The inflammasome: Learning from bacterial evasion strategies

Seminars in Immunology

Volumn 27, Issue 2, 2015, Pages 102-110

  Shin, Sunny ^a   Brodsky, Igor E ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Caspase 1; Inflammasome; Microbial evasion; Salmonella; Yersinia

Indexed keywords

ANTIVIRUS AGENT; CASPASE 11; CRYOPYRIN; FLAGELLIN; INFLAMMASOME; PHOSPHOLIPASE; PATTERN RECOGNITION RECEPTOR;

ACTIN FILAMENT; BACTERIAL EVASION; BACTERIAL VIRULENCE; DOWN REGULATION; ENZYME ACTIVITY; GRAM NEGATIVE BACTERIUM; IMMUNE EVASION; INFLAMMATORY DISEASE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; REVIEW; SHIGELLA; TOXOPLASMOSIS; YERSINIA; ANIMAL; BACTERIAL INFECTION; BACTERIUM; HUMAN; IMMUNOLOGY;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; HUMANS; IMMUNE EVASION; INFLAMMASOMES; RECEPTORS, PATTERN RECOGNITION;

EID: 84931567250     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2015.03.006     Document Type: Review

References (141)

1. Janeway C.A. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 1989, 54 Pt 1:1-13.
2. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
3. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
4. Gurcel L., Abrami L., Girardin S., Tschopp J., van der Goot F.G. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 2006, 126:1135-1145.
5. Lamkanfi M., Dixit V.M. Inflammasomes: guardians of cytosolic sanctity. Immunol. Rev. 2009, 227:95-105.
6. Lamkanfi M., Dixit V.M. Mechanisms and functions of inflammasomes. Cell 2014, 157:1013-1022.
7. Davis B.K., Wen H., Ting J.P. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 2011, 29:707-735.
8. Faustin B., Lartigue L., Bruey J.M., Luciano F., Sergienko E., Bailly-Maitre B., et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 2007, 25:713-724.
9. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 2002, 10:417-426.
10. Lu A., Magupalli V.G., Ruan J., Yin Q., Atianand M.K., Vos M.R., et al. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 2014, 156:1193-1206.
11. Dostert C., Petrilli V., Van Bruggen R., Steele C., Mossman B.T., Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008, 320:674-677.
12. Hornung V., Latz E. Critical functions of priming and lysosomal damage for NLRP3 activation. Eur. J. Immunol. 2010, 40:620-623.
13. Kahlenberg J.M., Dubyak G.R. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am. J. Physiol. Cell Physiol. 2004, 286:C1100-C1108.
14. Kanneganti T.D., Body-Malapel M., Amer A., Park J.H., Whitfield J., Franchi L., et al. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 2006, 281:36560-36568.
15. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006, 440:228-232.
16. Martinon F., Petrilli V., Mayor A., Tardivel A., Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006, 440:237-241.
17. Petrilli V., Papin S., Dostert C., Mayor A., Martinon F., Tschopp J. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 2007, 14:1583-1589.
18. Wen H., Gris D., Lei Y., Jha S., Zhang L., Huang M.T., et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 2011, 12:408-415.
19. Wen H., Ting J.P., O'Neill L.A. A role for the NLRP3 inflammasome in metabolic diseases - did Warburg miss inflammation. Nat. Immunol. 2012, 13:352-357.
20. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
21. Iyer S.S., He Q., Janczy J.R., Elliott E.I., Zhong Z., Olivier A.K., et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 2013, 39:311-323.
22. Munoz-Planillo R., Kuffa P., Martinez-Colon G., Smith B.L., Rajendiran T.M., Nunez G. K(+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 2013, 38:1142-1153.
23. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 2006, 7:569-575.
24. Miao E.A., Ernst R.K., Dors M., Mao D.P., Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2562-2567.
25. Miao E.A., Mao D.P., Yudkovsky N., Bonneau R., Lorang C.G., Warren S.E., et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3076-3080.
26. Molofsky A.B., Byrne B.G., Whitfield N.N., Madigan C.A., Fuse E.T., Tateda K., et al. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 2006, 203:1093-1104.
27. 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.
28. Sun Y.H., Rolan H.G., Tsolis R.M. Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J. Biol. Chem. 2007, 282:33897-33901.
29. 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.
30. Yang J., Zhao Y., Shi J., Shao F. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14408-14413.
31. Zhao Y., Yang J., Shi J., Gong Y.N., Lu Q., Xu H., et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011, 477:596-600.
32. Kofoed E.M., Vance R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011, 477:592-595.
33. Lightfield K.L., Persson J., Brubaker S.W., Witte C.E., von Moltke J., Dunipace E.A., et al. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 2008, 9:1171-1178.
34. Rayamajhi M., Zak D.E., Chavarria-Smith J., Vance R.E., Miao E.A. Cutting edge: mouse NAIP1 detects the type III secretion system needle protein. J. Immunol. 2013, 191:3986-3989.
35. Suzuki S., Franchi L., He Y., Munoz-Planillo R., Mimuro H., Suzuki T., et al. Shigella type III secretion protein MxiI is recognized by Naip2 to induce Nlrc4 inflammasome activation independently of Pkcdelta. PLoS Pathog. 2014, 10:e1003926.
36. Zamboni D.S., Kobayashi K.S., Kohlsdorf T., Ogura Y., Long E.M., Vance R.E., et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 2006, 7:318-325.
37. 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.
38. Boyden E.D., Dietrich W.F. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 2006, 38:240-244.
39. Cirelli K.M., Gorfu G., Hassan M.A., Printz M., Crown D., Leppla S.H., et al. Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii. PLoS Pathog. 2014, 10:e1003927.
40. Ewald S.E., Chavarria-Smith J., Boothroyd J.C. NLRP1 is an inflammasome sensor for Toxoplasma gondii. Infect. Immun. 2014, 82:460-468.
41. Gorfu G., Cirelli K.M., Melo M.B., Mayer-Barber K., Crown D., Koller B.H., et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. MBio 2014, 2014.
42. Chavarria-Smith J., Vance R.E. Direct proteolytic cleavage of NLRP1B is necessary and sufficient for inflammasome activation by anthrax lethal factor. PLoS Pathog. 2013, 9:e1003452.
43. Levinsohn J.L., Newman Z.L., Hellmich K.A., Fattah R., Getz M.A., Liu S., et al. Anthrax lethal factor cleavage of Nlrp1 is required for activation of the inflammasome. PLoS Pathog. 2012, 8:e1002638.
44. Guey B., Bodnar M., Manie S.N., Tardivel A., Petrilli V. Caspase-1 autoproteolysis is differentially required for NLRP1b and NLRP3 inflammasome function. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:17254-17259.
45. Witola W.H., Mui E., Hargrave A., Liu S., Hypolite M., Montpetit A., et al. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells. Infect. Immun. 2011, 79:756-766.
46. Kayagaki N., Warming S., Lamkanfi M., Vande Walle L., Louie S., Dong J., et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011, 479:117-121.
47. Broz P., Ruby T., Belhocine K., Bouley D.M., Kayagaki N., Dixit V.M., et al. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 2012, 490:288-291.
48. Gurung P., Malireddi R.K., Anand P.K., Demon D., Walle L.V., Liu Z., et al. 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. 2012, 287:34474-34483.
49. Rathinam V.A., Vanaja S.K., Waggoner L., Sokolovska A., Becker C., Stuart L.M., et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012.
50. Case C.L., Kohler L.J., Lima J.B., Strowig T., de Zoete M.R., Flavell R.A., et al. Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1851-1856.
51. Casson C.N., Copenhaver A.M., Zwack E.E., Nguyen H.T., Strowig T., Javdan B., et al. Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog. 2013, 9:e1003400.
52. Casson C.N., Shin S. Inflammasome-mediated cell death in response to bacterial pathogens that access the host cell cytosol: lessons from legionella pneumophila. Front. Cell. Infect. Microbiol. 2013, 3:111.
53. Hagar J.A., Powell D.A., Aachoui Y., Ernst R.K., Miao E.A. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 2013, 341:1250-1253.
54. Kayagaki N., Wong M.T., Stowe I.B., Ramani S.R., Gonzalez L.C., Akashi-Takamura S., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013, 341:1246-1249.
55. Meunier E., Dick M.S., Dreier R.F., Schurmann N., Kenzelmann Broz D., Warming S., et al. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 2014, 509:366-370.
56. Pilla D.M., Hagar J.A., Haldar A.K., Mason A.K., Degrandi D., Pfeffer K., et al. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6046-6051.
57. Shi J., Zhao Y., Wang Y., Gao W., Ding J., Li P., et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 2014, 514:187-192.
58. Knodler L.A., Crowley S.M., Sham H.P., Yang H., Wrande M., Ma C., et al. Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 2014, 16:249-256.
59. Wang S., Miura M., Jung Y.K., Zhu H., Li E., Yuan J. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 1998, 92:501-509.
60. von Moltke J., Ayres J.S., Kofoed E.M., Chavarria-Smith J., Vance R.E. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 2013, 31:73-106.
61. Taxman D.J., Huang M.T., Ting J.P. Inflammasome inhibition as a pathogenic stealth mechanism. Cell Host Microbe 2010, 8:7-11.
62. Palm N.W., Rosenstein R.K., Yu S., Schenten D.D., Florsheim E., Medzhitov R. Bee venom phospholipase A2 induces a primary type 2 response that is dependent on the receptor ST2 and confers protective immunity. Immunity 2013, 39:976-985.
63. Galle M., Schotte P., Haegman M., Wullaert A., Yang H.J., Jin S., et al. The Pseudomonas aeruginosa Type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1beta maturation. J. Cell. Mol. Med. 2008, 12:1767-1776.
64. Schotte P., Denecker G., Van Den Broeke A., Vandenabeele P., Cornelis G.R., Beyaert R. Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1beta. J. Biol. Chem. 2004, 279:25134-25142.
65. Hoffmann C., Galle M., Dilling S., Kappeli R., Muller A.J., Songhet P., et al. In macrophages, caspase-1 activation by SopE and the type III secretion system-1 of S. typhimurium can proceed in the absence of flagellin. PLoS ONE 2010, 5:e12477.
66. Muller A.J., Hoffmann C., Galle M., Van Den Broeke A., Heikenwalder M., Falter L., et al. The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 2009, 6:125-136.
67. Fu Y., Galan J.E. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999, 401:293-297.
68. Hardt W.D., Chen L.M., Schuebel K.E., Bustelo X.R., Galan J.E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998, 93:815-826.
69. Raffatellu M., George M.D., Akiyama Y., Hornsby M.J., Nuccio S.P., Paixao T.A., et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 2009, 5:476-486.
70. Winter S.E., Thiennimitr P., Winter M.G., Butler B.P., Huseby D.L., Crawford R.W., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010, 467:426-429.
71. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 2008, 9:847-856.
72. Bruno V.M., Hannemann S., Lara-Tejero M., Flavell R.A., Kleinstein S.H., Galan J.E. Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog. 2009, 5:e1000538.
73. Keestra A.M., Winter M.G., Auburger J.J., Frassle S.P., Xavier M.N., Winter S.E., et al. Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 2013, 496:233-237.
74. LaRock C.N., Cookson B.T. The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing. Cell Host Microbe 2012, 12:799-805.
75. Miao E.A., Scherer C.A., Tsolis R.M., Kingsley R.A., Adams L.G., Baumler A.J., et al. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 1999, 34:850-864.
76. Leung K.Y., Reisner B.S., Straley S.C. YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect. Immun. 1990, 58:3262-3271.
77. McPhee J.B., Mena P., Zhang Y., Bliska J.B. Interleukin-10 induction is an important virulence function of the Yersinia pseudotuberculosis type III effector YopM. Infect. Immun. 2012, 80:2519-2527.
78. Boland A., Cornelis G.R. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 1998, 66:1878-1884.
79. Chung L.K., Philip N.H., Schmidt V.A., Koller A., Strowig T., Flavell R.A., et al. IQGAP1 is important for activation of caspase-1 in macrophages and is targeted by Yersinia pestis type III effector YopM. MBio 2014, 5:e01402-e01414.
80. Jameson K.L., Mazur P.K., Zehnder A.M., Zhang J., Zarnegar B., Sage J., et al. IQGAP1 scaffold-kinase interaction blockade selectively targets RAS-MAP kinase-driven tumors. Nat. Med. 2013, 19:626-630.
81. McLaughlin L.M., Govoni G.R., Gerke C., Gopinath S., Peng K., Laidlaw G., et al. The Salmonella SPI2 effector SseI mediates long-term systemic infection by modulating host cell migration. PLoS Pathog. 2009, 5:e1000671.
82. Philip N.H., Dillon C.P., Snyder A.G., Fitzgerald P., Wynosky-Dolfi M.A., Zwack E.E., et al. Caspase-8 mediates caspase-1 processing and innate immune defense in response to bacterial blockade of NF-kappaB and MAPK signaling. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7385-7390.
83. Weng D., Marty-Roix R., Ganesan S., Proulx M.K., Vladimer G.I., Kaiser W.J., et al. Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7391-7396.
84. Fernandes-Alnemri T., Yu J.W., Datta P., Wu J., Alnemri E.S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009.
85. Hornung V., Ablasser A., Charrel-Dennis M., Bauernfeind F., Horvath G., Caffrey D.R., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009.
86. Jones J.W., Kayagaki N., Broz P., Henry T., Newton K., O'Rourke K., et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9771-9776.
87. Peng K., Broz P., Jones J., Joubert L.M., Monack D. Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell. Microbiol. 2011, 13:1586-1600.
88. Rathinam V.A., Jiang Z., Waggoner S.N., Sharma S., Cole L.E., Waggoner L., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 2010, 11:395-402.
89. Sauer J.D., Witte C.E., Zemansky J., Hanson B., Lauer P., Portnoy D.A. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 2010, 7:412-419.
90. Warren S.E., Armstrong A., Hamilton M.K., Mao D.P., Leaf I.A., Miao E.A., et al. Cutting edge: cytosolic bacterial DNA activates the inflammasome via Aim2. J. Immunol. 2010, 185:818-821.
91. Yang Y., Zhou X., Kouadir M., Shi F., Ding T., Liu C., et al. the AIM2 inflammasome is involved in macrophage activation during infection with virulent Mycobacterium bovis strain. J. Infect. Dis. 2013, 208:1849-1858.
92. Shah S., Bohsali A., Ahlbrand S.E., Srinivasan L., Rathinam V.A., Vogel S.N., et al. Cutting edge: Mycobacterium tuberculosis but not nonvirulent mycobacteria inhibits IFN-beta and AIM2 inflammasome-dependent IL-1beta production via its ESX-1 secretion system. J. Immunol. 2013, 191:3514-3518.
93. Carlsson F., Kim J., Dumitru C., Barck K.H., Carano R.A., Sun M., et al. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog. 2010, 6:e1000895.
94. Koo I.C., Wang C., Raghavan S., Morisaki J.H., Cox J.S., Brown E.J. ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell. Microbiol. 2008, 10:1866-1878.
95. Mishra B.B., Moura-Alves P., Sonawane A., Hacohen N., Griffiths G., Moita L.F., et al. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell. Microbiol. 2010, 12:1046-1063.
96. Le H.T., Harton J.A. Pyrin- and CARD-only proteins as regulators of NLR functions. Front. Immunol. 2013, 4:275.
97. Johnston J.B., Barrett J.W., Nazarian S.H., Goodwin M., Ricciuto D., Wang G., et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 2005, 23:587-598.
98. Rahman M.M., Mohamed M.R., Kim M., Smallwood S., McFadden G. Co-regulation of NF-kappaB and inflammasome-mediated inflammatory responses by myxoma virus pyrin domain-containing protein M013. PLoS Pathog. 2009, 5:e1000635.
99. Gregory S.M., Davis B.K., West J.A., Taxman D.J., Matsuzawa S., Reed J.C., et al. Discovery of a viral NLR homolog that inhibits the inflammasome. Science 2011, 331:330-334.
100. Ichinohe T., Pang I.K., Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 2010, 11:404-410.
101. Kobayashi T., Ogawa M., Sanada T., Mimuro H., Kim M., Ashida H., et al. The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection. Cell Host Microbe 2013, 13:570-583.
102. Hajjar A.M., Ernst R.K., Fortuno E.S., Brasfield A.S., Yam C.S., Newlon L.A., et al. Humanized TLR4/MD-2 mice reveal LPS recognition differentially impacts susceptibility to Yersinia pestis and Salmonella enterica. PLoS Pathog. 2012, 8:e1002963.
103. Montminy S.W., Khan N., McGrath S., Walkowicz M.J., Sharp F., Conlon J.E., et al. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 2006, 7:1066-1073.
104. Rebeil R., Ernst R.K., Gowen B.B., Miller S.I., Hinnebusch B.J. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 2004, 52:1363-1373.
105. Hammer B.K., Swanson M.S. Co-ordination of legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 1999, 33:721-731.
106. Iyoda S., Kamidoi T., Hirose K., Kutsukake K., Watanabe H. A flagellar gene fliZ regulates the expression of invasion genes and virulence phenotype in Salmonella enterica serovar Typhimurium. Microb. Pathog. 2001, 30:81-90.
107. Lucas R.L., Lostroh C.P., DiRusso C.C., Spector M.P., Wanner B.L., Lee C.A. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar typhimurium. J. Bacteriol. 2000, 182:1872-1882.
108. Cummings L.A., Wilkerson W.D., Bergsbaken T., Cookson B.T. In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol. Microbiol. 2006, 61:795-809.
109. Winter S.E., Winter M.G., Godinez I., Yang H.J., Russmann H., Andrews-Polymenis H.L., et al. A rapid change in virulence gene expression during the transition from the intestinal lumen into tissue promotes systemic dissemination of Salmonella. PLoS Pathog. 2010, 6:e1001060.
110. Franchi L., Kamada N., Nakamura Y., Burberry A., Kuffa P., Suzuki S., et al. NLRC4-driven production of IL-1beta discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat. Immunol. 2012.
111. Miao E.A., Leaf I.A., Treuting P.M., Mao D.P., Dors M., Sarkar A., et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 2010, 11:1136-1142.
112. Minnich S.A., Rohde H.N. A rationale for repression and/or loss of motility by pathogenic Yersinia in the mammalian host. Adv. Exp. Med. Biol. 2007, 603:298-310.
113. Chain P.S., Carniel E., Larimer F.W., Lamerdin J., Stoutland P.O., Regala W.M., et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13826-13831.
114. Perez-Lopez A., Rosales-Reyes R., Alpuche-Aranda C.M., Ortiz-Navarrete V. Salmonella downregulates Nod-like receptor family CARD domain containing protein 4 expression to promote its survival in B cells by preventing inflammasome activation and cell death. J. Immunol. 2013, 190:1201-1209.
115. Abdelaziz D.H., Gavrilin M.A., Akhter A., Caution K., Kotrange S., Khweek A.A., et al. Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J. Biol. Chem. 2011, 286:3203-3208.
116. Brodsky I.E., Palm N.W., Sadanand S., Ryndak M.B., Sutterwala F.S., Flavell R.A., et al. A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 2010, 7:376-387.
117. Holmstrom A., Petterson J., Rosqvist R., Hakansson S., Tafazoli F., Fallman M., et al. YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol. Microbiol. 1997, 24:73-91.
118. Kwuan L., Adams W., Auerbuch V. Impact of host membrane pore formation by the Yersinia pseudotuberculosis type III secretion system on the macrophage innate immune response. Infect. Immun. 2013, 81:905-914.
119. Zwack E.E., Snyder A.G., Wynosky-Dolfi M.A., Ruthel G., Philip N.H., Marketon M.M., et al. Inflammasome activation in response to the Yersinia type III secretion system requires hyperinjection of translocon proteins YopB and YopD. MBio 2014, 2014.
120. Collazo C.M., Galan J.E. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol. 1997, 24:747-756.
121. Francis M.S., Wolf-Watz H. YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 1998, 29:799-813.
122. Hersh D., Monack D.M., Smith M.R., Ghori N., Falkow S., Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2396-2401.
123. Edqvist P.J., Aili M., Liu J., Francis M.S. Minimal YopB and YopD translocator secretion by Yersinia is sufficient for Yop-effector delivery into target cells. Microbes Infect. 2007, 9:224-233.
124. Dewoody R., Merritt P.M., Houppert A.S., Marketon M.M. YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol. Microbiol. 2011, 79:1445-1461.
125. Thorslund S.E., Edgren T., Pettersson J., Nordfelth R., Sellin M.E., Ivanova E., et al. The RACK1 signaling scaffold protein selectively interacts with Yersinia pseudotuberculosis virulence function. PLoS ONE 2011, 6:e16784.
126. Brodsky I.E., Medzhitov R. Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 2008, 4:e1000067.
127. Zauberman A., Tidhar A., Levy Y., Bar-Haim E., Halperin G., Flashner Y., et al. Yersinia pestis endowed with increased cytotoxicity is avirulent in a bubonic plague model and induces rapid protection against pneumonic plague. PLoS ONE 2009, 4:e5938.
128. Blander J.M., Sander L.E. Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 2012, 12:215-225.
129. Sander L.E., Davis M.J., Boekschoten M.V., Amsen D., Dascher C.C., Ryffel B., et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011, 474:385-389.
130. 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.
131. Chang P.V., Hao L., Offermanns S., Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:2247-2252.
132. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., deRoos P., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504:451-455.
133. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013, 504:446-450.
134. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Bohlooly Y.M., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
135. Wynosky-Dolfi M.A., Snyder A.G., Philip N.H., Doonan P.J., Poffenberger M.C., Avizonis D., et al. Oxidative metabolism enables Salmonella evasion of the NLRP3 inflammasome. J. Exp. Med. 2014, 211:653-668.
136. Lawley T.D., Chan K., Thompson L.J., Kim C.C., Govoni G.R., Monack D.M. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2006, 2:e11.
137. Fang F.C., Libby S.J., Castor M.E., Fung A.M. Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infect. Immun. 2005, 73:2547-2549.
138. McKinney J.D., Honer zu Bentrup K., Munoz-Elias E.J., Miczak A., Chen B., Chan W.T., et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 2000, 406:735-738.
139. Egan F., Barret M., O'Gara F. The SPI-1-like Type III secretion system: more roles than you think. Front. Plant Sci. 2014, 5:34.
140. Ayres J.S., Trinidad N.J., Vance R.E. Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota. Nat. Med. 2012, 18:799-806.
141. West A.P., Shadel G.S., Ghosh S. Mitochondria in innate immune responses. Nat. Rev. Immunol. 2011, 11:389-402.