Role of type i interferons in inflammasome activation, cell death, and disease during microbial infection

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue NOV, 2013, Pages

  Subbarao Malireddi, R K ^a   Kanneganti, Thirumala Devi ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Caspase 1; Cell death; I IFN; IFN ; Inflammasome; NLR; Nlrp3

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CRYOPYRIN; GAMMA INTERFERON; INFLAMMASOME; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9;

ANTHRAX; APOPTOSIS; ARTICLE; BACTERIAL LOAD; BACTERIAL VIRULENCE; CELL DEATH; DISEASE COURSE; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATION; LEGIONNAIRE DISEASE; LISTERIOSIS; NONHUMAN; PSEUDOMONAS INFECTION; SALMONELLOSIS; STAPHYLOCOCCUS INFECTION; STREPTOCOCCUS INFECTION; TISSUE INJURY; TULAREMIA;

EID: 84897921386     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00077     Document Type: Article

References (152)

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. Allen, I. C., Scull, M. A., Moore, C. B., Holl, E. K., McElvania-TeKippe, E., Taxman, D. J., et al. (2009). The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556-565. doi: 10.1016/j.immuni.2009.02.005
3. Anand, P. K., Malireddi, R. K., and Kanneganti, T. D. (2011). Role of the nlrp3 inflammasome in microbial infection. Front. Microbiol. 2:12. doi: 10.3389/fmicb.2011.00012
4. Arlehamn, C. S., and Evans, T. J. (2011). Pseudomonas aeruginosa pilin activates the inflammasome. Cell Microbiol. 13, 388-401. doi: 10.1111/j.1462-5822.2010.01541.x
5. Auerbuch, V., Brockstedt, D. G., Meyer-Morse, N., O'Riordan, M., and Portnoy, D. A. (2004). Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200, 527-533. doi: 10.1084/jem.20040976
6. Balachandran, S., Roberts, P. C., Kipperman, T., Bhalla, K. N., Compans, R. W., Archer, D. R., et al. (2000). Alpha/beta interferons potentiate virus-induced apoptosis through activation of the FADD/Caspase-8 death signaling pathway. J. Virol. 74, 1513-1523. doi: 10.1128/JVI.74.3.1513-1523.2000
7. 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
8. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A., Oni, T., et al. (2010). An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466, 973-977. doi: 10.1038/nature09247
9. Biondo, C., Malara, A., Costa, A., Signorino, G., Cardile, F., Midiri, A., et al. (2012). Recognition of fungal RNA by TLR7 has a non-redundant role in host defense against experimental candidiasis. Eur. J. Immunol. 42, 2632-2643. doi: 10.1002/eji.201242532
10. Biondo, C., Midiri, A., Gambuzza, M., Gerace, E., Falduto, M., Galbo, R., et al. (2008). IFN-alpha/beta signaling is required for polarization of cytokine responses toward a protective type 1 pattern during experimental cryptococcosis. J. Immunol. 181, 566-573.
11. Biondo, C., Signorino, G., Costa, A., Midiri, A., Gerace, E., Galbo, R., et al. (2011). Recognition of yeast nucleic acids triggers a host-protective type I interferon response. Eur. J. Immunol. 41, 1969-1979. doi: 10.1002/eji.201141490
12. Bouchonnet, F., Boechat, N., Bonay, M., and Hance, A. J. (2002). Alpha/beta interferon impairs the ability of human macrophages to control growth of Mycobacterium bovis BCG. Infect. Immun. 70, 3020-3025. doi: 10.1128/IAI.70.6.3020-3025.2002
13. Bourgeois, C., Majer, O., Frohner, I. E., Lesiak-Markowicz, I., Hildering, K. S., Glaser, W., et al. (2011). Conventional dendritic cells mount a type I IFN response against Candida spp. requiring novel phagosomal TLR7-mediated IFN-beta signaling. J. Immunol. 186, 3104-3112. doi: 10.4049/jimmunol.1002599
14. Bowie, A. G., and Unterholzner, L. (2008). Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 8, 911-922. doi: 10.1038/nri2436
15. Boyden, E. D., and Dietrich, W. F. (2006). Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38, 240-244. doi: 10.1038/ng1724
16. Brown, G. D. (2011). Innate antifungal immunity: the key role of phagocytes. Annu. Rev. Immunol. 29, 1-21. doi: 10.1146/annurev-immunol-030409-101229
17. Broz, P., and Monack, D. M. (2013). Non-canonical inflammasomes: caspase-11 activation and effector mechanisms. PLoS Pathog. 9:e1003144. doi: 10.1371/journal.ppat.1003144
18. Broz, P., Newton, K., Lamkanfi, M., Mariathasan, S., Dixit, V. M., and Monack, D. M. (2010). Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 207, 1745-1755. doi: 10.1084/jem.20100257
19. 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
20. Carrero, J. A., Calderon, B., and Unanue, E. R. (2004). Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 200, 535-540. doi: 10.1084/jem.20040769
21. Carrigan, S. O., Junkins, R., Yang, Y. J., Macneil, A., Richardson, C., Johnston, B., et al. (2010). IFN regulatory factor 3 contributes to the host response during Pseudomonas aeruginosa lung infection in mice. J. Immunol. 185, 3602-3609. doi: 10.4049/jimmunol.0903429
22. Cohen, T. S., and Prince, A. S. (2013). Activation of inflammasome signaling mediates pathology of acute P. aeruginosa pneumonia. J. Clin. Invest. 123, 1630-1637. doi: 10.1172/JCI66142
23. Craven, R. R., Gao, X., Allen, I. C., Gris, D., Bubeck Wardenburg, J., McElvania-Tekippe, E., et al. (2009). Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS ONE 4:e7446. doi: 10.1371/journal.pone.0007446
24. David, M. Z., and Daum, R. S. (2010). Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 23, 616-687. doi: 10.1128/CMR.00081-09
25. Del Fresno, C., Soulat, D., Roth, S., Blazek, K., Udalova, I., Sancho, D., et al. (2013). Interferon-beta production via Dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 38, 1176-1186. doi: 10.1016/j.immuni.2013.05.010
26. Der, S. D., Yang, Y. L., Weissmann, C., and Williams, B. R. (1997). A double-stranded RNA-activated protein kinase-dependent pathway mediating stress-induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 94, 3279-3283. doi: 10.1073/pnas.94.7.3279
27. Der, S. D., Zhou, A., Williams, B. R., and Silverman, R. H. (1998). Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U.S.A. 95, 15623-15628. doi: 10.1073/pnas.95.26.15623
28. de Veer, M. J., Holko, M., Frevel, M., Walker, E., Der, S., Paranjape, J. M., et al. (2001). Functional classification of interferon-stimulated genes identified using microarrays. J. Leukoc. Biol. 69, 912-920.
29. Diaz-Guerra, M., Rivas, C., and Esteban, M. (1997). Activation of the IFN-inducible enzyme RNase L causes apoptosis of animal cells. Virology 236, 354-363. doi: 10.1006/viro.1997.8719
30. Dixon, T. C., Meselson, M., Guillemin, J., and Hanna, P. C. (1999). Anthrax. N. Engl. J. Med. 341, 815-826. doi: 10.1056/NEJM199909093411107
31. Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J., et al. (2011). NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745-757. doi: 10.1016/j.cell.2011.04.022
32. Ezelle, H. J., Balachandran, S., Sicheri, F., Polyak, S. J., and Barber, G. N. (2001). Analyzing the mechanisms of interferon-induced apoptosis using CrmA and hepatitis C virus NS5A. Virology 281, 124-137. doi: 10.1006/viro.2001.0815
33. Faure, K., Sawa, T., Ajayi, T., Fujimoto, J., Moriyama, K., Shime, N., et al. (2004). TLR4 signaling is essential for survival in acute lung injury induced by virulent Pseudomonas aeruginosa secreting type III secretory toxins. Respir. Res. 5, 1. doi: 10.1186/1465-9921-5-1
34. Fernandes-Alnemri, T., Yu, J. W., Juliana, C., Solorzano, L., Kang, S., Wu, J., et al. (2010). The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11, 385-393. doi: 10.1038/ni.1859
35. Fitzgerald, K. A., McWhirter, S. M., Faia, K. L., Rowe, D. C., Latz, E., Golenbock, D. T., et al. (2003a). IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496. doi: 10.1038/ni921
36. Fitzgerald, K. A., Rowe, D. C., Barnes, B. J., Caffrey, D. R., Visintin, A., Latz, E., et al. (2003b). LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198, 1043-1055. doi: 10.1084/jem.20031023
37. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Ozoren, 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
38. Franchi, L., Munoz-Planillo, R., and Nunez, G. (2012). Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 13, 325-332. doi: 10.1038/ni.2231
39. Fuertes Marraco, S. A., Scott, C. L., Bouillet, P., Ives, A., Masina, S., Vremec, D., et al. (2011). Type I interferon drives dendritic cell apoptosis via multiple BH3-only proteins following activation by PolyIC in vivo. PLoS ONE 6:e20189. doi: 10.1371/journal.pone.0020189
40. Galluzzi, L., Kepp, O., Morselli, E., Vitale, I., Senovilla, L., Pinti, M., et al. (2010). Viral strategies for the evasion of immunogenic cell death. J. Intern. Med. 267, 526-542. doi: 10.1111/j.1365-2796.2010.02223.x
41. Gavrilin, M. A., and Wewers, M. D. (2011). Francisella recognition by inflammasomes: differences between mice and men. Front. Microbiol. 2:11. doi: 10.3389/fmicb.2011.00011
42. Giosue, S., Casarini, M., Alemanno, L., Galluccio, G., Mattia, P., Pedicelli, G., et al. (1998). Effects of aerosolized interferon-alpha in patients with pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 158, 1156-1162. doi: 10.1164/ajrccm.158.4.9803065
43. Gold, J. A., Hoshino, Y., Jones, M. B., Hoshino, S., Nolan, A., and Weiden, M. D. (2007). Exogenous interferon-alpha and interferon-gamma increase lethality of murine inhalational anthrax. PLoS ONE 2:e736. doi: 10.1371/journal.pone.0000736
44. Gonzalez-Navajas, J. M., Lee, J., David, M., and Raz, E. (2012). Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12, 125-135. doi: 10.1038/nri3133
45. Gregory, S. M., Davis, B. K., West, J. A., Taxman, D. J., Matsuzawa, S., Reed, J. C., et al. (2011). Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331, 330-334. doi: 10.1126/science.1199478
46. Guarda, G., Braun, M., Staehli, F., Tardivel, A., Mattmann, C., Forster, I., et al. (2011). Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34, 213-223. doi: 10.1016/j.immuni.2011.02.006
47. Gurung, P., Malireddi, R. K., Anand, P. K., Demon, D., Walle, L. V., Liu, Z., et al. (2012). Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-beta (TRIF)-mediated caspase-11 protease production integrates Toll-like receptor 4 (TLR4) protein- and Nlrp3 inflammasome-mediated host defense against enteropathogens. J. Biol. Chem. 287, 34474-34483. doi: 10.1074/jbc.M112.401406
48. 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
49. Havell, E. A. (1986). Augmented induction of interferons during Listeria monocytogenes infection. J. Infect. Dis. 153, 960-969. doi: 10.1093/infdis/153.5.960
50. Henry, T., Brotcke, A., Weiss, D. S., Thompson, L. J., and Monack, D. M. (2007). Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J. Exp. Med. 204, 987-994. doi: 10.1084/jem.20062665
51. Henry, T., and Monack, D. M. (2007). Activation of the inflammasome upon Francisella tularensis infection: interplay of innate immune pathways and virulence factors. Cell Microbiol. 9, 2543-2551. doi: 10.1111/j.1462-5822.2007.01022.x
52. Hertzog, P. J., and Williams, B. R. (2013). Fine tuning type i interferon responses. Cytokine Growth Factor Rev. 24, 217-225. doi: 10.1016/j.cytogfr.2013.04.002
53. Hogner, K., Wolff, T., Pleschka, S., Plog, S., Gruber, A. D., Kalinke, U., et al. (2013). Macrophage-expressed IFN-beta contributes to apoptotic alveolar epithelial cell injury in severe influenza virus pneumonia. PLoS Pathog. 9:e1003188. doi: 10.1371/journal.ppat.1003188
54. Huys, L., Van Hauwermeiren, F., Dejager, L., Dejonckheere, E., Lienenklaus, S., Weiss, S., et al. (2009). Type I interferon drives tumor necrosis factor-induced lethal shock. J. Exp. Med. 206, 1873-1882. doi: 10.1084/jem.20090213
55. Inglis, D. O., Berkes, C. A., Hocking Murray, D. R., and Sil, A. (2010). Conidia but not yeast cells of the fungal pathogen Histoplasma capsulatum trigger a type I interferon innate immune response in murine macrophages. Infect. Immun. 78, 3871-3882. doi: 10.1128/IAI.00204-10
56. Ishikawa, H., Ma, Z., and Barber, G. N. (2009). STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792. doi: 10.1038/nature08476
57. Jensen, J., and Balish, E. (1993). Enhancement of susceptibility of CB-17 mice to systemic candidiasis by poly(I. C)-induced interferon. Infect. Immun. 61, 3530-3532.
58. Jensen, J., Vazquez-Torres, A., and Balish, E. (1992). Poly(I.C)-induced interferons enhance susceptibility of SCID mice to systemic candidiasis. Infect. Immun. 60, 4549-4557.
59. Jones, J. W., Kayagaki, N., Broz, P., Henry, T., Newton, K., O'Rourke, K., et al. (2010). Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U.S.A. 107, 9771-9776. doi: 10.1073/pnas.1003738107
60. Joyce, E. A., Popper, S. J., and Falkow, S. (2009). Streptococcus pneumoniae nasopharyngeal colonization induces type I interferons and interferon-induced gene expression. BMC Genomics 10:404. doi: 10.1186/1471-2164-10-404
61. Kaminskyy, V., and Zhivotovsky, B. (2010). To kill or be killed: how viruses interact with the cell death machinery. J. Intern. Med. 267, 473-482. doi: 10.1111/j.1365-2796.2010.02222.x
62. Kanneganti, T. D. (2010). Central roles of NLRs and inflammasomes in viral infection. Nat. Rev. Immunol. 10, 688-698. doi: 10.1038/nri2851
63. Kanneganti, T. D., Body-Malapel, M., Amer, A., Park, J. H., Whitfield, J., Franchi, L., et al. (2006a). Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281, 36560-36568. doi: 10.1074/jbc.M607594200
64. Kanneganti, T. D., Ozoren, N., Body-Malapel, M., Amer, A., Park, J. H., Franchi, L., et al. (2006b). Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440, 233-236. doi: 10.1038/nature04517
65. Kaplan, A., Ma, J., Kyme, P., Wolf, A. J., Becker, C. A., Tseng, C. W., et al. (2012). Failure to induce IFN-beta production during Staphylococcus aureus infection contributes to pathogenicity. J. Immunol. 189, 4537-4545. doi: 10.4049/jimmunol.1201111
66. Karaghiosoff, M., Steinborn, R., Kovarik, P., Kriegshauser, G., Baccarini, M., Donabauer, B., et al. (2003). Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat. Immunol. 4, 471-477. doi: 10.1038/ni910
67. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., et al. (2011). Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121. doi: 10.1038/nature10558
68. Kayagaki, N., Wong, M. T., Stowe, I. B., Ramani, S. R., Gonzalez, L. C., Akashi-Takamura, S., et al. (2013). Non-canonical inflammasome activation by intracellular LPS independent of TLR4. Science 341, 1246-1249. doi: 10.1126/science.1240248
69. Kerur, N., Veettil, M. V., Sharma-Walia, N., Bottero, V., Sadagopan, S., Otageri, P., et al. (2011). IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9, 363-375. doi: 10.1016/j.chom.2011.04.008
70. Kibler, K. V., Shors, T., Perkins, K. B., Zeman, C. C., Banaszak, M. P., Biesterfeldt, J., et al. (1997). Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells. J. Virol. 71, 1992-2003.
71. Kim, S., Bauernfeind, F., Ablasser, A., Hartmann, G., Fitzgerald, K. A., Latz, E., et al. (2010). Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. Eur. J. Immunol. 40, 1545-1551. doi: 10.1002/eji.201040425
72. Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., et al. (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Jama 298, 1763-1771. doi: 10.1001/jama.298.15.1763
73. 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
74. Kotredes, K. P., and Gamero, A. M. (2013). Interferons as inducers of apoptosis in malignant cells. J. Interferon Cytokine Res. 33, 162-170. doi: 10.1089/jir.2012.0110
75. Liljeroos, M., Vuolteenaho, R., Rounioja, S., Henriques-Normark, B., Hallman, M., and Ojaniemi, M. (2008). Bacterial ligand of TLR2 signals Stat activation via induction of IRF1/2 and interferon-alpha production. Cell Signal 20, 1873-1881. doi: 10.1016/j.cellsig.2008.06.017
76. Lindgren, S. W., Stojiljkovic, I., and Heffron, F. (1996). Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc. Natl. Acad. Sci. U.S.A. 93, 4197-4201. doi: 10.1073/pnas.93.9.4197
77. Lippmann, J., Muller, H. C., Naujoks, J., Tabeling, C., Shin, S., Witzenrath, M., et al. (2011). Dissection of a type I interferon pathway in controlling bacterial intracellular infection in mice. Cell Microbiol. 13, 1668-1682. doi: 10.1111/j.1462-5822.2011.01646.x
78. Liu, Y. J. (2005). IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23, 275-306. doi: 10.1146/annurev.immunol.23.021704.115633
79. Lizak, M., and Yarovinsky, T. O. (2012). Phospholipid scramblase 1 mediates type i interferon-induced protection against staphylococcal alpha-toxin. Cell Host Microbe 11, 70-80. doi: 10.1016/j.chom.2011.12.004
80. Lupfer, C. R., and Kanneganti, T. D. (2012). The role of inflammasome modulation in virulence. Virulence 3, 262-270. doi: 10.4161/viru.20266
81. MacMicking, J. D. (2012). Interferon-inducible effector mechanisms in cell-autonomous immunity. Nat. Rev. Immunol. 12, 367-382. doi: 10.1038/nri3210
82. Majer, O., Bourgeois, C., Zwolanek, F., Lassnig, C., Kerjaschki, D., Mack, M., et al. (2012). Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog. 8:e1002811. doi: 10.1371/journal.ppat.1002811
83. Manca, C., Tsenova, L., Bergtold, A., Freeman, S., Tovey, M., Musser, J. M., et al. (2001). Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc. Natl. Acad. Sci. U.S.A. 98, 5752-5757. doi: 10.1073/pnas.091096998
84. Mariathasan, S., Newton, K., Monack, D. M., Vucic, D., French, D. M., Lee, W. P., et al. (2004). Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218. doi: 10.1038/nature02664
85. Mariathasan, S., Weiss, D. S., Dixit, V. M., and Monack, D. M. (2005). Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202, 1043-1049. doi: 10.1084/jem.20050977
86. 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
87. Martin, F. J., Gomez, M. I., Wetzel, D. M., Memmi, G., O'Seaghdha, M., Soong, G., et al. (2009). Staphylococcus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J. Clin. Invest. 119, 1931-1939. doi: 10.1172/JCI35879
88. Masters, S. L., Gerlic, M., Metcalf, D., Preston, S., Pellegrini, M., O'Donnell, J. A., et al. (2012). NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity 37, 1009-1023. doi: 10.1016/j.immuni.2012.08.027
89. Mayer-Barber, K. D., Andrade, B. B., Barber, D. L., Hieny, S., Feng, C. G., Caspar, P., et al. (2011). Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 35, 1023-1034. doi: 10.1016/j.immuni.2011.12.002
90. 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
91. Miao, E. A., Ernst, R. K., Dors, M., Mao, D. P., and Aderem, A. (2008). Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. U.S.A. 105, 2562-2567. doi: 10.1073/pnas.0712183105
92. Moayeri, M., Crown, D., Newman, Z. L., Okugawa, S., Eckhaus, M., Cataisson, C., et al. (2010). Inflammasome sensor Nlrp1b-dependent resistance to anthrax is mediated by caspase-1, IL-1 signaling and neutrophil recruitment. PLoS Pathog. 6:e1001222. doi: 10.1371/journal.ppat.1001222
93. 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
94. Morens, D. M., Taubenberger, J. K., and Fauci, A. S. (2008). Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198, 962-970. doi: 10.1086/591708
95. Netea, M. G., Brown, G. D., Kullberg, B. J., and Gow, N. A. (2008). An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6, 67-78. doi: 10.1038/nrmicro1815
96. Nogueira, C. V., Lindsten, T., Jamieson, A. M., Case, C. L., Shin, S., Thompson, C. B., et al. (2009). Rapid pathogen-induced apoptosis: a mechanism used by dendritic cells to limit intracellular replication of Legionella pneumophila. PLoS Pathog. 5:e1000478. doi: 10.1371/journal.ppat.1000478
97. Novikov, A., Cardone, M., Thompson, R., Shenderov, K., Kirschman, K. D., Mayer-Barber, K. D., et al. (2011). Mycobacterium tuberculosis triggers host type I IFN signaling to regulate IL-1beta production in human macrophages. J. Immunol. 187, 2540-2547. doi: 10.4049/jimmunol.1100926
98. O'Connell, R. M., Saha, S. K., Vaidya, S. A., Bruhn, K. W., Miranda, G. A., Zarnegar, B., et al. (2004). Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 200, 437-445. doi: 10.1084/jem.20040712
99. Opitz, B., Vinzing, M., van Laak, V., Schmeck, B., Heine, G., Gunther, S., et al. (2006). Legionella pneumophila induces IFNbeta in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J. Biol. Chem. 281, 36173-36179. doi: 10.1074/jbc.M604638200
100. O'Riordan, M., Yi, C. H., Gonzales, R., Lee, K. D., and Portnoy, D. A. (2002). Innate recognition of bacteria by a macrophage cytosolic surveillance pathway. Proc. Natl. Acad. Sci. U.S.A. 99, 13861-13866. doi: 10.1073/pnas.202476699
101. Palmero, D., Eiguchi, K., Rendo, P., Castro Zorrilla, L., Abbate, E., and Gonzalez Montaner, L. J. (1999). Phase II trial of recombinant interferon-alpha2b in patients with advanced intractable multidrug-resistant pulmonary tuberculosis: long-term follow-up. Int. J. Tuberc. Lung Dis. 3, 214-218.
102. Pamer, E. G. (2004). Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4, 812-823. doi: 10.1038/nri1461
103. Pandey, A. K., Yang, Y., Jiang, Z., Fortune, S. M., Coulombe, F., Behr, M. A., et al. (2009). NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog. 5:e1000500. doi: 10.1371/journal.ppat.1000500
104. Parker, D., Cohen, T. S., Alhede, M., Harfenist, B. S., Martin, F. J., and Prince, A. (2012). Induction of type I interferon signaling by Pseudomonas aeruginosa is diminished in cystic fibrosis epithelial cells. Am. J. Respir. Cell Mol. Biol. 46, 6-13. doi: 10.1165/rcmb.2011-0080O
105. Parker, D., Martin, F. J., Soong, G., Harfenist, B. S., Aguilar, J. L., Ratner, A. J., et al. (2011). Streptococcus pneumoniae DNA initiates type I interferon signaling in the respiratory tract. MBio 2, e00016-e00011. doi: 10.1128/mBio.00016-11
106. Pestka, S., Krause, C. D., and Walter, M. R. (2004). Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202, 8-32. doi: 10.1111/j.0105-2896.2004.00204.x
107. Platanias, L. C. (2005). Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5, 375-386. doi: 10.1038/nri1604
108. Poeck, H., Bscheider, M., Gross, O., Finger, K., Roth, S., Rebsamen, M., et al. (2010). Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat. Immunol. 11, 63-69. doi: 10.1038/ni.1824
109. 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. doi: 10.1084/jem.167.4.1459
110. Pothlichet, J., Meunier, I., Davis, B. K., Ting, J. P., Skamene, E., von Messling, V., et al. (2013). Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog. 9:e1003256. doi: 10.1371/journal.ppat.1003256
111. Power, M. R., Li, B., Yamamoto, M., Akira, S., and Lin, T. J. (2007). A role of Toll-IL-1 receptor domain-containing adaptor-inducing IFN-beta in the host response to Pseudomonas aeruginosa lung infection in mice. J. Immunol. 178, 3170-3176.
112. 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.
113. Rathinam, V. A., Jiang, Z., Waggoner, S. N., Sharma, S., Cole, L. E., Waggoner, L., et al. (2010). The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395-402. doi: 10.1038/ni.1864
114. Rathinam, V. A., Vanaja, S. K., Waggoner, L., Sokolovska, A., Becker, C., Stuart, L. M., et al. (2012). TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150, 606-619. doi: 10.1016/j.cell.2012.07.007
115. Rayamajhi, M., Humann, J., Penheiter, K., Andreasen, K., and Lenz, L. L. (2010). Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J. Exp. Med. 207, 327-337. doi: 10.1084/jem.20091746
116. Reich, N. C. (2013). A death-promoting role for ISG54/IFIT2. J. Interferon Cytokine Res. 33, 199-205. doi: 10.1089/jir.2012.0159
117. Reimer, T., Schweizer, M., and Jungi, T. W. (2007). Type I IFN induction in response to Listeria monocytogenes in human macrophages: evidence for a differential activation of IFN regulatory factor 3 (IRF3). J. Immunol. 179, 1166-1177.
118. Robinson, N., McComb, S., Mulligan, R., Dudani, R., Krishnan, L., and Sad, S. (2012). Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat. Immunol. 13, 954-962. doi: 10.1038/ni.2397
119. Roquilly, A., Gautreau, L., Segain, J. P., de Coppet, P., Sebille, V., Jacqueline, C., et al. (2010). CpG-ODN and MPLA prevent mortality in a murine model of post-hemorrhage-Staphyloccocus aureus pneumonia. PLoS ONE 5:e13228. doi: 10.1371/journal.pone.0013228
120. Roy, S., Bonfield, T., and Tartakoff, A. M. (2013). Non-apoptotic toxicity of Pseudomonas aeruginosa toward murine cells. PLoS ONE 8:e54245. doi: 10.1371/journal.pone.0054245
121. Rusinova, I., Forster, S., Yu, S., Kannan, A., Masse, M., Cumming, H., et al. (2013). Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res. 41, D1040-D1046. doi: 10.1093/nar/gks1215
122. Sander, L. E., Davis, M. J., Boekschoten, M. V., Amsen, D., Dascher, C. C., Ryffel, B., et al. (2011). Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474, 385-389. doi: 10.1038/nature10072
123. Sato, S., Sugiyama, M., Yamamoto, M., Watanabe, Y., Kawai, T., Takeda, K., et al. (2003). Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171, 4304-4310.
124. Sauer, J. D., Witte, C. E., Zemansky, J., Hanson, B., Lauer, P., and Portnoy, D. A. (2010). Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7, 412-419. doi: 10.1016/j.chom.2010.04.004
125. Schiavoni, G., Mauri, C., Carlei, D., Belardelli, F., Pastoris, M. C., and Proietti, E. (2004). Type I IFN protects permissive macrophages from Legionella pneumophila infection through an IFN-gamma-independent pathway. J. Immunol. 173, 1266-1275.
126. Schmitz, F., Heit, A., Guggemoos, S., Krug, A., Mages, J., Schiemann, M., et al. (2007). Interferon-regulatory-factor 1 controls Toll-like receptor 9-mediated IFN-beta production in myeloid dendritic cells. Eur. J. Immunol. 37, 315-327. doi: 10.1002/eji.200636767
127. Shahangian, A., Chow, E. K., Tian, X., Kang, J. R., Ghaffari, A., Liu, S. Y., et al. (2009). Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J. Clin. Invest. 119, 1910-1920. doi: 10.1172/JCI35412
128. Skerrett, S. J., Wilson, C. B., Liggitt, H. D., and Hajjar, A. M. (2007). Redundant Toll-like receptor signaling in the pulmonary host response to Pseudomonas aeruginosa. Am. J. Physiol. Lung Cell Mol. Physiol. 292, L312-L322. doi: 10.1152/ajplung.00250.2006
129. Stetson, D. B., and Medzhitov, R. (2006a). Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24, 93-103. doi: 10.1016/j.immuni.2005.12.003
130. Stetson, D. B., and Medzhitov, R. (2006b). Type I interferons in host defense. Immunity 25, 373-381. doi: 10.1016/j.immuni.2006.08.007
131. Sutterwala, F. S., Mijares, L. A., Li, L., Ogura, Y., Kazmierczak, B. I., and Flavell, R. A. (2007). Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204, 3235-3245. doi: 10.1084/jem.20071239
132. Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., et al. (2006). Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327. doi: 10.1016/j.immuni.2006.02.004
133. Swiecki, M., Wang, Y., Vermi, W., Gilfillan, S., Schreiber, R. D., and Colonna, M. (2011). Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J. Exp. Med. 208, 2367-2374. doi: 10.1084/jem.20110654
134. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820. doi: 10.1016/j.cell.2010.01.022
135. Teijaro, J. R., Ng, C., Lee, A. M., Sullivan, B. M., Sheehan, K. C., Welch, M., et al. (2013). Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340, 207-211. doi: 10.1126/science.1235214
136. Teles, R. M., Graeber, T. G., Krutzik, S. R., Montoya, D., Schenk, M., Lee, D. J., et al. (2013). Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science 339, 1448-1453. doi: 10.1126/science.1233665
137. Terra, J. K., Cote, C. K., France, B., Jenkins, A. L., Bozue, J. A., Welkos, S. L., et al. (2010). Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J. Immunol. 184, 17-20. doi: 10.4049/jimmunol.0903114
138. Thomas, P. G., Dash, P., Aldridge, J. R. Jr., Ellebedy, A. H., Reynolds, C., Funk, A. J., et al. (2009). The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30, 566-575. doi: 10.1016/j.immuni.2009.02.006
139. Tsuchiya, K., Hara, H., Kawamura, I., Nomura, T., Yamamoto, T., Daim, S., et al. (2010). Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J. Immunol. 185, 1186-1195. doi: 10.4049/jimmunol.1001058
140. Vladimer, G. I., Weng, D., Paquette, S. W., Vanaja, S. K., Rathinam, V. A., Aune, M. H., et al. (2012). The NLRP12 inflammasome recognizes Yersinia pestis. Immunity 37, 96-107. doi: 10.1016/j.immuni.2012.07.006
141. Walberg, K., Baron, S., Poast, J., Schwartz, B., Izotova, L., Pestka, S., et al. (2008). Interferon protects mice against inhalation anthrax. J. Interferon Cytokine Res. 28, 597-601. doi: 10.1089/jir.2007.0143
142. 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
143. Warren, S. E., Mao, D. P., Rodriguez, A. E., Miao, E. A., and Aderem, A. (2008). Multiple Nod-like receptors activate caspase 1 during Listeria monocytogenes infection. J. Immunol. 180, 7558-7564.
144. Weigent, D. A., Huff, T. L., Peterson, J. W., Stanton, G. J., and Baron, S. (1986). Role of interferon in streptococcal infection in the mouse. Microb. Pathog. 1, 399-407. doi: 10.1016/0882-4010(86)90071-9
145. Wilson, E. B., Yamada, D. H., Elsaesser, H., Herskovitz, J., Deng, J., Cheng, G., et al. (2013). Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340, 202-207. doi: 10.1126/science.1235208
146. Woodward, J. J., Iavarone, A. T., and Portnoy, D. A. (2010). c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328, 1703-1705. doi: 10.1126/science.1189801
147. Worthington, M., and Hasenclever, H. (1972). Effect of an interferon stimulator, polyinosinic: polycytidylic acid, on experimental fungus infections. Infect. Immun. 5, 199-202.
148. Wu, J., Fernandes-Alnemri, T., and Alnemri, E. S. (2010). Involvement of the AIM2, NLRC4, and NLRP3 inflammasomes in caspase-1 activation by Listeria monocytogenes. J. Clin. Immunol. 30, 693-702. doi: 10.1007/s10875-010-9425-2
149. Wu, K., Dong, D., Fang, H., Levillain, F., Jin, W., Mei, J., et al. (2012). An interferon-related signature in the transcriptional core response of human macrophages to Mycobacterium tuberculosis infection. PLoS ONE 7:e38367. doi: 10.1371/journal.pone.0038367
150. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., et al. (2003). Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643. doi: 10.1126/science.1087262
151. 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
152. Zhuo, H., Yang, K., Lynch, S. V., Dotson, R. H., Glidden, D. V., Singh, G., et al. (2008). Increased mortality of ventilated patients with endotracheal Pseudomonas aeruginosa without clinical signs of infection. Crit. Care Med. 36, 2495-2503. doi: 10.1097/CCM.0b013e318183f3f8