Innate Immunity to Intracellular Pathogens. Lessons Learned from Legionella pneumophila

Advances in Applied Microbiology

Volumn 79, Issue , 2012, Pages 43-71

  Shin, Sunny ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Endoplasmic reticulum; Legionella pneumophila; Nod like receptors; Pathogen associated molecular patterns; Pattern recognition receptors; Toll like receptors

Indexed keywords

CASPASE 3; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CRYOPYRIN; CXCL1 CHEMOKINE; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NAIP5 PROTEIN; NEURONAL APOPTOSIS INHIBITORY PROTEIN; NLRC4 PROTEIN; PROTEIN BAK; PROTEIN BAX; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOLOGICAL MODEL; CELL ORGANELLE; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOSOL; DENDRITIC CELL; ENZYME INACTIVATION; HUMAN; INNATE IMMUNITY; INTRACELLULAR BACTERIUM; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; LUNG ALVEOLUS MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTE; PHAGOSOME; PROTOZOON; SALMONELLA TYPHIMURIUM; METABOLISM; VIRULENCE;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; PROTOZOA;

BACTERIAL PROTEINS; IMMUNITY, INNATE; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; VIRULENCE;

EID: 84860557405     PISSN: 00652164     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394318-7.00003-6     Document Type: Chapter

References (128)

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., Amer A.O. Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J. Biol. Chem. 2011, 286:3203-3208.
2. Abdelaziz D.H., Gavrilin M.A., Akhter A., Caution K., Kotrange S., Khweek A.A., Abdulrahman B.A., Hassan Z.A., El-Sharkawi F.Z., Bedi S.S., Ladner K., Gonzalez-Mejia M.E., et al. Asc-dependent and independent mechanisms contribute to restriction of legionella pneumophila infection in murine macrophages. Front. Microbiol. 2011, 2:18.
3. Abu Kwaik Y. The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 1996, 62:2022-2028.
4. Abu-Zant A., Jones S., Asare R., Suttles J., Price C., Graham J., Kwaik Y.A. Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell. Microbiol. 2007, 9:246-264.
5. Akhter A., Gavrilin M.A., Frantz L., Washington S., Ditty C., Limoli D., Day C., Sarkar A., Newland C., Butchar J., Marsh C.B., Wewers M.D., et al. Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog. 2009, 5:e1000361.
6. Amer A.O., Swanson M.S. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell. Microbiol. 2005, 7:765-778.
7. Amer A., Franchi L., Kanneganti T.D., Body-Malapel M., Ozoren N., Brady G., Meshinchi S., Jagirdar R., Gewirtz A., Akira S., Nunez G. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 2006, 281:35217-35223.
8. Ang D.K., Oates C.V., Schuelein R., Kelly M., Sansom F.M., Bourges D., Boon L., Hertzog P.J., Hartland E.L., van Driel I.R. Cutting edge: Pulmonary Legionella pneumophila is controlled by plasmacytoid dendritic cells but not type I IFN. J. Immunol. 2010, 184:5429-5433.
9. Archer K.A., Roy C.R. 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. 2006, 74:3325-3333.
10. Archer K.A., Alexopoulou L., Flavell R.A., Roy C.R. Multiple MyD88-dependent responses contribute to pulmonary clearance of Legionella pneumophila. Cell. Microbiol. 2009, 11:21-36.
11. Archer K.A., Ader F., Kobayashi K.S., Flavell R.A., Roy C.R. Cooperation between multiple microbial pattern recognition systems is important for host protection against the intracellular pathogen Legionella pneumophila. Infect. Immun. 2010, 78:2477-2487.
12. Bartfeld S., Engels C., Bauer B., Aurass P., Flieger A., Bruggemann H., Meyer T.F. Temporal resolution of two-tracked NF-kappaB activation by Legionella pneumophila. Cell. Microbiol. 2009, 11:1638-1651.
13. Beckers M.C., Yoshida S., Morgan K., Skamene E., Gros P. Natural resistance to infection with Legionella pneumophila: Chromosomal localization of the Lgn1 susceptibility gene. Mamm. Genome 1995, 6:540-545.
14. Belyi Y., Niggeweg R., Opitz B., Vogelsgesang M., Hippenstiel S., Wilm M., Aktories K. Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc. Natl. Acad. Sci. USA 2006, 103:16953-16958.
15. Belyi Y., Tabakova I., Stahl M., Aktories K. Lgt: A family of cytotoxic glucosyltransferases produced by Legionella pneumophila. J. Bacteriol. 2008, 190:3026-3035.
16. Berger K.H., Isberg R.R. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 1993, 7:7-19.
17. Berrington W.R., Iyer R., Wells R.D., Smith K.D., Skerrett S.J., Hawn T.R. NOD1 and NOD2 regulation of pulmonary innate immunity to Legionella pneumophila. Eur. J. Immunol. 2010, 40:3519-3527.
18. Brieland J., Freeman P., Kunkel R., Chrisp C., Hurley M., Fantone J., Engleberg C. Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human Legionnaires' disease. Am. J. Pathol. 1994, 145:1537-1546.
19. Brieland J.K., Remick D.G., Freeman P.T., Hurley M.C., Fantone J.C., Engleberg N.C. In vivo regulation of replicative Legionella pneumophila lung infection by endogenous tumor necrosis factor alpha and nitric oxide. Infect. Immun. 1995, 63:3253-3258.
20. Brieland J.K., Remick D.G., LeGendre M.L., Engleberg N.C., Fantone J.C. In vivo regulation of replicative Legionella pneumophila lung infection by endogenous interleukin-12. Infect. Immun. 1998, 66:65-69.
21. Brieland J.K., Jackson C., Hurst S., Loebenberg D., Muchamuel T., Debets R., Kastelein R., Churakova T., Abrams J., Hare R., O'Garra A. Immunomodulatory role of endogenous interleukin-18 in gamma interferon-mediated resolution of replicative Legionella pneumophila lung infection. Infect. Immun. 2000, 68:6567-6573.
22. Broz P., von Moltke J., Jones J.W., Vance R.E., Monack D.M. Differential requirement for caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 2010, 8:471-483.
23. Burdette D.L., Monroe K.M., Sotelo-Troha K., Iwig J.S., Eckert B., Hyodo M., Hayakawa Y., Vance R.E. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011, 478:515-518.
24. Byrd T.F., Horwitz M.A. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Invest. 1989, 83:1457-1465.
25. Byrd T.F., Horwitz M.A. Lactoferrin inhibits or promotes Legionella pneumophila intracellular multiplication in nonactivated and interferon gamma-activated human monocytes depending upon its degree of iron saturation. Iron-lactoferrin and nonphysiologic iron chelates reverse monocyte activation against Legionella pneumophila. J. Clin. Invest. 1991, 88:1103-1112.
26. Case C.L., Roy C.R. ASC modulates the function of NLRC4 in response to infection of macrophages by Legionella pneumophila. MBio 2011, 2:e00117.
27. Case C.L., Shin S., Roy C.R. Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 2009, 77:1981-1991.
28. Chen G., Zhuchenko O., Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 2007, 317:678-681.
29. Chin A.I., Dempsey P.W., Bruhn K., Miller J.F., Xu Y., Cheng G. Involvement of receptor-interacting protein 2 in innate and adaptive immune responses. Nature 2002, 416:190-194.
30. Chiu Y.H., Macmillan J.B., Chen Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138:576-591.
31. Coers J., Vance R.E., Fontana M.F., Dietrich W.F. Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell. Microbiol. 2007, 9:2344-2357.
32. Derre I., Isberg R.R. Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect. Immun. 2004, 72:6221-6229.
33. Dietrich W.F., Damron D.M., Isberg R.R., Lander E.S., Swanson M.S. Lgn1, a gene that determines susceptibility to Legionella pneumophila, maps to mouse chromosome 13. Genomics 1995, 26:443-450.
34. Diez E., Lee S.H., Gauthier S., Yaraghi Z., Tremblay M., Vidal S., Gros P. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 2003, 33:55-60.
35. Finlay B.B., Falkow S. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 1997, 61:136-169.
36. Fontana M.F., Banga S., Barry K.C., Shen X., Tan Y., Luo Z.Q., Vance R.E. Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog. 2011, 7:e1001289.
37. Fortier A., de Chastellier C., Balor S., Gros P. Birc1e/Naip5 rapidly antagonizes modulation of phagosome maturation by Legionella pneumophila. Cell. Microbiol. 2007, 9:910-923.
38. Fortier A., Doiron K., Saleh M., Grinstein S., Gros P. Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irf1 and Irf8 and nod-like receptors Naip5 and Nlrc4. Infect. Immun. 2009, 77:4794-4805.
39. Fortier A., Faucher S.P., Diallo K., Gros P. Global cellular changes induced by Legionella pneumophila infection of bone marrow-derived macrophages. Immunobiology 2011, 216:1274-1285.
40. Fritz J.H., Girardin S.E., Fitting C., Werts C., Mengin-Lecreulx D., Caroff M., Cavaillon J.M., Philpott D.J., Adib-Conquy M. Synergistic stimulation of human monocytes and dendritic cells by Toll-like receptor 4 and NOD1- and NOD2-activating agonists. Eur. J. Immunol. 2005, 35:2459-2470.
41. Fritz J.H., Ferrero R.L., Philpott D.J., Girardin S.E. Nod-like proteins in immunity, inflammation and disease. Nat. Immunol. 2006, 7:1250-1257.
42. Frutuoso M.S., Hori J.I., Pereira M.S., Junior D.S., Sonego F., Kobayashi K.S., Flavell R.A., Cunha F.Q., Zamboni D.S. The pattern recognition receptors Nod1 and Nod2 account for neutrophil recruitment to the lungs of mice infected with Legionella pneumophila. Microbes Infect. 2010, 12:819-827.
43. Ge J., Xu H., Li T., Zhou Y., Zhang Z., Li S., Liu L., Shao F. A Legionella type IV effector activates the NF-kappaB pathway by phosphorylating the IkappaB family of inhibitors. Proc. Natl. Acad. Sci. USA 2009, 106:13725-13730.
44. Hawn T.R., Smith K.D., Aderem A., Skerrett S.J. Myeloid differentiation primary response gene (88)- and toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J. Infect. Dis. 2006, 193:1693-1702.
45. Heath L., Chrisp C., Huffnagle G., LeGendre M., Osawa Y., Hurley M., Engleberg C., Fantone J., Brieland J. Effector mechanisms responsible for gamma interferon-mediated host resistance to Legionella pneumophila lung infection: The role of endogenous nitric oxide differs in susceptible and resistant murine hosts. Infect. Immun. 1996, 64:5151-5160.
46. Horwitz M.A. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 1983, 158:1319-1331.
47. Horwitz M.A. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 1983, 158:2108-2126.
48. Horwitz M.A., Maxfield F.R. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J. Cell Biol. 1984, 99:1936-1943.
49. Horwitz M.A., Silverstein S.C. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J. Clin. Invest. 1980, 66:441-450.
50. Horwitz M.A., Silverstein S.C. Activated human monocytes inhibit the intracellular multiplication of Legionnaires' disease bacteria. J. Exp. Med. 1981, 154:1618-1635.
51. Hsu Y.M., Zhang Y., You Y., Wang D., Li H., Duramad O., Qin X.F., Dong C., Lin X. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat. Immunol. 2007, 8:198-205.
52. Hubber A., Roy C.R. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol. 2010, 26:261-283.
53. Ishii K.J., Coban C., Kato H., Takahashi K., Torii Y., Takeshita F., Ludwig H., Sutter G., Suzuki K., Hemmi H., Sato S., Yamamoto M., et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 2006, 7:40-48.
54. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455:674-678.
55. Ishikawa H., Ma Z., Barber G.N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009, 461:788-792.
56. Jin L., Hill K.K., Filak H., Mogan J., Knowles H., Zhang B., Perraud A.L., Cambier J.C., Lenz L.L. MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J. Immunol. 2011, 187:2595-2601.
57. Joller N., Sporri R., Hilbi H., Oxenius A. Induction and protective role of antibodies in Legionella pneumophila infection. Eur. J. Immunol. 2007, 37:3414-3423.
58. Joshi A.D., Swanson M.S. Secrets of a successful pathogen: Legionella resistance to progression along the autophagic pathway. Front. Microbiol. 2011, 2:138.
59. Kagan J.C., Roy C.R. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 2002, 4:945-954.
60. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007, 27:549-559.
61. Kaufmann A.F., McDade J.E., Patton C.M., Bennett J.V., Skaliy P., Feeley J.C., Anderson D.C., Potter M.E., Newhouse V.F., Gregg M.B., Brachman P.S. Pontiac fever: Isolation of the etiologic agent (Legionella pneumophila) and demonstration of its mode of transmission. Am. J. Epidemiol. 1981, 114:337-347.
62. Kobayashi K., Inohara N., Hernandez L.D., Galan J.E., Nunez G., Janeway C.A., Medzhitov R., Flavell R.A. RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 2002, 416:194-199.
63. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
64. Kofoed E.M., Vance R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011, 477:592-595.
65. Laguna R.K., Creasey E.A., Li Z., Valtz N., Isberg R.R. A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc. Natl. Acad. Sci. USA 2006, 103:18745-18750.
66. Lamkanfi M., Dixit V.M. Inflammasomes: Guardians of cytosolic sanctity. Immunol. Rev. 2009, 227:95-105.
67. Lamkanfi M., Amer A., Kanneganti T.D., Munoz-Planillo R., Chen G., Vandenabeele P., Fortier A., Gros P., Nunez G. The Nod-like receptor family member Naip5/Birc1e restricts Legionella pneumophila growth independently of caspase-1 activation. J. Immunol. 2007, 178:8022-8027.
68. Li Z., Dugan A.S., Bloomfield G., Skelton J., Ivens A., Losick V., Isberg R.R. The amoebal MAP kinase response to Legionella pneumophila is regulated by DupA. Cell Host Microbe 2009, 6:253-267.
69. 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.F., Monack D.M., Tsolis R.M., et al. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 2008, 9:1171-1178.
70. Lightfield K.L., Persson J., Trinidad N.J., Brubaker S.W., Kofoed E.M., Sauer J.D., Dunipace E.A., Warren S.E., Miao E.A., Vance R.E. Differential requirements for NAIP5 in activation of the NLRC4 (IPAF) inflammasome. Infect. Immun. 2011, 79:1606-1614.
71. Lippmann J., Rothenburg S., Deigendesch N., Eitel J., Meixenberger K., van Laak V., Slevogt H., N'Guessan P.D., Hippenstiel S., Chakraborty T., Flieger A., Suttorp N., et al. IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell. Microbiol. 2008, 10:2579-2588.
72. Lippmann J., Muller H.C., Naujoks J., Tabeling C., Shin S., Witzenrath M., Hellwig K., Kirschning C.J., Taylor G.A., Barchet W., Bauer S., Suttorp N., et al. Dissection of a type I interferon pathway in controlling bacterial intracellular infection in mice. Cell. Microbiol. 2011, 13:1668-1682.
73. Losick V.P., Isberg R.R. NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J. Exp. Med. 2006, 203:2177-2189.
74. Losick V.P., Haenssler E., Moy M.Y., Isberg R.R. LnaB: A Legionella pneumophila activator of NF-kappaB. Cell. Microbiol. 2010, 12:1083-1097.
75. Luhrmann A., Nogueira C.V., Carey K.L., Roy C.R. Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc. Natl. Acad. Sci. USA 2010, 107:18997-19001.
76. Luo Z.Q., Isberg R.R. Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. USA 2004, 101:841-846.
77. Marra A., Blander S.J., Horwitz M.A., Shuman H.A. Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc. Natl. Acad. Sci. USA 1992, 89:9607-9611.
78. Masumoto J., Yang K., Varambally S., Hasegawa M., Tomlins S.A., Qiu S., Fujimoto Y., Kawasaki A., Foster S.J., Horie Y., Mak T.W., Nunez G., et al. Nod1 acts as an intracellular receptor to stimulate chemokine production and neutrophil recruitment in vivo. J. Exp. Med. 2006, 203:203-213.
79. McDade J.E., Shepard C.C., Fraser D.W., Tsai T.R., Redus M.A., Dowdle W.R. Legionnaires' disease: Isolation of a bacterium and demonstration of its role in other respiratory disease. N. Engl. J. Med. 1977, 297:1197-1203.
80. McHugh S.L., Yamamoto Y., Klein T.W., Friedman H. Murine macrophages differentially produce proinflammatory cytokines after infection with virulent vs. avirulent Legionella pneumophila. J. Leukoc. Biol. 2000, 67:863-868.
81. McWhirter S.M., Barbalat R., Monroe K.M., Fontana M.F., Hyodo M., Joncker N.T., Ishii K.J., Akira S., Colonna M., Chen Z.J., Fitzgerald K.A., Hayakawa Y., et al. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J. Exp. Med. 2009, 206:1899-1911.
82. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 2006, 7:569-575.
83. Miao E.A., Ernst R.K., Dors M., Mao D.P., Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. USA 2008, 105:2562-2567.
84. Miao E.A., Leaf I.A., Treuting P.M., Mao D.P., Dors M., Sarkar A., Warren S.E., Wewers M.D., Aderem A. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 2010, 11:1136-1142.
85. Miao E.A., Mao D.P., Yudkovsky N., Bonneau R., Lorang C.G., Warren S.E., Leaf I.A., Aderem A. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. USA 2010, 107:3076-3080.
86. Molofsky A.B., Byrne B.G., Whitfield N.N., Madigan C.A., Fuse E.T., Tateda K., Swanson M.S. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 2006, 203:1093-1104.
87. Monroe K.M., McWhirter S.M., Vance R.E. Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog. 2009, 5:e1000665.
88. Neild A.L., Roy C.R. Legionella reveal dendritic cell functions that facilitate selection of antigens for MHC class II presentation. Immunity 2003, 18:813-823.
89. Neild A.L., Roy C.R. Immunity to vacuolar pathogens: What can we learn from Legionella?. Cell. Microbiol. 2004, 6:1011-1018.
90. Nimchuk Z., Eulgem T., Holt B.F., Dangl J.L. Recognition and response in the plant immune system. Annu. Rev. Genet. 2003, 37:579-609.
91. Opitz B., Vinzing M., van Laak V., Schmeck B., Heine G., Gunther S., Preissner R., Slevogt H., N'Guessan P.D., Eitel J., Goldmann T., Flieger A., et al. Legionella pneumophila induces IFNbeta in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J. Biol. Chem. 2006, 281:36173-36179.
92. Pereira M.S., Marques G.G., Dellama J.E., Zamboni D.S. The Nlrc4 inflammasome contributes to restriction of pulmonary infection by flagellated Legionella spp that trigger pyroptosis. Front. Microbiol. 2011, 2:33.
93. Pereira M.S., Morgantetti G.F., Massis L.M., Horta C.V., Hori J.I., Zamboni D.S. Activation of NLRC4 by Flagellated bacteria triggers caspase-1-dependent and -independent responses to restrict Legionella pneumophila replication in macrophages and in vivo. J. Immunol. 2011, 187:6447-6455.
94. Plumlee C.R., Lee C., Beg A.A., Decker T., Shuman H.A., Schindler C. Interferons direct an effective innate response to Legionella pneumophila infection. J. Biol. Chem. 2009, 284:30058-30066.
95. Ren T., Zamboni D.S., Roy C.R., Dietrich W.F., Vance R.E. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2006, 2:e18.
96. Robinson C.G., Roy C.R. Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila. Cell. Microbiol. 2006, 8:793-805.
97. Roy C.R., Berger K.H., Isberg R.R. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 1998, 28:663-674.
98. Sauer J.D., Sotelo-Troha K., von Moltke J., Monroe K.M., Rae C.S., Brubaker S.W., Hyodo M., Hayakawa Y., Woodward J.J., Portnoy D.A., Vance R.E. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 2011, 79:688-694.
99. Schiavoni G., Mauri C., Carlei D., Belardelli F., Pastoris M.C., Proietti E. Type I IFN protects permissive macrophages from Legionella pneumophila infection through an IFN-gamma-independent pathway. J. Immunol. 2004, 173:1266-1275.
100. Segal G., Purcell M., Shuman H.A. 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 1998, 95:1669-1674.
101. Shen X., Banga S., Liu Y., Xu L., Gao P., Shamovsky I., Nudler E., Luo Z.Q. Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell. Microbiol. 2009, 11:911-926.
102. Shin S., Case C.L., Archer K.A., Nogueira C.V., Kobayashi K.S., Flavell R.A., Roy C.R., Zamboni D.S. Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog. 2008, 4:e1000220.
103. Shinozawa Y., Matsumoto T., Uchida K., Tsujimoto S., Iwakura Y., Yamaguchi K. Role of interferon-gamma in inflammatory responses in murine respiratory infection with Legionella pneumophila. J. Med. Microbiol. 2002, 51:225-230.
104. Silveira T.N., Zamboni D.S. Pore formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect. Immun. 2010, 78:1403-1413.
105. Skerrett S.J., Martin T.R. Roles for tumor necrosis factor alpha and nitric oxide in resistance of rat alveolar macrophages to Legionella pneumophila. Infect. Immun. 1996, 64:3236-3243.
106. Skerrett S.J., Bagby G.J., Schmidt R.A., Nelson S. Antibody-mediated depletion of tumor necrosis factor-alpha impairs pulmonary host defenses to Legionella pneumophila. J. Infect. Dis. 1997, 176:1019-1028.
107. Sporri R., Joller N., Albers U., Hilbi H., Oxenius A. MyD88-dependent IFN-gamma production by NK cells is key for control of Legionella pneumophila infection. J. Immunol. 2006, 176:6162-6171.
108. Sporri R., Joller N., Hilbi H., Oxenius A. A novel role for neutrophils as critical activators of NK cells. J. Immunol. 2008, 181:7121-7130.
109. Stetson D.B., Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006, 24:93-103.
110. Sutterwala F.S., Mijares L.A., Li L., Ogura Y., Kazmierczak B.I., Flavell R.A. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 2007, 204:3235-3245.
111. Suzuki T., Franchi L., Toma C., Ashida H., Ogawa M., Yoshikawa Y., Mimuro H., Inohara N., Sasakawa C., Nunez G. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 2007, 3:e111.
112. Swanson M.S., Isberg R.R. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 1995, 63:3609-3620.
113. Tada H., Aiba S., Shibata K., Ohteki T., Takada H. Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect. Immun. 2005, 73:7967-7976.
114. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., Ohba Y., Taniguchi T. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
115. Tilney L.G., Harb O.S., Connelly P.S., Robinson C.G., Roy C.R. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: Implications for conversion of plasma membrane to the ER membrane. J. Cell Sci. 2001, 114:4637-4650.
116. Travassos L.H., Carneiro L.A., Ramjeet M., Hussey S., Kim Y.G., Magalhaes J.G., Yuan L., Soares F., Chea E., Le Bourhis L., Boneca I.G., Allaoui A., et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 2010, 11:55-62.
117. Vance R.E. Immunology taught by bacteria. J. Clin. Immunol. 2010, 30:507-511.
118. Vance R.E., Isberg R.R., Portnoy D.A. Patterns of pathogenesis: Discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 2009, 6:10-21.
119. Viala J., Chaput C., Boneca I.G., Cardona A., Girardin S.E., Moran A.P., Athman R., Memet S., Huerre M.R., Coyle A.J., DiStefano P.S., Sansonetti P.J., et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 2004, 5:1166-1174.
120. 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., et al. NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 2008, 180:6808-6815.
121. Vogel J.P., Andrews H.L., Wong S.K., Isberg R.R. Conjugative transfer by the virulence system of Legionella pneumophila. Science 1998, 279:873-876.
122. Whitfield N.N., Byrne B.G., Swanson M.S. Mouse macrophages are permissive to motile Legionella species that fail to trigger pyroptosis. Infect. Immun. 2010, 78:423-432.
123. Wilmanski J.M., Petnicki-Ocwieja T., Kobayashi K.S. NLR proteins: Integral members of innate immunity and mediators of inflammatory diseases. J. Leukoc. Biol. 2007, 83:13-30.
124. Woodward J.J., Iavarone A.T., Portnoy D.A. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 2010, 328:1703-1705.
125. 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., Dietrich W.F. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 2003, 13:27-36.
126. Yamamoto Y., Klein T.W., Newton C.A., Widen R., Friedman H. Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect. Immun. 1988, 56:370-375.
127. Zamboni D.S., Kobayashi K.S., Kohlsdorf T., Ogura Y., Long E.M., Vance R.E., Kuida K., Mariathasan S., Dixit V.M., Flavell R.A., Dietrich W.F., Roy C.R. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 2006, 7:318-325.
128. Zhao Y., Yang J., Shi J., Gong Y.N., Lu Q., Xu H., Liu L., Shao F. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011, 477:596-600.