Murine splenocytes produce inflammatory cytokines in a MyD88-dependent response to Bacillus anthracis spores

Cellular Microbiology

Volumn 9, Issue 2, 2007, Pages 502-513

  Glomski, Ian J ^a,b   Fritz, Jörg H ^a   Keppler, Selina J ^a,b   Balloy, Viviane ^a,c   Chignard, Michel ^a,c   Mock, Michèle ^a,b   Goossens, Pierre L ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; ANTHRAX TOXIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD11B ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; MYELOID DIFFERENTIATION FACTOR 88; PARAFORMALDEHYDE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANTHRAX; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL SPORE; BACTERIAL VIRULENCE; CELL ACTIVATION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; GENETIC TRANSFECTION; GRAM POSITIVE BACTERIUM; HOST CELL; HUMAN; HUMAN CELL; INFECTION RESISTANCE; INNATE IMMUNITY; MOLECULAR RECOGNITION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SPLEEN CELL; SPORE GERMINATION; SPOROGENESIS;

ANIMALS; BACILLUS ANTHRACIS; CELL LINE; CYTOKINES; HUMANS; MICE; MYELOID DIFFERENTIATION FACTOR 88; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SPLEEN; SPORES, BACTERIAL;

BACILLI (CLASS); BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); MURINAE; POSIBACTERIA;

EID: 33846249228     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00806.x     Document Type: Article

References (60)

1. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., et.al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
2. Agrawal, A., Lingappa, J., Leppla, S.H., Agrawal, S., Jabbar, A., Quinn, C., and Pulendran, B. (2003) Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424: 329-334.
3. Ahmad-Nejad, P., Hacker, H., Rutz, M., Bauer, S., Vabulas, R.M., and Wagner, H. (2002) Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur J Immunol 32: 1958-1968.
4. Balloy, V., Si-Tahar, M., Takeuchi, O., Philippe, B., Nahori, M.A., Tanguy, M., et.al. (2005) Involvement of toll-like receptor 2 in experimental invasive pulmonary aspergillosis. Infect Immun 73: 5420-5425.
5. Brossier, F., Weber-Levy, M., Mock, M., and Sirard, J.C. (2000) Role of toxin functional domains in anthrax pathogenesis. Infect Immun 68: 1781-1786.
6. Brossier, F., Levy, M., and Mock, M. (2002) Anthrax spores make an essential contribution to vaccine efficacy. Infect Immun 70: 661-664.
7. Chamaillard, M., Hashimoto, M., Horie, Y., Masumoto, J., Qiu, S., Saab, L., et.al. (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4: 702-707.
8. Cote, C.K., Rea, K.M., Norris, S.L., van Rooijen, N., and Welkos, S.L. (2004) The use of a model of in vivo macrophage depletion to study the role of macrophages during infection with Bacillus anthracis spores. Microb Pathog 37: 169-175.
9. D'Andrea, A., Rengaraju, M., Valiante, N.M., Chehimi, J., Kubin, M., Aste, M., et.al. (1992) Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J Exp Med 176: 1387-1398.
10. Erwin, J.L., DaSilva, L.M., Bavari, S., Little, S.F., Friedlander, A.M., and Chanh, T.C. (2001) Macrophage-derived cell lines do not express proinflammatory cytokines after exposure to Bacillus anthracis lethal toxin. Infect Immun 69: 1175-1177.
11. Gimenez, A.P., Wu, Y.Z., Paya, M., Delclaux, C., Touqui, L., and Goossens, P.L. (2004) High bactericidal efficiency of type iia phospholipase A2 against Bacillus anthracis and inhibition of its secretion by the lethal toxin. J Immunol 173: 521-530.
12. Girardin, S.E., Boneca, I.G., Viala, J., Chamaillard, M., Labigne, A., Thomas, G., et.al. (2003a) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872.
13. Girardin, S.E., Travassos, L.H., Herve, M., Blanot, D., Boneca, I.G., Philpott, D.J., et.al. (2003b) Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 278: 41702-41708.
14. Gold, J.A., Hoshino, Y., Hoshino, S., Jones, M.B., Nolan, A., and Weiden, M.D. (2004) Exogenous gamma and alpha/beta interferon rescues human macrophages from cell death induced by Bacillus anthracis. Infect Immun 72: 1291-1297.
15. Goossens, P.L., Jouin, H., and Milon, G. (1991) Dynamics of lymphocytes and inflammatory cells recruited in liver during murine listeriosis. A cytofluorimetric study. J Immunol 147: 3514-3520.
16. Green, B.D., Battisti, L., Koehler, T.M., Thorne, C.B., and Ivins, B.E. (1985) Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49: 291-297.
17. Guidi-Rontani, C., Weber-Levy, M., Labruyere, E., and Mock, M. (1999) Germination of Bacillus anthracis spores within alveolar macrophages. Mol Microbiol 31: 9-17.
18. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., et.al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
19. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, T., Takeda, Y., et.al. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J Immunol 162: 3749-3752.
20. Hughes, M.A., Green, C.S., Lowchyj, L., Lee, G.M., Grippe, V.K., Smith, M.F., Jr, et.al. (2005) MyD88-dependent signaling contributes to protection following Bacillus anthracis spore challenge of mice: implications for toll-like receptor signaling. Infect Immun 73: 7535-7540.
21. Kang, T.J., Fenton, M.J., Weiner, M.A., Hibbs, S., Basu, S., Baillie, L., and Cross, A.S. (2005) Murine macrophages kill the vegetative form of Bacillus anthracis. Infect Immun 73: 7495-7501.
22. Kawai, T., and Akira, S. (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131-137.
23. Kobayashi, M., Fitz, L., Ryan, M., Hewick, R.M., Clark, S.C., Chan, S., et.al. (1989) Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 170: 827-845.
24. Kufer, T.A., Fritz, J.H., and Philpott, D.J. (2005) NACHT-LRR proteins (NLRs) in bacterial infection and immunity. Trends Microbiol 13: 381-388.
25. Kufer, T.A., Kremmer, E., Banks, D.J., and Philpott, D.J. (2006) Role for erbin in bacterial activation of Nod2. Infect Immun 74: 3115-3124.
26. Lincoln, R.E., Hodges, D.R., Klein, F., Mahlandt, B.G., Jones, W.I., Jr, Haines, B.W., et.al. (1965) Role of the lymphatics in the pathogenesis of anthrax. J Infect Dis 115: 481-494.
27. Magalhaes, J.G., Philpott, D.J., Nahori, M.A., Jehanno, M., Fritz, J., Bourhis, L.L., et.al. (2005) Murine Nod1 but not its human orthologue mediates innate immune detection of tracheal cytotoxin. EMBO Rep 6: 1201-1207.
28. Makino, S., Uchida, I., Terakado, N., Sasakawa, C., and Yoshikawa, M. (1989) Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J Bacteriol 171: 722-730.
29. Middleton, M.K., Rubinstein, T., and Pure, E. (2006) Cellular and molecular mechanisms of the selective regulation of IL-12 production by 12/15-lipoxygenase. J Immunol 176: 265-274.
30. Mishell, B.B., and Shiigi, S.M. (1980) Selected Methods in Cellular Immunology. San Francisco: W.H. Freeman and Co., pp. 23-24.
31. Mock, M., and Fouet, A. (2001) Anthrax. Annu Rev Microbiol 55: 647-671.
32. Nahori, M.A., Fournie-Amazouz, E., Que-Gewirth, N.S., Balloy, V., Chignard, M., Raetz, C.R., et.al. (2005) Differential TLR recognition of leptospiral lipid A and lipopolysaccharide in murine and human cells. J Immunol 175: 6022-6031.
33. Nakashio, S., and Gerhardt, P. (1985) Protoplast dehydration correlated with heat resistance of bacterial spores. J Bacteriol 162: 571-578.
34. Neurath, M.F., Fuss, I., Kelsall, B., Meyer zum Buschenfelde, K.H., and Strober, W. (1996) Effect of IL-12 and antibodies to IL-12 on established granulomatous colitis in mice. Ann N Y Acad Sci 795: 368-370.
35. O'Neill, L.A. (2004) Immunology. After the toll rush. Science 303: 1481-1482.
36. Ozinsky, A., Underhill, D.M., Fontenot, J.D., Hajjar, A.M., Smith, K.D., Wilson, C.B., et.al. (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 97: 13766-13771.
37. Paccani, S.R., Tonello, F., Ghittoni, R., Natale, M., Muraro, L., D'Elios, M.M., et.al. (2005) Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signaling. J Exp Med 201: 325-331.
38. Park, J.M., Greten, F.R., Li, Z.W., and Karin, M. (2002) Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051.
39. Park, J.M., Ng, V.H., Maeda, S., Rest, R.F., and Karin, M. (2004) Anthrolysin O and other Gram-positive cytolysins are toll-like receptor 4 agonists. J Exp Med 200: 1647-1655.
40. Pellizzari, R., Guidi-Rontani, C., Vitale, G., Mock, M., and Montecucco, C. (1999) Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNgamma-induced release of NO and TNFalpha. FEBS Lett 462: 199-204.
41. Pezard, C., Duflot, E., and Mock, M. (1993) Construction of Bacillus anthracis mutant strains producing a single toxin component. J Gen Microbiol 139: 2459-2463.
42. Philpott, D.J., and Girardin, S.E. (2004) The role of Toll-like receptors and Nod proteins in bacterial infection. Mol Immunol 41: 1099-1108.
43. Pickering, A.K., Osorio, M., Lee, G.M., Grippe, V.K., Bray, M., and Merkel, T.J. (2004) Cytokine response to infection with Bacillus anthracis spores. Infect Immun 72: 6382-6389.
44. Piris-Gimenez, A., Paya, M., Lambeau, G., Chignard, M., Mock, M., Touqui, L., and Goossens, P.L. (2005) In vivo protective role of human group IIA phospholipase A2 against experimental anthrax. J Immunol 175: 6786-6791.
45. Popov, S.G., Popova, T.G., Grene, E., Klotz, F., Cardwell, J., Bradburne, C., et.al. (2004) Systemic cytokine response in murine anthrax. Cell Microbiol 6: 225-233.
46. Portnoy, D.A., Jacks, P.S., and Hinrichs, D.J. (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
47. Ramphal, R., Balloy, V., Huerre, M., Si-Tahar, M., and Chignard, M. (2005) TLRs 2 and 4 are not involved in hypersusceptibility to acute Pseudomonas aeruginosa lung infections. J Immunol 175: 3927-3934.
48. Rasko, D.A., Ravel, J., Okstad, O.A., Helgason, E., Cer, R.Z., Jiang, L., et.al. (2004) The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32: 977-988.
49. Ross, J.M. (1957) The pathogenesis of anthrax following the administration of spores by the respiratory route. J Pathol Bacteriol 73: 485-494.
50. Setlow, P. (1994) Mechanisms which contribute to the long-term survival of spores of Bacillus species. Soc Appl Bacteriol Symp Ser 23: 49S-60S.
51. Skeen, M.J., and Ziegler, H.K. (1995) Activation of gamma delta T cells for production of IFN-gamma is mediated by bacteria via macrophage-derived cytokines IL-1 and IL-12. J Immunol 154: 5832-5841.
52. Skeen, M.J., Miller, M.A., Shinnick, T.M., and Ziegler, H.K. (1996) Regulation of murine macrophage IL-12 production. Activation of macrophages in vivo, restimulation in vitro, and modulation by other cytokines. J Immunol 156: 1196-1206.
53. Sylvestre, P., Couture-Tosi, E., and Mock, M. (2005) Contribution of ExsFA and ExsFB proteins to the localization of BclA on the spore surface and to the stability of the Bacillus anthracis exosporium. J Bacteriol 187: 5122-5128.
54. Takeda, K., Kaisho, T., and Akira, S. (2003) Toll-like receptors. Annu Rev Immunol 21: 335-376.
55. Takeuchi, O., Hoshino, K., Kawai, T., Sanjo, H., Takada, H., Ogawa, T., et.al. (1999) Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11: 443-451.
56. Tournier, J.N., Quesnel-Hellmann, A., Mathieu, J., Montecucco, C., Tang, W.J., Mock, M., et.al. (2005) Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J Immunol 174: 4934-4941.
57. Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3: 133-146.
58. Welkos, S.L., Keener, T.J., and Gibbs, P.H. (1986) Differences in susceptibility of inbred mice to Bacillus anthracis. Infect Immun 51: 795-800.
59. Xu, D., and Cote, J.C. (2003) Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3′ end 16S rDNA and 5′ end 16S-23S ITS nucleotide sequences. Int J Syst Evol Microbiol 53: 695-704.
60. Zhang, D., Zhang, G., Hayden, M.S., Greenblatt, M.B., Bussey, C., Flavell, R.A., and Ghosh, S. (2004) A toll-like receptor that prevents infection by uropathogenic bacteria. Science 303: 1522-1526.