Bacterial programming of host responses: Coordination between type I interferon and cell death

Frontiers in Microbiology

Volumn 5, Issue OCT, 2014, Pages

  Dhariwala, Miqdad O ^a   Anderson, Deborah M ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Bacterial infection; Cell death; Francisella; Listeria; Plague; Salmonella; Type I interferon; Yersinia

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; CASPASE 11; INFLAMMASOME; INTERFERON; INTERLEUKIN 1BETA CONVERTING ENZYME; LISTERIOLYSIN O; MEMBRANE PROTEIN; TOLL LIKE RECEPTOR 4;

BACTERIAL GENETICS; CELL DEATH; DENDRITIC CELL; ENZYME ACTIVATION; FRANCISELLA; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SALMONELLA; SIGNAL TRANSDUCTION; YERSINIA PESTIS;

EID: 84987829322     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00545     Document Type: Review

References (127)

1. Amer, A., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Ozoren, N., Brady, G., et al. (2006). Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281, 35217-35223. doi: 10.1074/jbc.M604933200
2. Auerbuch, V., Brockstedt, D., Meyer-Morse, N., O'riordan, M., and Portnoy, D. (2004). Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200, 527-533. doi: 10.1084/jem.20040976
3. Bauler, T., Chase, J., and Bosio, C. (2011). IFN-β mediates suppression of IL-12p40 in human dendritic cells following infection with virulenr Francisella tularensis. J. Immunol. 187, 1845-1855. doi: 10.4049/jimmunol.1100377
4. Biswas, P., Pedicord, V., Ploss, A., Menet, E., Leiner, I., and Pamer, E. (2007). Pathogen-specific CD8 T cell responses are directly inhibited by IL-10. J. Immunol. 179, 4520-4528. doi: 10.4049/jimmunol.179.7.4520
5. Bosio, C., Bielefeldt-Ohmann, H., and Belisle, J. (2007). Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J. Immunol. 178.
6. Brodsky, I., and Medzhitov, R. (2008). Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 4:1-14. doi: 10.1371/journal.ppat.1000067
7. Brodsky, I., Palm, N., Sadanand, S., Ryndak, M., Sutterwala, F., Flavell, R., et al. (2010). A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7, 376-387. doi: 10.1016/j.chom.2010.04.009
8. Bröms, J., Lavander, M., Meyer, L., and Sjöstedt, A. (2011). IglG and IglI of the Francisella pathogenicity island are important virulence determinants of Francisella tularensis LVS. Infect. Immun. 79, 3683-3696. doi: 10.1128/IAI.01344-10
9. Broms, J., Sjöstedt, A., and Lavander, M. (2010). The role of the Francisella tularensis pathogenicity island in type VI secretion, intracellular survival, and modulation of host cell signaling. Front. Microbiol. 1:136. doi: 10.3389/fmicb.2010.00136
10. Browne, S., Lesnick, M., and Guiney, D. (2002). Genetic requirements for Salmonella-induced cytopathology in human monocyte-derived macrophages. Infect. Immun. 70, 7126-7135. doi: 10.1128/IAI.70.12.7126-7135.2002
11. Broz, P., Newton, K., Lamkanfi, M., Mariathasan, S., Dixit, V., and Monack, D. (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
12. Broz, P., Ruby, T., Belhocine, K., Bouley, D., Kayagaki, N., Dixit, V., et al. (2012). Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490, 288-291. doi: 10.1038/nature11419
13. Burdette, D., and Vance, R. (2013). STING and the innate immune response to nucleic acids in the cytosol. Nat. Immunol. 14, 19-26. doi: 10.1038/ni.2491
14. Butler, T. (2013). Plague gives surprises in the first decade of the 21st century in the United States and worldwide. Am. J. Trop. Med. Hyg. 89, 788-793. doi: 10.4269/ajtmh.13-0191
15. Carrero, J., Calderon, B., and Unanue, E. (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
16. Carrero, J., and Calderon, B. U., and Unanue, E. R. (2006). Lymphocytes are detrimental during the early innate immune response against Listeria monocytogenes. J. Exp. Med. 203, 933-940. doi: 10.1084/jem.20060045
17. Carrigan, S., Junkins, R., Yang, Y., 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
18. Chen, M., Gan, H., and Remold, H. G. (2006). A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J. Immunol. 176, 3707-3716. doi: 10.4049/jimmunol.176.6.3707
19. Colino, J., and Snapper, C. M. (2003). Two distinct mechanisms for induction of dendritic cell apoptosis in response to intact Streptococcus pneumoniae. J. Immunol. 171, 2354-2365. doi: 10.4049/jimmunol.171.5.2354
20. Cornelis, G. (2006). The Type III injectisome. Nat. Rev. Microbiol. 4, 811-825. doi: 10.1038/nrmicro1526
21. de Veer, M., Holko, M., Frevel, M., Walker, E., Der, S., Paranjape, J., et al. (2001). Functional classification of interferon-stimulated genes identified using microarrays. J. Leuk. Biol. 69, 912-920.
22. de Weerd, N., Vivian, J., Nguyen, T., Mangan, N., Gould, J., Braniff, S., et al. (2013). Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1. Nat. Immunol. 14, 901-907. doi: 10.1038/ni.2667
23. Decker, T., Muller, M., and Stockinger, S. (2005). The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 5, 675-687. doi: 10.1038/nri1684
24. Dennis, D., Inglesby, T., Henderson, D., Bartlett, J., Ascher, M., Eitzen, E., et al. (2002). Tularemia as a biological weapon. JAMA 285, 2763-2773. doi: 10.1001/jama.285.21.2763
25. Dorhoi, A., Yeremeev, V., Nouailles, G., Weiner, J., Jörg, S., Heinemann, E., et al. (2014). Type I IFN signaling triggers immunopathology in tuberculosis susceptible mice by modulating lung phagocyte dynamics. Eur. J. Immunol. 44, 2380-2393. doi: 10.1002/eji.201344219
26. Dotson, R., Rabadi, S., Westcott, E., Bradley, S., Catlett, S., Banik, S., et al. (2013). Repression of inflammasome by Francisella tularensis during early stages of infection. J. Biol. Chem. 288, 23844-23857. doi: 10.1074/jbc.M113.490086
27. Du, Z., Yang, H., Tan, Y., Tian, G., Zhang, Q., Cui, Y., et al. (2014). Transcriptomic response to Yersinia pestis: RIG-I like receptor signaling response is detrimental to the host against plague. J. Genet. Genomics 41, 379-396. doi: 10.1016/j.jgg.2014.05.006
28. Eisele, N., Lee-Lewis, H., Besch-Williford, C., Brown, C., and Anderson, D. (2011). Chemokine receptor CXCR2 mediates bacterial clearance rather than neutrophil recruitment in a murine model of pneumonic plague. Am. J. Pathol. 178, 1190-1200. doi: 10.1016/j.ajpath.2010.11.067
29. Fàbrega, A., and Vilaa, J. (2013). Salmonella enterica serovar typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev. 26, 308-341. doi: 10.1128/CMR.00066-12
30. 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
31. Feng, H., Zhang, D., Palliser, D., Zhu, P., Cai, S., Schlesinger, A., et al. (2005). Listeria-infected myeloid dendritic cells produce IFN-beta, priming T cell activation. J. Immunol. 175, 421-432. doi: 10.4049/jimmunol.175.1.421
32. Fernandes-Alnemri, T., Yu, J., Juliana, C., Solorzano, L., Kang, S., Wu, J., et al. (2010). The AIM2 inflammasome is critical for innate immunity against Francisella tularensis. Nat. Immunol. 11, 385-393. doi: 10.1038/ni.1859
33. Foley, J. E., and Nieto, N. C. (2010). Tularemia. Vet. Microbiol. 140, 332-338. doi: 10.1016/j.vetmic.2009.07.017
34. García-del Portillo, F. (2001). Salmonella intracellular proliferation: where, when and how? Microbes Infect. 3, 1305-1311. doi: 10.1016/S1286-4579(01)01491-5
35. Grabenstein, J., Marceau, M., Pujol, C., Simonet, M., and Bliska, J. (2004). The response regulator PhoP of Yersinia pseudotubeculosis is important for replication in macrophages and for virulence. Infect. Immun. 72, 4973-4984. doi: 10.1128/IAI.72.9.4973-4984.2004
36. Hall, J., Woolard, M., Gunn, B., Craven, R., Taft-Benz, S., Frelinger, J., et al. (2008). Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis SchuS4, LVS, or U112. Infect. Immun. 76, 5843-5852. doi: 10.1128/IAI.01176-08
37. Heine, H., Chuvala, L., Riggins, R., Hurteau, G., Cirz, R., Cass, R., et al. (2013). Natural history of Yersinia pestis pneumonia in aerosol-challenged BALB/c mice. Antimicrob. Agents Chemother. 57, 2010-2015. doi: 10.1128/AAC.02504-12
38. Henry, T., Brotcke, A., Weiss, D., Thompson, L., and Monack, D. (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
39. Henry, T., Kirimanjeswara, G., Ruby, T., Jones, J., Peng, K., Perret, M., et al. (2010). Type I IFN signaling constrains IL-17A/F secretion by gamma-delta T cells during bacterial infections. J. Immunol. 184, 3755-3767. doi: 10.4049/jimmunol.0902065
40. Holmstrom, A., Rosqvist, R., Wolf-Watz, H., and Forsberg, A. (1995). Virulence plasmid-encoded YopK is essential for Yersinia pseudotuberculosis to cause systemic infection in mice. Infect. Immun. 63, 2269-2276.
41. Ireland, R., Wang, R., Alinger, J., Small, P., and Bosio, C. (2013). Francisella tularensis SchuS4 and SchuS4 lipids inhibit IL-12p40 in primary human dendritic cells by inhibition of IRF1 and IRF8. J. Immunol. 191, 1276-1286. doi: 10.4049/jimmunol.1300867
42. Ivashkiv, L., and Donlin, L. (2014). Regulation of type I interferon responses. Nat. Rev. Immunol. 14, 36-49. doi: 10.1038/nri3581
43. Jin, L., Hill, K., Filak, H., Mogan, J., Knowles, H., Zhang, B., et al. (2011a). 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. 187, 2595-2601. doi: 10.4049/jimmunol.1100088
44. Jin, L., Hill, K. K., Filak, H., Mogan, J., Knowles, H., Zhang, B., et al. (2011b). 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. 187, 2595-2601. doi: 10.4049/jimmunol.1100088
45. Jones, J., 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
46. Jones, J. V. V., Broz, P., and Monack, D. M. (2011). Innate immune recognition of Francisella tularensis: activation of type-I interferons and the inflammasome. Front. Microbiol. 2:16. doi: 10.3389/fmicb.2011.00016
47. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B., and Matsuura, M. (2002). Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70, 4092-4098. doi: 10.1128/IAI.70.8.4092-4098.2002
48. Ke, Y., Chen, Z., and Yang, R. (2013). Yersinia pestis: mechanisms of entry into and resistance to the host cell. Front. Cell. Infect. Microbiol. 3:106. doi: 10.3389/fcimb.2013.00106
49. Koo, I. C., Wang, C., Raghavan, S., Morisaki, J. H., Cox, J. S., and Brown, E. J. (2008). ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell. Microbiol. 10, 1866-1878. doi: 10.1111/j.1462-5822.2008.01177.x
50. Laws, T., Davey, M., Titball, R., and Lukaszewski, R. (2010). Neutrophils are important in early control of lung infection by Yersinia pestis. Microbes Infect. 12, 331-335. doi: 10.1016/j.micinf.2010.01.007
51. Lemaitre, N., Sebbane, F., Long, D., and Hinnebusch, B. (2006). Yersinia pestis YopJ suppresses tumor necrosis factor alpha induction and contributes to apoptosis of immune cells in the lymph node but is not required for virulence in a rat model of bubonic plague. Infect. Immun. 74, 5126-5131. doi: 10.1128/IAI.00219-06
52. Libby, S., Adams, L., Ficht, T., Allen, C., Whitford, H., Buchmeier, N., et al. (1997). The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host. Infect. Immun. 65, 1786-1792.
53. 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
54. Lindemann, S., Peng, K., Long, M., Hunt, J., Apicella, M., Monack, D., et al. (2011). Francisella tularensis SchuS4 O-antigen and capsule biosynthesis gene mutants induce early cell death in human macrophages. Infect. Immun. 79, 581-594. doi: 10.1128/IAI.00863-10
55. Lindgren, M., Eneslätt, K., Bröms, J., and Sjöstedt, A. (2013). Importance of PdpC, IglC, IglI, and IglG for modulation of a host cell death pathway induced by Francisella tularensis. Infect. Immun. 81, 2076-2084. doi: 10.1128/IAI.00275-13
56. 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
57. Long, M., Lindemann, S., Rasmussen, J., Jones, B., and Allen, L. (2012). Disruption of Francisella tularensis Schu S4 iglI, iglJ, and pdpC genes results in attenuation for growth in human macrophages and in vivo virulence in mice and reveals a unique phenotype for pdpC. Infect. Immun. 81, 850-861. doi: 10.1128/IAI.00822-12
58. Maldonado-Arocho, F., Green, C., Fisher, M., Paczosa, M., and Mecsas, J. (2013). Adhesins and host serum factors drive Yop translocation by Yersinia into professional phagocytes during animal infection. PLoS Pathog. 9:e1003415. doi: 10.1371/journal.ppat.1003415
59. Mancuso, G., Gambuzza, M., Midiri, A., Biondo, C., Papasergi, S., Akira, S., et al. (2009). Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat. Immunol. 10, 587-594. doi: 10.1038/ni.1733
60. Manzanillo, P. S., Shiloh, M. U., Portnoy, D. A., and Cox, J. S. (2012). Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11, 469-480. doi: 10.1016/j.chom.2012.03.007
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. Marketon, M., Depaolo, R., Debord, K., Jabri, B., and Schneewind, O. (2005). Plague bacteria target immune cells during infection. Science 309, 1739-1741. doi: 10.1126/science.1114580
63. Martin, F., Gomez, M., Wetzel, D., Memmi, G., O'seaghdha, M., Soong, G., et al. (2009). Staphyloccus aureus activates type I IFN signaling in mice and humans through the Xr repeated sequences of protein A. J. Clin. Invest. 119, 1931-1939.
64. McCaffrey, R., Fawcett, P., O'riordan, M., Lee, K., Havell, E., Brown, P., et al. (2004). A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc. Natl. Acad. Sci. U.S.A. 101, 11386-11391. doi: 10.1073/pnas.0403215101
65. Mishra, B. B., Moura-Alves, P., Sonawane, A., Hacohen, N., Griffiths, G., Moita, L. F., et al. (2010). Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell. Microbiol. 12, 1046-1063. doi: 10.1111/j.1462-5822.2010.01450.x
66. Monack, D., Mecsas, J., Ghori, N., and Falkow, S. (1997). Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. U.S.A. 94, 10385-10390. doi: 10.1073/pnas.94.19.10385
67. Monroe, K., Mcwhirter, S., and Vance, R. (2009). Identification of host cytosolic sensors and bacterila factors regulating the type I interferon response to Legionella pneumophilea. PLoS Pathog. 5:e1000665. doi: 10.1371/journal.ppat.1000665
68. Montminy, S., Khan, N., Mcgrath, S., Walkowicz, M., Sharp, F., Conlon, J., et al. (2006). Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7, 1066-1073. doi: 10.1038/ni1386
69. N'Guessan, P. D., Schmeck, B., Ayim, A., Hocke, A. C., Brell, B., Hammerschmidt, S., et al. (2005). Streptococcus pneumoniae R6x induced p38 MAPK and JNK-mediated caspase-dependent apoptosis in human endothelial cells. Thromb. Haemost. 94, 295-303.
70. Navarini, A., Recher, M., Lang, K., Georgiev, P., Meury, S., Bergthaler, A., et al. (2006). Increased susceptibility to bacterial superinfection as a consequence of innate antiviral responses. Proc. Natl. Acad. Sci. U.S.A. 103, 15535-15539. doi: 10.1073/pnas.0607325103
71. 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.100047
72. O'Connell, R., Saha, S., Vaidya, S., Bruhn, K., Miranda, G., 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
73. Ochman, H., Soncini, F., Solomon, F., and Groisman, E. (1996). Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl. Acad. Sci. U.S.A. 93, 7800-7804. doi: 10.1073/pnas.93.15.7800
74. Orth, K., Palmer, L., Bao, Z., Stewart, S., Rudolph, A., Bliska, J., et al. (1999). Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285, 1920-1923. doi: 10.1126/science.285.5435.1920
75. Oyston, P., Dorrell, N., Williams, K., Shu-Rui, L., Green, M., Titball, R., et al. (2000). The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68, 3419-3425. doi: 10.1128/IAI.68.6.3419-3425.2000
76. Palmer, L. E., Hobbie, S., Galan, J. E., and Bliska, J. B. (1998). YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27, 953-965. doi: 10.1046/j.1365-2958.1998.00740.x
77. Pandey, A., Yang, Y., Jiang, Z., Fortune, S., Coulombe, F., Behr, M., 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
78. Panne, D., Maniatis, T., and Harrison, S. (2007). An atomic model of enhanceosome structure in the vicinity of DNA. Cell 129, 1111-1123. doi: 10.1016/j.cell.2007.05.019
79. 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.2011-0080OC
80. Parker, D., Martin, F., Soong, G., Harfenist, B., Aguilar, J., Ratner, A., et al. (2011). Streptococcus pneumoniae DNA initiates type I interferon signaling in the respiratory tract. MBio 2:e00016-00011. doi: 10.1128/mBio.00016-11
81. Parker, D., Planet, P. J., Soong, G., Narechania, A., and Prince, A. (2014). Induction of type I interferon signaling determines the relative pathogenicity of Staphylococcus aureus strains. PLoS Pathog. 10:e1003951. doi: 10.1371/journal.ppat.1003951
82. Parker, D., and Prince, A. (2012). Staphylococcus aureus induces type I IFN signaling in dendritic cells via TLR9. J. Immunol. 189, 4040-4046. doi: 10.4049/jimmunol.1201055
83. Parvatiyar, K., Zhang, Z., Teles, R., Ouyang, S., Jiang, Y., Iyer, S., et al. (2012). DDX41 recognizes bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat. Immunol. 13, 1155-1161. doi: 10.1038/ni.2460
84. Patel, A., Lee-Lewis, H., Hughes-Hanks, J., Lewis, C., and Anderson, D. (2012). Opposing roles for interferon regulatory factor-3 (IRF-3) and type I interferon signaling during plague. PLoS Pathog. 8:e1002817. doi: 10.1371/journal.ppat.1002817
85. Pechous, R., Sivaraman, V., Price, P., Stasulli, N., and Goldman, W. (2013). Early host cell targets of Yersinia pestis during primary pneumonic plague. PLoS Pathog. 9:e1003679. doi: 10.1371/journal.ppat.1003679
86. Peng, K., Broz, P., Jones, J., Joubert, L. M., and Monack, D. (2011). Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell. Microbiol. 13, 1586-1600. doi: 10.1111/j.1462-5822.2011.01643.x
87. Peters, K., Dhariwala, M., Hughes-Hanks, J., Brown, C., and Anderson, D. (2013). Early apoptosis of macrophages modulated by injection of Yersinia pestis YopK promotes progression of primary pneumonic plague. PLoS Pathog. 9:e1003324. doi: 10.1371/journal.ppat.1003324
88. Philip, N., Dillon, C., Snyder, A., Fitzgerald, P., Wynosky-Dolfi, M., Zwack, E., et al. (2014). Caspase-8 mediates caspase-1 processing and innate immune defense in response to bacterial blockade of NF-κB and MAPK signaling. Proc. Natl. Acad. Sci. U.S.A. 111, 7385-7390. doi: 10.1073/pnas.1403252111
89. Pierini, R., Perret, M., Djebali, S., Juruj, C., Michallet, M., Förster, I., et al. (2013). ASC controls IFN-γ levels in an IL-18-dependent manner in caspase-1-deficient mice infected with Francisella novicida. J. Immunol. 191, 3847-3857. doi: 10.4049/jimmunol.1203326
90. Pinto, A., Ramos, H., Wu, X., Aggarwal, S., Shrestha, B., Gorman, M., et al. (2014). Deficient IFN signaling by myeloid cells leads to MAVS-dependent virus-induced sepsis. PLoS Pathog. 10:e1004086. doi: 10.1371/journal.ppat.1004086
91. Plumlee, C., Lee, C., Berg, A., Decker, T., Shuman, H., and Schindler, C. (2009). Interferons direct an effective innate response to Legionella pneumophila infection. J. Biol. Chem. 284, 30058-30066. doi: 10.1074/jbc.M109.018283
92. Pollitzer, R. (1954). Plague. Geneva: World Health Organization.
93. 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. doi: 10.4049/jimmunol.178.5.3170
94. Price, P., Jin, J., and Goldman, W. (2012). Pulmonary infection by Yersinia pestis rapidly establishes a permissive environment for microbial proliferation. Proc. Natl. Acad. Sci. U.S.A. 109, 3083-3088. doi: 10.1073/pnas.1112729109
95. Rayamajhi, M., Humann, J., Penheiter, K., Andreasen, K., and Lenz, L. (2010). Induction of IFN-ab enables Listeria monocytogenes to suppress macrophage activation by IFN-g. J. Exp. Med. 207, 327-337. doi: 10.1084/jem.20091746
96. Raymond, B., Young, J., Pallett, M., Endres, R., Clements, A., and Frankel, G. (2013). Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 21, 430-441. doi: 10.1016/j.tim.2013.06.008
97. Rebeil, R., Ernst, R. K., Jarrett, C. O., Adams, K. N., Miller, S. I., and Hinnebusch, B. J. (2006). Characterization of late acyltransferase genes of Yersinia pestis and their role in temperature-dependent lipid a variation. J. Bacteriol. 188, 1381-1388. doi: 10.1128/JB.188.4.1381-1388.2006
98. Repasy, T., Lee, J., Marino, S., Martinez, N., Kirschner, D. E., Hendricks, G., et al. (2013). Intracellular bacillary burden reflects a burst size for Mycobacterium tuberculosis in vivo. PLoS Pathog. 9:e1003190. doi: 10.1371/journal.ppat.1003190
99. 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
100. Rosenberger, C., Scott, M., Gold, M., Hancock, R., and Finlay, B. (2000). Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J. Immunol. 164, 5894-5904. doi: 10.4049/jimmunol.164.11.5894
101. Rytkonen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., et al. (2007). SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. U.S.A. 104, 3502-3507. doi: 10.1073/pnas.0610095104
102. Santos, R. (2014). Pathobiology of Salmonella, intestinal microbiota, and the host innate immune response. Front. Immunol. 5:252. doi: 10.3389/fimmu.2014.00252
103. Sato, M., Hata, N., Asagiri, M., Nakaya, T., Taniguchi, T., and Tanaka, N. (1998). Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441, 106-110. doi: 10.1016/S0014-5793(98)01514-2
104. Schmolke, M., Patel, J., De Castro, E., Sánchez-Aparicio, M., Uccellini, M., Miller, J., et al. (2014). RIG-I Detects mRNA of intracellular Salmonella enterica serovar typhimurium during bacterial infection. MBio 5:e01006-01014. doi: 10.1128/mBio.01006-14
105. Schnupf, P., and Portnoy, D. (2007). Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9, 1176-1187. doi: 10.1016/j.micinf.2007.05.005
106. Schoggins, J., and Rice, C. (2011). Interferon-stimulated genes and their antiviral effector functions. Curr. Opin. Virol. 1, 519-525. doi: 10.1016/j.coviro.2011.10.008
107. Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821-832. doi: 10.1016/j.cell.2010.01.040
108. Schwartz, J., Barker, J., Kaufman, J., Fayram, D., Mccracken, J., and Allen, L. (2012). Francisella tularensis inhibits the intrinsic and extrinsic pathways to delay constitutive apoptosis and prolong human neutrophil lifespan. J. Immunol. 188, 3351-3363. doi: 10.4049/jimmunol.1102863
109. Shah, S., Bohsali, A., Ahlbrand, S., Srinivasan, L., Rathinam, V., Vogel, S., et al. (2013). Cutting edge: Mycobacterium tuberculosis but not nonvirulent mycobacteria inhibits IFN-β and AIM2 inflammasome-dependent IL-1β production via its ESX-1 secretion system. J. Immunol. 191, 3514-3518. doi: 10.4049/jimmunol.1301331
110. Skyberg, J., Rollins, M., Samuel, J., Sutherland, M., Belisle, J., and Pascual, D. (2013). Interleukin-17 protects against the Francisella tularensis live vaccine strain but not against a virulent F. tularensis type A strain. Infect. Immun. 81, 3099-3105. doi: 10.1128/IAI.00203-13
111. Stark, G., Kerr, I., Williams, B., Silverman, R., and Schreiber, R. (1998). How cells respond to interferons. Ann. Rev. Biochem. 67, 227-264. doi: 10.1146/annurev.biochem.67.1.227
112. 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
113. Sweet, C., Conlon, J., Golenbock, D., Goguen, J., and Silverman, N. (2007). YopJ targets TRAF proteins to inhibit TLR-mediated NF-kB, MAPK and IRF3 signal transduction. Cell. Microbiol. 9, 2700-2715. doi: 10.1111/j.1462-5822.2007.00990.x
114. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820. doi: 10.1016/j.cell.2010.01.022
115. Torres, D., Barrier, M., Bihl, F., Quesniaux, V., Maillet, I., Akira, S., et al. (2004). Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 72, 2131-2139. doi: 10.1128/IAI.72.4.2131-2139.2004
116. Valdimer, G., Weng, D., Paquette, S., Vanaja, S., Rathinam, V., Aune, M., et al. (2012). The NLRP12 inflammasome recognizes Yersinia pestis. Immunity 37, 96-107. doi: 10.1016/j.immuni.2012.07.006
117. Vega-Ramos, J., Alari-Pahissa, E., Del Valle, J., Carrasco-Marin, E., Esplugues, E., Borras, M., et al. (2010). CD69 limits early inflammatory diseases associated with immune response to Listeria monocytogenes infection. Immunol. Cell Biol. 88, 707-715. doi: 10.1038/icb.2010.62
118. 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
119. Weng, D., Marty-Roix, R., Ganesan, S., Proulx, M. K., Vladimer, G. I., Kaiser, W. J., et al. (2014). Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death. Proc. Natl. Acad. Sci. U.S.A. 111, 7391-7396. doi: 10.1073/pnas.1403477111
120. Winter, S., Thiennimitr, P., Winter, M., Butler, B., Huseby, D., Crawford, R., et al. (2010). Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426-429. doi: 10.1038/nature09415
121. Woodward, J., Iavarone, A., and Portnoy, D. (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
122. Wyant, T., Tanner, M., and Sztein, M. (1999). Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect. Immun. 67, 3619-3624.
123. Zauberman, A., Tidhar, A., Levy, Y., Bar-Haim, E., Halperin, G., Flashner, Y., et al. (2009). Yersinia pestis endowed with increased cytotoxicity is avirulent in a bubonic plague model and induces rapid protection against pneumonic plague. PLoS ONE 4:e5938. doi: 10.1371/journal.pone.0005938
124. Zhang, Y., Romanov, G., and Bliska, J. (2011). Type III secretion system-dependent translocation of ectopically expressed Yop effectors into macrophages by intracellular Yersinia pseudotuberculosis. Infect. Immun. 79, 4322-4331. doi: 10.1128/IAI.05396-11
125. Zheng, Y., Lilo, S., Brodsky, I., Zhang, Y., Medzhitov, R., Marcu, K., et al. (2011). A Yersinia effector with enhanced inhibitory activity on the NF-κB pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages. PLoS Pathog. 7:e1002026. doi: 10.1371/journal.ppat.1002026
126. Zhou, H., Monack, D., Kayagaki, N., Wertz, I., Yin, J., Wolf, B., et al. (2005). Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J. Exp. Med. 202, 1327-1332. doi: 10.1084/jem.20051194
127. Zwaferink, H., Stockinger, S., Hazemi, P., Lemmens-Gruber, R., and Decker, T. (2008). IFN-β increases Listeriolysin O-induced membrane permeabilization and death of macrophages. J. Immunol. 180, 4116-4123. doi: 10.4049/jimmunol.180.6.4116