. Nussenzweig. 1980. Dendritic cells: features and functions. Immunol. Rev. 53:127-147.
37. Steinman, R. M., M. Pack, and K. Inaba. 1997. Dendritic cell development and maturation. Adv. Exp. Med. Biol. 417:1-6.
38. Stockwin, L. H., D. McGonagle, I. G. Martin, and G. E. Blair. 2000. Dendritic cells: immunological sentinels with a central role in health and disease. Immunol. Cell Biol. 78:91-102.
39. Wiley, J. A., R. J. Hoggan, D. L. Woodland, and A. G. Harmsen. 2001. Antigen-specific CD8(+) T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167:3293-3299.
40. Woolfrey, B. F., and J. A. Moody. 1991. Human infections associated with Bordetella bronchiseptica. J. Clin. Microbiol. Rev. 4:243-255.
41. Yuk, M. H., E. T. Harvill, P. A. Cotter, and J. F. Miller. 2000. Modulation of host immune responses, induction of apoptosis and inhibition of NF-κB activation by the Bordetella type III secretion system. Mol. Microbiol. 35:991-1004.
42. Zuercher, A. W., S. E. Coffin, M. C. Thurnheer, P. Fundova, and J. J. Cebra. 2002. Nasal-associated lymphoid tissue is a mucosal inductive site for virus-specific humoral and cellular immune responses. J. Immunol. 168:1796-1803.