Multiple MyD88-dependent responses contribute to pulmonary clearance of Legionella pneumophila

Cellular Microbiology

Volumn 11, Issue 1, 2009, Pages 21-36

  Archer, Kristina A ^a   Alexopoulou, Lena ^b   Flavell, Richard A ^c   Roy, Craig R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 18 RECEPTOR; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; IMMUNE RESPONSE; INFECTION RISK; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MICROBIAL ACTIVITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RISK ASSESSMENT; SIGNAL TRANSDUCTION;

ANIMALS; COLONY COUNT, MICROBIAL; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LEGIONELLA PNEUMOPHILA; LUNG; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; RECEPTORS, INTERLEUKIN-18; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 5; TOLL-LIKE RECEPTOR 9;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; MUS;

EID: 58149295583     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01234.x     Document Type: Article

References (61)

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. Akamine, M., Higa, F., Arakaki, N., Kawakami, K., Takeda, K., Akira, S., and Saito, A. (2005) Differential roles of Toll-like receptors 2 and 4 in in vitro responses of macrophages to Legionella pneumophila. Infect Immun 73: 352-361.
3. Amer, A., Franchi, L., Kanneganti, T.D., Body-Malapel, M., Ozoren, N., Brady, G., et al. (2006) Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J Biol Chem 281: 35217-35223.
4. Archer, K.A., and Roy, C.R. (2006) MyD88-dependent responses involving toll-like receptor 2 are important for protection and clearance of Legionella pneumophila in a mouse model of Legionnaires' disease. Infect Immun 74: 3325-3333.
5. Bafica, A., Scanga, C.A., Feng, C.G., Leifer, C., Cheever, A., and Sher, A. (2005) TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 202: 1715-1724.
6. Bhan, U., Trujillo, G., Lyn-Kew, K., Newstead, M.W., Zeng, X., Hogaboam, C.M., et al. (2008) Toll-like receptor 9 regulates the lung macrophage phenotype and host immunity in murine pneumonia caused by Legionella pneumophila. Infect Immun 76: 2895-2904.
7. Bhardwaj, N., Nash, T.W., and Horwitz, M.A. (1986) Interferon-gamma-activated human monocytes inhibit the intracellular multiplication of Legionella pneumophila. J Immunol 137: 2662-2669.
8. Blander, J.M., and Medzhitov, R. (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304: 1014-1018.
9. Brieland, J., Freeman, P., Kunkel, R., Chrisp, C., Hurley, M., Fantone, J., and Engleberg, C. (1994) Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human Legionnaires' disease. Am J Pathol 145: 1537-1546.
10. Brieland, J.K., Remick, D.G., Freeman, P.T., Hurley, M.C., Fantone, J.C., and Engleberg, N.C. (1995) In vivo regulation of replicative Legionella pneumophila lung infection by endogenous tumor necrosis factor alpha and nitric oxide. Infect Immun 63: 3253-3258.
11. Brieland, J.K., Remick, D.G., LeGendre, M.L., Engleberg, N.C., and Fantone, J.C. (1998) In vivo regulation of replicative Legionella pneumophila lung infection by endogenous interleukin-12. Infect Immun 66: 65-69.
12. Brieland, J.K., Jackson, C., Hurst, S., Loebenberg, D., Muchamuel, T., Debets, R., et al. (2000) Immunomodulatory role of endogenous interleukin-18 in gamma interferon-mediated resolution of replicative Legionella pneumophila lung infection. Infect Immun 68: 6567-6573.
13. Carding, S.R., and Egan, P.J. (2002) Gammadelta T cells: Functional plasticity and heterogeneity. Nat Rev Immunol 2: 336-345.
14. Derre, I., and Isberg, R.R. (2004) Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 72: 3048-3053.
15. Edelstein, P.H., and Edelstein, M.A. (1989) WIN 57273 is bactericidal for Legionella pneumophila grown in alveolar macrophages. Antimicrob Agents Chemother 33: 2132-2136.
16. Feeley, J.C., Gibson, R.J., Gorman, G.W., Langford, N.C., Rasheed, J.K., Mackel, D.C., and Baine, W.B. (1979) Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J Clin Microbiol 10: 437-441.
17. Feuillet, V., Medjane, S., Mondor, I., Demaria, O., Pagni, P.P., Galan, J.E., et al. (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci USA 103: 12487-12492.
18. Fields, B.S. (1996) The molecular ecology of Legionellae. Trends Microbiol 4: 286-290.
19. Fraser, D.W., Tsai, T.R., Orenstin, W., Parken, W.E., Beechan, H.J., Sharrar, R.G., et al. (1977) Legionnaires' disease: Description of an epidemic of pneumonia. N Engl J Med 297: 1189-1197.
20. Girard, R., Pedron, T., Uematsu, S., Balloy, V., Chignard, M., Akira, S., and Chaby, R. (2002) Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J Cell Sci 116: 293-302.
21. Hawn, T.R., Verbon, A., Lettinga, K.D., Zhao, L.P., Li, S.S., Laws, R.J., etal. (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 198: 1563-1572.
22. Hawn, T.R., Smith, K.D., Aderem, A., and Skerrett, S.J. (2006) Myeloid differentiation primary response gene (88)- and toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J Infect Dis 193: 1693-1702.
23. Hawn, T.R., Berrington, W.R., Smith, I.A., Uematsu, S., Akira, S., Aderem, A., et al. (2007) Altered inflammatory responses in TLR5-deficient mice infected with Legionella pneumophila. J Immunol 179: 6981-6987.
24. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
25. 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.
26. Horwitz, M.A. (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
27. Horwitz, M.A., and Silverstein, S.C. (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiplies intracellularly in human monocytes. J Clin Invest 66: 441-450.
28. Janeway, C.A., Jr, and Medzhitov, R. (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
29. Kagan, J.C., and Roy, C.R. (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
30. Kagan, J.C., Stein, M.P., Pypaert, M., and Roy, C.R. (2004) Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 199: 1201-1211.
31. Kawai, T., Sato, S., Ishii, K.J., Coban, C., Hemmi, H., Yamamoto, M., et al. (2004) Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 5: 1061-1068.
32. Lauwerys, B.R., Garot, N., Renauld, J.C., and Houssiau, F.A. (2000) Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18. J Immunol 165: 1847-1853.
33. Lettinga, K.D., Florquin, S., Speelman, P., van Ketel, R., van der Poll, T., and Verbon, A. (2002) Toll-like receptor 4 is not involved in host defense against pulmonary Legionella pneumophila infection in a mouse model. J Infect Dis 186: 570-573.
34. Losick, V.P., and Isberg, R.R. (2006) NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J Exp Med 203: 2177-2189.
35. Luo, Z.Q., and Isberg, R.R. (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA 101: 841-846.
36. McDade, J.E., Shepard, C.C., Fraser, D.W., Tsai, T.R., Redus, M.A., and Dowdle, W.R. (1977) Legionnaires' disease: Isolation of a bacterium and demonstration of its role in other respiratory diseases. N Engl J Med 297: 1197-1203.
37. Marra, A., Blander, S.J., Horwitz, M.A., and Shuman, H.A. (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci USA 89: 9607-9611.
38. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C.A., Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
39. Molofsky, A.B., Byrne, B.G., Whitfield, N.N., Madigan, C.A., Fuse, E.T., Tateda, K., and Swanson, M.S. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
40. Nagai, H., Kagan, J.C., Zhu, X., Kahn, R.A., and Roy, C.R. (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
41. Nagarajan, N.A., and Kronenberg, M. (2007) Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J Immunol 178: 2706-2713.
42. Nakanishi, K., Yoshimoto, T., Tsutsui, H., and Okamura, H. (2001) Interleukin-18 regulates both Th1 and Th2 responses. Annu Rev Immunol 19: 423-474.
43. Nash, T.W., Libby, D.M., and Horwitz, M.A. (1988) IFN-gamma-activated human alveolar macrophages inhibit the intracellular multiplication of Legionella pneumophila. J Immunol 140: 3978-3981.
44. Neild, A.L., Shin, S., and Roy, C.R. (2005) Activated macrophages infected with Legionella inhibit T cells by means of MyD88-dependent production of prostaglandins. J Immunol 175: 8181-8190.
45. Newton, C.A., Perkins, I., Widen, R.H., Friedman, H., and Klein, T.W. (2007) Role of Toll-like receptor 9 in Legionella pneumophila -induced interleukin-12 p40 production in bone marrow-derived dendritic cells and macrophages from permissive and nonpermissive mice. Infect Immun 75: 146-151.
46. Reiner, S.L., and Locksley, R.M. (1995) The regulation of immunity to Leishmania major. Annu Rev Immunol 13: 151-177.
47. Ren, T., Zamboni, D.S., Roy, C.R., Dietrich, W.F., and Vance, R.E. (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: E18.
48. Roy, C.R., Berger, K.H., and Isberg, R.R. (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663-674.
49. Sadosky, A.B., Wiater, L.A., and Shuman, H.A. (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61: 5361-5373.
50. Segal, G., Purcell, M., and Shuman, H.A. (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA 95: 1669-1674.
51. Shinozawa, Y., Matsumoto, T., Uchida, K., Tsujimoto, S., Iwakura, Y., and Yamaguchi, K. (2002) Role of interferon-gamma in inflammatory responses in murine respiratory infection with Legionella pneumophila. J Med Microbiol 51: 225-230.
52. Skerrett, S.J., Bagby, G.J., Schmidt, R.A., and Nelson, S. (1997) Antibody-mediated depletion of tumor necrosis factor-alpha impairs pulmonary host defenses to Legionella pneumophila. J Infect Dis 176: 1019-1028.
53. Sporri, R., Joller, N., Albers, U., Hilbi, H., and Oxenius, A. (2006) MyD88-dependent IFN-gamma production by NK cells is key for control of Legionella pneumophila infection. J Immunol 176: 6162-6171.
54. Stober, D., Schirmbeck, R., and Reimann, J. (2001) IL-12/IL-18-dependent IFN-gamma release by murine dendritic cells. J Immunol 167: 957-965.
55. Swanson, M.S., and Isberg, R.R. (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
56. Takeuchi, O., Hoshino, K., Kawai, T., Sanjo, H., Takada, H., Ogawa, T., etal. (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11: 443-451.
57. Vogel, J.P., Andrews, H.L., Wong, S.K., and Isberg, R.R. (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
58. Yarovinsky, F., Zhang, D., Andersen, J.F., Bannenberg, G.L., Serhan, C.N., Hayden, M.S., et al. (2005) TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308: 1626-1629.
59. Zamboni, D.S., Kobayashi, K.S., Kohlsdorf, T., Ogura, Y., Long, E.M., Vance, R.E., et al. (2006) The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 7: 318-325.
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.
61. Zhang, T., Kawakami, K., Qureshi, M.H., Okamura, H., Kurimoto, M., and Saito, A. (1997) Interleukin-12 (IL-12) and IL-18 synergistically induce the fungicidal activity of murine peritoneal exudate cells against Cryptococcus neoformans through production of gamma interferon by natural killer cells. Infect Immun 65: 3594-3599.