Immune control of Legionella infection: An in vivo perspective

Frontiers in Microbiology

Volumn 2, Issue JUNE, 2011, Pages

  Schuelein, Ralf ^a   Ang, Desmond K Y ^b   van Driel, Ian R ^b   Hartland, Elizabeth L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cytokines; Inflammation; Legionnaire's disease; Macrophages; Plasmacytoid dendritic cells

Indexed keywords

EID: 84869870920     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00126     Document Type: Article

References (78)

1. Abdelaziz, D. H., Gavrilin, M. A., Akhter, A., Caution, K., Kotrange, S., Khweek, A. A., Abdulrahman, B.A., Grandhi, J., Hassan, Z. A., Marsh, C.,Wewers, M. D., and Amer, A. O. (2011). Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J. Biol. Chetn. 286, 3203-3208.
2. Abu-Zant, A., Jones, S., Asare, R., Suttles, J., Price, C, Graham, J., and Kwaik,Y. A. (2007). Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell. Microbiol. 9, 246-264.
3. Abu-Zant, A., Santic, M., Molmeret, M., Jones, S., Helbig, J., and Abu Kwaik, Y. (2005). Incomplete activation of macrophage apoptosis during intra-cellular replication of Legionella pneumophila. Infect. Immun. 73, 5339-5349.
4. Akhter, A., Gavrilin, M. A., Frantz, L., Washington, S., Ditty, C, Limoli, D., Day, C, Sarkar, A., Newland, C,Butchar, J., Marsh, C. B., Wew-ers, M. D., Tridandapani, S., Kan-neganti, T. D., and Amer, A. O. (2009). Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 5, el000361. doi:10.1371/joumal.ppat.l000361
5. Amer, A., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Ozoren, N., Brady, G., Meshinchi, S., Jagir-dar, R., Gewirtz, A., Akira, S., and Nunez, G. (2006). Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281, 35217-35223.
6. Ang, D. K., Oates, C. V., Schuelein, R., Kelly, M., Sansom, F. M., Bourges, D., Boon, L., Hertzog, P. J., Hartland, E. L., and Van Driel, I. R. (2010). Cutting edge: pulmonary Legionella pneumophila is controlled by plasmacytoid dendritic cells but not type I IFN. J. Immunol. 184, 5429-5433.
7. Archer, K. A., Alexopoulou, L., Flavell, R. A., and Roy, C. R. (2009). Multiple MyD88-dependent responses contribute to pulmonary clearance of Legionella pneumophila. Cell. Microbiol. 11,21-36.
8. Banga, S., Gao, P., Shen, X., Fiscus, V., Zong, W. X., Chen, L., and Luo, Z. Q. (2007). Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc. Natl. Acad. Sci. U.S.A. 104,5121-5126.
9. Bartfeld, S., Engels, C, Bauer, B., Aurass, P., Flieger, A., Bruggemann, H., and Meyer, T. F. (2009). Temporal resolution of two-tracked NF-kappaB activation by Legionella pneumophila. Cell. Microbiol. 11, 1638-1651.
10. Beckers, M. C, Yoshida, S., Morgan, K., Skamene, E., and Gros, P. (1995). Natural resistance to infection with Legionella pneumophila: chromosomal localization of the Lgnl susceptibility gene. Mamm. Genome 6, 540-545.
11. Brieland, J. K., Remick, D. G., Legendre, M. L., Engleberg, N. C, and Fan-tone, J. C. (1998). In vivo regulation of replicative Legionella pneumophila lung infection by endogenous interleukin-12. Infect. Immun. 66, 65-69.
12. Case, C. L., Shin, S., and Roy, C. R. (2009). Asc and Ipaf Inflam-masomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 77,1981-1991.
13. Chandler, F. W., Hicklin, M. D., and Blackmon, J. A. (1977). Demonstration of the agent of Legionnaires' disease in tissue. N. Engl. J. Med. 297, 1218-1220.
14. Coers, J., Vance, R. E., Fontana, M. F., and Dietrich, W. F. (2007). Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell. Microbiol. 9, 2344-2357.
15. Colonna, M., Trinchieri, G., and Liu, Y. J. (2004). Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5, 1219-1226.
16. Davis, B. K., Wen, H., and Ting, J. P. (2011). The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707-735.
17. Dietrich, W. E, Damron, D. M., Isberg, R. R., Lander, E. S., and Swanson, M. S. (1995). Lgnl, a gene that determines susceptibility to Legionella pneumophila, maps to mouse chromosome 13. Genomics 26, 443-450.
18. Diez, E.,Lee, S. H., Gauthier, S., Yaraghi, Z., Tremblay, M., Vidal, S., and Gros, P. (2003). Bircle is the gene within the Lgnl locus associated with resistance to Legionella pneumophila. Nat. Genet. 33, 55-60.
19. Fields, B. S. (1996). The molecular ecology of legionellae. Trends Microbiol. 4,286-290.
20. Fitzgerald-Bocarsly, P., Dai, J., and Singh, S. (2008). Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev. 19,3-19.
21. Fortier, A., Doiron, K., Saleh, M., Grin-stein, S., and Gros, P. (2009). Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irfl and Irf8 and NOD-like receptors Naip5 and Nlrc4. Infect. Immun. 77,4794-4805.
22. Franco, I. S., Shuman, H. A., and Char-pentier, X. (2009). The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell. Microbiol. 11, 1435-1443.
23. Fraser, D. W., Tsai, T. R., Orenstein, W, Parkin, W E., Beecham, H. J., Shar-rar, R. G., Harris, J., Mallison, G. F., Martin, S. M., Mcdade, J. E., Shepard, C. C, and Brachman, P. S. (1977). Legionnaires' disease: description of an epidemic of pneumonia. N Engl. J.Med. 297, 1189-1197.
24. Fujita, M., Ikegame, S., Harada, E., Ouchi, H., Inoshima, L, Watanabe, K., Yoshida, S., and Nakanishi, Y. (2008). TNF receptor 1 and 2 contribute in different ways to resistance to Legionella pneumophila-induced mortality in mice. Cytokine 44,298-303.
25. Furugen, M., Higa, E, Hibiya, K., Teruya, H., Akamine, M., Haranaga, S., Yara, S., Koide, M., Tateyama, M., Mori, N., and Fujita, J. (2008). Legionella pneuniophila infection induces programmed cell death, caspase activation, and release of high-mobility group box 1 protein in A549 alveolar epithelial cells: inhibition by methyl prednisolone. Respir. Res. 9, 39.
26. Gao, L. Y., and Abu Kwaik, Y. (1999). Activation of caspase 3 during Legionella pneumophila-induced apoptosis. Infect. Itntnun. 67, 4886-4894.
27. Glavin, F. L., Winn, W. C, Jr., and Craig-head, 1. E. (1979). Ultrastructure of lung in Legionnaires' disease. Observations of three biopsies done during the Vermont epidemic. Ann. Intern. Med. 90, 555-559.
28. Hagele, S., Hacker, J., and Brand, B. C. (1998). Legionella pneuniophila kills human phagocytes but not protozoan host cells by inducing apoptotic cell death. FEMSMicrobiol. Lett. 169, 51-58.
29. Heath, W. R., and Carbone, E R. (2009). Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10, 1237-1244.
30. Hernandez, E J., Kirby, B. D., Stanley, T. M., and Edelstein, P. H. (1980). Legionnaires' disease. Postmortem pathologic findings of 20 cases. Am. J. Clin. Pathol. 73, 488-495.
31. Horwitz, M. A. (1983a). Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158, 1319-1331.
32. Horwitz, M. A. (1983b). The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158, 2108-2126.
33. Horwitz, M. A., and Silverstein, S. C. (1980). Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J. Clin. Invest. 66, 441-450.
34. Hubber, A., and Roy, C. R. (2010). Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol 26,261-283.
35. Isberg, R. R., O'Connor, T. J., and Hei-dtman, M. (2009). The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7,13-24.
36. Janeway, C. A., Jr. (1992). The immune system evolved to discriminate infectious nonself from noninfec-tiousself. Immunol. Today 13,11-16.
37. Joller, N., Sporri, R., Hilbi, H., and Oxenius, A. (2007). Induction and protective role of antibodies in Legionella pneumophila infection. Eur.J. Immunol. 37, 3414-3423.
38. Kagan, J. C, and Roy, C. R. (2002). Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4, 945-954.
39. Kikuchi, T., Andarini, S., Xin, H., Gomi, K., Tokue, Y, Saijo, Y, Honjo, T., Watanabe, A., and Nukiwa, T. (2005). Involvement of fractalkine/CX3CLl expression by dendritic cells in the enhancement of host immunity against Legionella pneumophila. Infect. Immun. 73, 5350-5357.
40. Laguna, R. K., Creasey, E. A., Li, Z., Valtz, N., and Isberg, R. R. (2006). A Legionella pneu-mophila-tmnslocated substrate that is required for growth within macrophages and protection from host cell death. Proc. Natl. Acad. Sci. U.S.A 103, 18745-18750.
41. Lamkanfi, M., Amer, A., Kanneganti, T. D., Munoz-Planillo, R., Chen, G., Vandenabeele, P., Fortier, A., Gros, P., and Nunez, G. (2007). The NOD-like receptor family member Naip5/Bircle restricts Legionella pneumophila growth independently of caspase-1 activation. J. Immunol. 178, 8022-8027.
42. LeibundGut-Landmann, S., Weidner, K., Hilbi, H., and Oxenius, A. (2011). Nonhematopoietic cells are key players in innate control of bacterial airway infection. J. Immunol. 186, 3130-3137.
43. Lightfield, K. L., Persson, J., Brubaker, S. W., Witte, C. E., Von Moltke, J., Dunipace, E. A., Henry, T., Sun, Y H., Cado, D., Dietrich, W. E, Monack, D. M., Tsolis, R. M., and Vance, R. E. (2008). Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9, 1171-1178.
44. 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.
45. Luhrmann, A., Nogueira, C. V, Carey, K. L., and Roy, C. R. (2010). Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc. Natl. Acad. Sci. U.S.A. 107, 18997-19001.
46. Matsunaga, K., Klein, T. W., Newton, C, Friedman, H., and Yamamoto, Y (2001). Legionella pneumophila suppresses interleukin-12 production by macrophages. Infect. Immun. 69, 1929-1933.
47. Matsunaga, K., Yamaguchi, H., Klein, T. W., Friedman, H., and Yamamoto, Y. (2003). Legionella pneumophila suppresses macrophage interleukin-12 production by activating the p42/44 mitogen-activated protein kinase cascade. Infect. Immun. 71, 6672-6675.
48. McCoy-Simandle, K., Stewart, C. R., Dao, J., Debroy, S., Rossier, O., Bryce, P. J., and Cianciotto, N. P. (2011). Legionella pneumophila type II secretion dampens the cytokine response of infected macrophages and epithelia. Infect. Immun. 79, 1984-1997.
49. 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 disease. N. Engl. J. Med. 297,1197-1203.
50. Miao, E. A., Leaf, I. A., Treuting, P. M., Mao, D. P., Dors, M., Sarkar, A., Warren, S. E., Wewers, M. D., and Aderem, A. (2010). Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11,1136-1142.
51. Molmeret, M., Zink, S. D., Han, L., Abu-Zant, A., Asari, R., Bitar, D. M., and Abu Kwaik, Y (2004). Activation of caspase-3 by the Dot/Icm virulence system is essential for arrested biogenesis of the Legionella-containing phagosome. Cell. Microbiol. 6, 33-48.
52. Molofsky, A. B., Byrne, B. G., Whit-field, N. N., Madigan, C. A., Fuse, E T., Tateda, K., and Swanson, M. S. (2006). Cytosolic recog nition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203,1093-1104.
53. Monroe, K. M., Mcwhirter, S. M., and Vance, R. E. (2009). Identification of host cytosolic sensors and bacterial factors regulating the type I inter-feron response to Legionella pneumophila. PLoS Pathog 5, el000665. doi:10.1371/journal.ppat.l000665
54. Neild, A. L, and Roy, C. R. (2003). Legionella reveal dendritic cell functions that facilitate selection of antigens for MHC class II presentation. Immunity 18,813-823.
55. Newton, H. J., Ang, D. K., Van Driel, I. R., and Hartland, E. L. (2010). Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev. 23, 274-298.
56. Nogueira, C. V, Lindsten, T., Jamieson, A. M., Case, C. L., Shin, S., Thompson, C. B., and Roy, C. R. (2009). Rapid pathogen-induced apoptosis: a mechanism used by dendritic cells to limit intracellular replication of Legionella pneumophila. PLoS Pathog. 5, el000478. doi:10.1371/journal.ppat.l000478
57. Plumlee, C. R., Lee, C, Beg, A. A., Decker, T., Shuman, H. A., and Schindler, C. (2009). Interferons direct an effective innate response to Legionella pneumophila infection. J. Biol. Chem. 284, 30058-30066.
58. Ren, T., Zamboni, D. S., Roy, C. R., Dietrich, W E, and Vance, R. E. (2006). Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2, el8. doi:10.1371/journal.ppat.0020018
59. Rowbotham, T. J. (1980). Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33,1179-1183.
60. Roy, C. R., and Tilney, L. G. (2002). The road less traveled: transport of Legionella to the endoplasmic reticulum. J. Cell Biol. 158, 415-419.
61. Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821-832.
62. 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. U.S.A. 95, 1669-1674.
63. Segal, G., and Shuman, H. A. (1997). Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect. Immun. 65, 5057-5066.
64. Shin, S., Case, C. L., Archer, K. A., Nogueira, C. V, Kobayashi, K. S., Flavell, R. A., Roy, C. R., and Zamboni, D. S. (2008). Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog. 4, el000220. doi:10.1371/journal.ppat.l000220
65. 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.
66. Silveira, T. N., and Zamboni, D. S. (2010). Pore formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect. Immun. 78,1403-1413.
67. Sporri, R., Joller, N., Hilbi, H., and Oxenius, A. (2008). A novel role for neutrophils as critical activators of NK cells. J. Immunol 181, 7121-7130.
68. Susa, M., Ticac, B., Rukavina, T., Doric, M., and Marre, R. (1998). Legionella pneumophila infection in intratra-cheally inoculated T cell-depleted or -nondepleted A/J mice. J. Immunol 160,316-321.
69. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820.
70. Tyndall, R. L., and Domingue, E. L. (1982). Cocultivation of Legionella pneumophila and free-living amoebae. Appl. Environ. Microbiol AA, 954-959.
71. Vinzing, M., Eitel, J., Lippmann, J., Hocke, A. C, Zahlten, J., Slevogt, H., N'Guessan P, D., Gunther, S., Schmeck, B., Hippenstiel, S., Flieger, A., Suttorp, N., and Opitz, B. (2008). NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 180, 6808-6815.
72. Vogel, J. P., Andrews, H. L, Wong, S. K., andIsberg,R.R. (1998). Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873-876.
73. Weber, S. S., Ragaz, C, and Hilbi, H. (2009). Pathogen trafficking pathways and host phosphoinositide metabolism. Mol Microbiol. 71, 1341-1352.
74. Winn, W. C, Jr. (1988). Legionnaires disease: historical perspective. Clin. Microbiol Rev. 1,60-81.
75. Wright, E. K., Goodart, S. A., Growney, J. D., Hadinoto, V., Endrizzi, M. G., Long, E. M., Sadigh, K., Abney, A. L., Bernstein-Hanley, I., and Dietrich, W. F. (2003). Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr.Biol 13,27-36.
76. Yamamoto, Y., Klein, T. W, Newton, C. A., Widen, R., and Friedman, H. (1988). Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect. Immun. 56, 370-375.
77. Zamboni, D. S., Kobayashi, K. S., Kohls-dorf, T., Ogura, Y, Long, E. M., Vance, R. E., Kuida, K., Mariathasan, S., Dixit, V. M., Flavell, R. A., Dietrich, W E, and Roy, C. R. (2006). The Bircle cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7, 318-325.
78. Zhu, W., Banga, S., Tan, Y., Zheng, C, Stephenson, R., Gately, J., and Luo, Z. Q. (2011). Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE, 6, el7638. doi:10.1371/jour-nal.pone.0017638