Inflammasome-mediated cell death in response to bacterial pathogens that access the host cell cytosol: Lessons from Legionella pneumophila

Frontiers in Cellular and Infection Microbiology

Volumn 3, Issue DEC, 2013, Pages

  Casson, Cierra N ^a   Shin, Sunny ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Caspase 1; Caspase 11; Cell death; Inflammasome; Legionella pneumophila; Pyroptosis

Indexed keywords

CASPASE 11; CRYOPYRIN; FLAGELLIN; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NEURONAL APOPTOSIS INHIBITORY PROTEIN; NLR FAMILY CARD DOMAIN CONTAINING 4 PROTEIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; PEPTIDES AND PROTEINS; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; CASPASE;

AUTOPHAGY; CELL DEATH; CYTOSOL; DOWN REGULATION; HUMAN; IMMUNE RESPONSE; LEGIONELLA PNEUMOPHILA; MACROPHAGE; NONHUMAN; PROTEIN EXPRESSION; PYROPTOSIS; SHORT SURVEY; UPREGULATION; CASPASE-1; CASPASE-11; IMMUNOLOGY; LEGIONNAIRE DISEASE; METABOLISM; MICROBIOLOGY; REVIEW;

CASPASE-1; CASPASE-11; CELL DEATH; INFLAMMASOME; LEGIONELLA PNEUMOPHILA; PYROPTOSIS;

CASPASES; CELL DEATH; CYTOSOL; INFLAMMASOMES; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE;

EID: 84897923374     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00111     Document Type: Short Survey

References (96)

1. Aachoui, Y., Leaf, I. A., Hagar, J. A., Fontana, M. F., Campos, C. G., Zak, D. E., et al. (2013). Caspase-11 protects against bacteria that escape the vacuole. Science 339, 975-978. doi: 10.1126/science.1230751.
2. Abdelaziz, D. H. A., Gavrilin, M. A., Akhter, A., Caution, K., Kotrange, S., Khweek, A. A., et al. (2011a). Asc-dependent and independent mechanisms contribute to restriction of Legionella pneumophila infection in murine macrophages. Front. Microbiol. 2:18. doi: 10.3389/fmicb.2011.00018.
3. Abdelaziz, D. H., Gavrilin, M. A., Akhter, A., Caution, K., Kotrange, S., Khweek, A. A., et al. (2011b). Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J. Biol. Chem. 286, 3203-3208. doi: 10.1074/jbc.M110.197681.
4. Akhter, A., Caution, K., Abu Khweek, A., Tazi, M., Abdulrahman, B. A., Abdelaziz, D. H. A., et al. (2012). Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37, 35-47. doi: 10.1016/j.immuni.2012.05.001.
5. Akhter, A., Gavrilin, M. A., Frantz, L., Washington, S., Ditty, C., Limoli, D., et al. (2009). Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog. 5:e1000361. doi: 10.1371/journal.ppat.1000361.
6. Amer, A., Franchi, L., Kanneganti, T.-D., Body-Malapel, M., Ozören, N., Brady, G., et al. (2006). Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281, 35217-35223. doi: 10.1074/jbc.M604933200.
7. Amer, A. O., and Swanson, M. S. (2005). Autophagy is an immediate macrophage response to Legionella pneumophila. Cell. Microbiol. 7, 765-778. doi: 10.1111/j.1462-5822.2005.00509.x.
8. 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. doi: 10.1111/j.1462-5822.2008.01234.x.
9. Barry, K. C., Fontana, M. F., Portman, J. L., Dugan, A. S., and Vance, R. E. (2013). IL-1α signaling initiates the inflammatory response to virulent Legionella pneumophila in vivo. J. Immunol. 190, 6329-6339. doi: 10.4049/jimmunol.1300100.
10. Berger, K. H., and Isberg, R. R. (1993). Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7, 7-19. doi: 10.1111/j.1365-2958.1993.tb01092.x.
11. Bergsbaken, T., Fink, S. L., and Cookson, B. T. (2009). Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7, 99-109. doi: 10.1038/nrmicro2070.
12. Bohn, E., Sing, A., Zumbihl, R., Bielfeldt, C., Okamura, H., Kurimoto, M., et al. (1998). IL-18 (IFN-gamma-inducing factor) regulates early cytokine production in, and promotes resolution of, bacterial infection in mice. J. Immunol. 160, 299-307.
13. Boniotto, M., Tailleux, L., Lomma, M., Gicquel, B., Buchrieser, C., Garcia, S., et al. (2012). Population variation in NAIP functional copy number confers increased cell death upon Legionella pneumophila infection. Hum. Immunol. 73, 196-200. doi: 10.1016/j.humimm.2011.10.014.
14. 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. doi: 10.1128/IAI.68.12.6567-6573.2000.
15. Broz, P., Ruby, T., Belhocine, K., Bouley, D. M., Kayagaki, N., Dixit, V. M., et al. (2012). Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490, 288-291. doi: 10.1038/nature11419.
16. Broz, P., von Moltke, J., Jones, J. W., Vance, R. E., and Monack, D. M. (2010). Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8, 471-483. doi: 10.1016/j.chom.2010.11.007.
17. Byrne, B. G., Dubuisson, J.-F., Joshi, A. D., Persson, J. J., and Swanson, M. S. (2013). Inflammasome components coordinate autophagy and pyroptosis as macrophage responses to infection. mBio 4:e00620-12. doi: 10.1128/mBio.00620-12.
18. Case, C. L., Kohler, L. J., Lima, J. B., Strowig, T., de Zoete, M. R., Flavell, R. A., et al. (2013). Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc. Natl. Acad. Sci. U.S.A. 110, 1851-1856. doi: 10.1073/pnas.1211521110.
19. Case, C. L., and Roy, C. R. (2011). Asc modulates the function of NLRC4 in response to infection of macrophages by Legionella pneumophila. mBio 2:e00117-11. doi: 10.1128/mBio.00117-11.
20. Case, C. L., Shin, S., and Roy, C. R. (2009). Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 77, 1981-1991. doi: 10.1128/IAI.01382-08.
21. Casson, C. N., Copenhaver, A. M., Zwack, E. E., Nguyen, H. T., Strowig, T., Javdan, B., et al. (2013). Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog. 9:e1003400. doi: 10.1371/journal.ppat.1003400.
22. Creasey, E. A., and Isberg, R. R. (2012). The protein SdhA maintains the integrity of the Legionella-containing vacuole. Proc. Natl. Acad. Sci. U.S.A. 109, 3481-3486. doi: 10.1073/pnas.1121286109.
23. Davis, B. K., Wen, H., and Ting, J. P. Y. (2011). The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707-735. doi: 10.1146/annurev-immunol-031210-101405.
24. Derré, I., and Isberg, R. R. (2004). Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect. Immun. 72, 6221-6229. doi: 10.1128/IAI.72.11.6221-6229.2004.
25. Diez, E., Lee, S.-H., Gauthier, S., Yaraghi, Z., Tremblay, M., Vidal, S., et al. (2003). Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33, 55-60. doi: 10.1038/ng1065.
26. Diez, E., Yaraghi, Z., MacKenzie, A., and Gros, P. (2000). The neuronal apoptosis inhibitory protein (Naip) is expressed in macrophages and is modulated after phagocytosis and during intracellular infection with Legionella pneumophila. J. Immunol. 164, 1470-1477.
27. Dinarello, C. A. (2009). Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27, 519-550. doi: 10.1146/annurev.immunol.021908.132612.
28. Fink, S. L., and Cookson, B. T. (2005). Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73, 1907-1916. doi: 10.1128/IAI.73.4.1907-1916.2005.
29. Fliermans, C. B., Cherry, W. B., Orrison, L. H., Smith, S. J., Tison, D. L., and Pope, D. H. (1981). Ecological distribution of Legionella pneumophila. Appl. Environ. Microbiol. 41, 9-16.
30. Fortier, A., de Chastellier, C., Balor, S., and Gros, P. (2007). Birc1e/Naip5 rapidly antagonizes modulation of phagosome maturation by Legionella pneumophila. Cell. Microbiol. 9, 910-923. doi: 10.1111/j.1462-5822.2006.00839.x.
31. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T.-D., Ozören, N., Jagirdar, R., et al. (2006). Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7, 576-582. doi: 10.1038/ni1346.
32. Franchi, L., Muñoz-Planillo, R., and Núñez, G. (2012). Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 13, 325-332. doi: 10.1038/ni.2231.
33. Fraser, D. W., Tsai, T. R., Orenstein, W., Parkin, W. E., Beecham, H. J., Sharrar, R. G., et al. (1977). Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297, 1189-1197. doi: 10.1056/NEJM197712012972201.
34. Fritz, J. H., Ferrero, R. L., Philpott, D. J., and Girardin, S. E. (2006). Nod-like proteins in immunity, inflammation and disease. Nat. Immunol. 7, 1250-1257. doi: 10.1038/ni1412.
35. Furugen, M., Higa, F., Hibiya, K., Teruya, H., Akamine, M., Haranaga, S., et al. (2008). Legionella pneumophila 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. doi: 10.1186/1465-9921-9-39.
36. Ge, J., Gong, Y.-N., Xu, Y., and Shao, F. (2012). Preventing bacterial DNA release and absent in melanoma 2 inflammasome activation by a Legionella effector functioning in membrane trafficking. Proc. Natl. Acad. Sci. U.S.A. 109, 6193-6198. doi: 10.1073/pnas.1117490109.
37. Ghayur, T., Banerjee, S., Hugunin, M., Butler, D., Herzog, L., Carter, A., et al. (1997). Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 386, 619-623. doi: 10.1038/386619a0.
38. Growney, J. D., and Dietrich, W. F. (2000). High-resolution genetic and physical map of the Lgn1 interval in C57BL/6J implicates Naip2 or Naip5 in Legionella pneumophila pathogenesis. Genome Res. 10, 1158-1171. doi: 10.1101/gr.10.8.1158.
39. Gu, Y., Kuida, K., Tsutsui, H., Ku, G., Hsiao, K., Fleming, M. A., et al. (1997). Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 275, 206-209. doi: 10.1126/science.275.5297.206.
40. Gurung, P., Malireddi, R. K. S., Anand, P. K., Demon, D., Walle, L. V., Liu, Z., et al. (2012). TRIF-mediated caspase-11 production integrates TLR4-and Nlrp3 inflammasome-mediated host defense against enteropathogens. J. Biol. Chem. 287, 34474-34483. doi: 10.1074/jbc.M112.401406.
41. Hagar, J. A., Powell, D. A., Aachoui, Y., Ernst, R. K., and Miao, E. A. (2013). Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341, 1250-1253. doi: 10.1126/science.1240988.
42. Harton, J. A., Linhoff, M. W., Zhang, J., and Ting, J. P. Y. (2002). Cutting edge: CATERPILLER: a large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucine-rich repeat domains. J. Immunol. 169, 4088-4093.
43. Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D. R., et al. (2009). AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514-518. doi: 10.1038/nature07725.
44. Howard, A. D., Kostura, M. J., Thornberry, N., Ding, G. J., Limjuco, G., Weidner, J., et al. (1991). IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1 beta precursor at two distinct sites and does not cleave 31-kDa IL-1 alpha. J. Immunol. 147, 2964-2969.
45. Janeway, C. A., and Medzhitov, R. (2002). Innate immune recognition. Annu. Rev. Immunol. 20, 197-216. doi: 10.1146/annurev.immunol.20.083001.084359.
46. Kanneganti, T.-D., Ozören, N., Body-Malapel, M., Amer, A., Park, J.-H., Franchi, L., et al. (2006). Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440, 233-236. doi: 10.1038/nature04517.
47. Katagiri, N., Shobuike, T., Chang, B., Kukita, A., and Miyamoto, H. (2012). The human apoptosis inhibitor NAIP induces pyroptosis in macrophages infected with Legionella pneumophila. Microbes Infect. 14, 1123-1132. doi: 10.1016/j.micinf.2012.03.006.
48. Kayagaki, N., Warming, S., Lamkanfi, M., Van de Walle, L., Louie, S., Dong, J., et al. (2011). Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121. doi: 10.1038/nature10558.
49. Kayagaki, N., Wong, M. T., Stowe, I. B., Ramani, S. R., Gonzalez, L. C., Akashi-Takamura, S., et al. (2013). Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341, 1246-1249. doi: 10.1126/science.1240248.
50. Keller, M., Rüegg, A., Werner, S., and Beer, H.-D. (2008). Active caspase-1 is a regulator of unconventional protein secretion. Cell 132, 818-831. doi: 10.1016/j.cell.2007.12.040.
51. Kofoed, E. M., and Vance, R. E. (2011). Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477, 592-595. doi: 10.1038/nature10394.
52. Kono, H., and Rock, K. L. (2008). How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8, 279-289. doi: 10.1038/nri2215.
53. Kuida, K., Lippke, J. A., Ku, G., Harding, M. W., Livingston, D. J., Su, M. S., et al. (1995). Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267, 2000-2003. doi: 10.1126/science.7535475.
54. Labow, M., Shuster, D., Zetterstrom, M., Nunes, P., Terry, R., Cullinan, E. B., et al. (1997). Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice. J. Immunol. 159, 2452-2461.
55. Laguna, R. K., Creasey, E. A., Li, Z., Valtz, N., and Isberg, R. R. (2006). A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc. Natl. Acad. Sci. U.S.A. 103, 18745-18750. doi: 10.1073/pnas.0609012103.
56. Lamkanfi, M., Amer, A., Kanneganti, T.-D., Muñoz-Planillo, R., Chen, G., Vandenabeele, P., et al. (2007). The Nod-like receptor family member Naip5/Birc1e restricts Legionella pneumophila growth independently of caspase-1 activation. J. Immunol. 178, 8022-8027.
57. Lamkanfi, M., and Dixit, V. M. (2009). Inflammasomes: guardians of cytosolic sanctity. Immunol. Rev. 227, 95-105. doi: 10.1111/j.1600-065X.2008.00730.x.
58. Lightfield, K. L., Persson, J., Brubaker, S. W., Witte, C. E., von Moltke, J., Dunipace, E. A., et al. (2008). Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9, 1171-1178. doi: 10.1038/ni.1646.
59. Lightfield, K. L., Persson, J., Trinidad, N. J., Brubaker, S. W., Kofoed, E. M., Sauer, J.-D., et al. (2011). Differential requirements for NAIP5 in activation of the NLRC4 inflammasome. Infect. Immun. 79, 1606-1614. doi: 10.1128/IAI.01187-10.
60. Liu, Y., Gao, P., Banga, S., and Luo, Z.-Q. (2008). An in vivo gene deletion system for determining temporal requirement of bacterial virulence factors. Proc. Natl. Acad. Sci. U.S.A. 105, 9385-9390. doi: 10.1073/pnas.0801055105.
61. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., et al. (2006). Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232. doi: 10.1038/nature04515.
62. 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. U.S.A. 89, 9607-9611. doi: 10.1073/pnas.89.20.9607.
63. Martinon, F., Burns, K., and Tschopp, J. (2002). The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10, 417-426. doi: 10.1016/S1097-2765(02)00599-3.
64. Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., and Tschopp, J. (2006). Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241. doi: 10.1038/nature04516.
65. Matsuda, F., Fujii, J., and Yoshida, S.-I. (2009). Autophagy induced by 2-deoxy-D-glucose suppresses intracellular multiplication of Legionella pneumophila in A/J mouse macrophages. Autophagy 5, 484-493. doi: 10.4161/auto.5.4.7760.
66. 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. doi: 10.1056/NEJM197712012972202.
67. Medzhitov, R. (2007). Recognition of microorganisms and activation of the immune response. Nature 449, 819-826. doi: 10.1038/nature06246.
68. Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I., et al. (2006). Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7, 569-575. doi: 10.1038/ni1344.
69. Miao, E. A., Leaf, I. A., Treuting, P. M., Mao, D. P., Dors, M., Sarkar, A., et al. (2010a). Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11, 1136-1142. doi: 10.1038/ni.1960.
70. Miao, E. A., Mao, D. P., Yudkovsky, N., Bonneau, R., Lorang, C. G., Warren, S. E., et al. (2010b). Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U.S.A. 107, 3076-3080. doi: 10.1073/pnas.0913087107.
71. Molofsky, A. B., Byrne, B. G., Whitfield, N. N., Madigan, C. A., Fuse, E. T., Tateda, K., et al. (2006). Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203, 1093-1104. doi: 10.1084/jem.20051659.
72. Monroe, K. M., McWhirter, S. M., and Vance, R. E. (2009). Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog. 5:e1000665. doi: 10.1371/journal.ppat.1000665.
73. Pereira, M. S. F., Morgantetti, G. F., Massis, L. M., Horta, C. V., Hori, J. I., and Zamboni, D. S. (2011). 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. 187, 6447-6455. doi: 10.4049/jimmunol.1003784.
74. Rathinam, V. A. K., Vanaja, S. K., and Fitzgerald, K. A. (2012a). Regulation of inflammasome signaling. Nat. Immunol. 13, 333-332. doi: 10.1038/ni.2237.
75. Rathinam, V. A. K., Vanaja, S. K., Waggoner, L., Sokolovska, A., Becker, C., Stuart, L. M., et al. (2012b). TRIF licenses Caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150, 606-619. doi: 10.1016/j.cell.2012.07.007.
76. 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. doi: 10.1371/journal.ppat.0020018.
77. Roberts, T. L., Idris, A., Dunn, J. A., Kelly, G. M., Burnton, C. M., Hodgson, S., et al. (2009). HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060. doi: 10.1126/science.1169841.
78. Rowbotham, T. J. (1980). Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33, 1179-1183. doi: 10.1136/jcp.33.12.1179.
79. 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. doi: 10.1046/j.1365-2958.1998.00841.x.
80. 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.
81. Santic, M., Asare, R., Doric, M., and Abu Kwaik, Y. (2007). Host-dependent trigger of caspases and apoptosis by Legionella pneumophila. Infect. Immun. 75, 2903-2913. doi: 10.1128/IAI.00147-07.
82. Scharf, J. M., Damron, D., Frisella, A., Bruno, S., Beggs, A. H., Kunkel, L. M., et al. (1996). The mouse region syntenic for human spinal muscular atrophy lies within the Lgn1 critical interval and contains multiple copies of Naip exon 5. Genomics 38, 405-417. doi: 10.1006/geno.1996.0644.
83. 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. doi: 10.1073/pnas.95.4.1669.
84. 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. doi: 10.1128/IAI.00905-09.
85. Spörri, 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.
86. Srinivasula, S. M., Poyet, J.-L., Razmara, M., Datta, P., Zhang, Z., and Alnemri, E. S. (2002). The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J. Biol. Chem. 277, 21119-21122. doi: 10.1074/jbc.C200179200.
87. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., et al. (1992). A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356, 768-774. doi: 10.1038/356768a0.
88. Vance, R. E., Isberg, R. R., and Portnoy, D. A. (2009). Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6, 10-21. doi: 10.1016/j.chom.2009.06.007.
89. Vinzing, M., Eitel, J., Lippmann, J., Hocke, A. C., Zahlten, J., Slevogt, H., et al. (2008). NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 180, 6808-6815.
90. 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. doi: 10.1126/science.279.5352.873.
91. Wang, S., Miura, M., Jung, Y. K., Zhu, H., Gagliardini, V., Shi, L., et al. (1996). Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE. J. Biol. Chem. 271, 20580-20587. doi: 10.1074/jbc.271.34.20580.
92. Wang, S., Miura, M., Jung, Y. K., Zhu, H., Li, E., and Yuan, J. (1998). Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92, 501-509. doi: 10.1016/S0092-8674(00)80943-5.
93. Wright, E. K., Goodart, S. A., Growney, J. D., Hadinoto, V., Endrizzi, M. G., Long, E. M., et al. (2003). Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13, 27-36. doi: 10.1016/S0960-9822(02)01359-3.
94. Yang, J., Zhao, Y., Shi, J., and Shao, F. (2013). Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc. Natl. Acad. Sci. U.S.A. 110, 14408-14413. doi: 10.1073/pnas.1306376110.
95. 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. doi: 10.1038/ni1305.
96. Zhao, Y., Yang, J., Shi, J., Gong, Y.-N., Lu, Q., Xu, H., et al. (2011). The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477, 596-600. doi: 10.1038/nature10510.