Lose the battle to win the war: Bacterial strategies for evading host inflammasome activation

Trends in Microbiology

Volumn 21, Issue 7, 2013, Pages 342-349

  Higa, Naomi ^a   Toma, Claudia ^a   Nohara, Toshitsugu ^a   Nakasone, Noboru ^a   Takaesu, Giichi ^a   Suzuki, Toshihiko ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

bacterial evasion; caspase 1; host inflammasome activation; pathogens

Indexed keywords

ABSENT IN MELANOMA 2 PROTEIN; BACTERIAL TOXIN; CATHEPSIN B; CATHEPSIN L; CRYOPYRIN; INFLAMMASOME; INTERFERON GAMMA INDUCIBLE PROTEIN 16; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NLR FAMILY CARD DOMAIN CONTAINING 4; NLR FAMILY PYRIN DOMAIN CONTAINING 1; NLR FAMILY PYRIN DOMAIN CONTAINING 12; NLR FAMILY PYRIN DOMAIN CONTAINING 6; OUTER MEMBRANE PROTEIN; PYRIN AND HIN 200 DOMAIN CONTAINING PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL SURVIVAL; CYTOKINE RELEASE; GRAM NEGATIVE BACTERIUM; HOST RESISTANCE; HUMAN; IMMUNE EVASION; INNATE IMMUNITY; LYSOSOME; MYCOBACTERIUM BOVIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SALMONELLA; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; VIRUS INFECTION; VIRUS SURVIVAL;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INFLAMMASOMES; MODELS, BIOLOGICAL;

BACTERIA (MICROORGANISMS);

EID: 84879781288     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.04.005     Document Type: Review

References (98)

1. Broz P., Monack D.M. Molecular mechanisms of inflammasome activation during microbial infections. Immunol. Rev. 2011, 243:174-190.
2. Franchi L., et al. Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 2012, 13:325-332.
3. Rathinam V.A., et al. Regulation of inflammasome signaling. Nat. Immunol. 2012, 13:333-342.
4. Strowig T., et al. Inflammasomes in health and disease. Nature 2012, 481:278-286.
5. von Moltke J., et al. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 2013, 31:73-106.
6. Koizumi Y., et al. Inflammasome activation via intracellular NLRs triggered by bacterial infection. Cell. Microbiol. 2012, 14:149-154.
7. Miao E.A., 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.
8. Kofoed E.M., Vance R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011, 477:592-595.
9. Zhao Y., et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011, 477:596-600.
10. Brodsky I.E., 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.
11. McCoy A.J., et al. Differential regulation of caspase-1 activation via NLRP3/NLRC4 inflammasomes mediated by aerolysin and type III secretion system during Aeromonas veronii infection. J. Immunol. 2010, 185:7077-7084.
12. Broz P., et al. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 2010, 207:1745-1755.
13. Broz P., et al. Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 2010, 8:471-483.
14. Qu Y., et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature 2012, 490:539-542.
15. Elinav E., et al. Regulation of the antimicrobial response by NLR proteins. Immunity 2011, 34:665-679.
16. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
17. McCoy A.J., et al. Cytotoxins of the human pathogen Aeromonas hydrophila trigger, via the NLRP3 inflammasome, caspase-1 activation in macrophages. Eur. J. Immunol. 2010, 40:2797-2803.
18. Dunne A., et al. Inflammasome activation by adenylate cyclase toxin directs Th17 responses and protection against Bordetella pertussis. J. Immunol. 2010, 185:1711-1719.
19. Hara H., et al. Dependency of caspase-1 activation induced in macrophages by Listeria monocytogenes on cytolysin, listeriolysin O, after evasion from phagosome into the cytoplasm. J. Immunol. 2008, 180:7859-7868.
20. Kim S., et al. Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. Eur. J. Immunol. 2010, 40:1545-1551.
21. Meixenberger K., et al. Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3. J. Immunol. 2010, 184:922-930.
22. McNeela E.A., et al. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog. 2010, 6:e1001191.
23. Shoma S., et al. Critical involvement of pneumolysin in production of interleukin-1alpha and caspase-1-dependent cytokines in infection with Streptococcus pneumoniae in vitro: a novel function of pneumolysin in caspase-1 activation. Infect. Immun. 2008, 76:1547-1557.
24. Witzenrath M., et al. The NLRP3 inflammasome is differentially activated by pneumolysin variants and contributes to host defense in pneumococcal pneumonia. J. Immunol. 2011, 187:434-440.
25. Harder J., et al. Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-kappa B activation but proceeds independently of TLR signaling and P2X7 receptor. J. Immunol. 2009, 183:5823-5829.
26. Costa A., et al. Activation of the NLRP3 inflammasome by group B streptococci. J. Immunol. 2012, 188:1953-1960.
27. Craven R.R., et al. Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS ONE 2009, 4:e7446.
28. Kebaier C., et al. Staphylococcus aureus alpha-hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J. Infect. Dis. 2012, 205:807-817.
29. Munoz-Planillo R., et al. A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J. Immunol. 2009, 183:3942-3948.
30. Toma C., et al. Pathogenic Vibrio activate NLRP3 inflammasome via cytotoxins and TLR/nucleotide-binding oligomerization domain-mediated NF-kappa B signaling. J. Immunol. 2010, 184:5287-5297.
31. Ng J., et al. Clostridium difficile toxin-induced inflammation and intestinal injury are mediated by the inflammasome. Gastroenterology 2010, 139:542-552.
32. Carlsson F., et al. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog. 2010, 6:e1000895.
33. Mishra B.B., et al. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell. Microbiol. 2010, 12:1046-1063.
34. Zheng Y., et al. A Yersinia effector with enhanced inhibitory activity on the NF-kappaB pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages. PLoS Pathog. 2011, 7:e1002026.
35. Zheng Y., et al. YopJ-induced caspase-1 activation in Yersinia-infected macrophages: independent of apoptosis, linked to necrosis, dispensable for innate host defense. PLoS ONE 2012, 7:e36019.
36. Jun H.K., et al. Integrin alpha5beta1 activates the NLRP3 inflammasome by direct interaction with a bacterial surface protein. Immunity 2012, 36:755-768.
37. Lacroix-Lamande S., et al. Downregulation of the Na/K-ATPase pump by leptospiral glycolipoprotein activates the NLRP3 inflammasome. J. Immunol. 2012, 188:2805-2814.
38. Abdul-Sater A.A., et al. Chlamydial infection of monocytes stimulates IL-1beta secretion through activation of the NLRP3 inflammasome. Microbes Infect. 2010, 12:652-661.
39. Eitel J., et al. Rac1 regulates the NLRP3 inflammasome which mediates IL-1beta production in Chlamydophila pneumoniae infected human mononuclear cells. PLoS ONE 2012, 7:e30379.
40. He X., et al. Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J. Immunol. 2010, 184:5743-5754.
41. Shimada K., et al. Caspase-1 dependent IL-1beta secretion is critical for host defense in a mouse model of Chlamydia pneumoniae lung infection. PLoS ONE 2011, 6:e21477.
42. Gomes M.T., et al. Critical role of ASC inflammasomes and bacterial type IV secretion system in caspase-1 activation and host innate resistance to Brucella abortus infection. J. Immunol. 2013, 190:3629-3638.
43. Kayagaki N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011, 479:117-121.
44. Liu Z., et al. Role of inflammasomes in host defense against Citrobacter rodentium infection. J. Biol. Chem. 2012, 287:16955-16964.
45. Willingham S.B., et al. NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and -independent pathways. J. Immunol. 2009, 183:2008-2015.
46. Huang M.T., et al. Critical role of apoptotic speck protein containing a caspase recruitment domain (ASC) and NLRP3 in causing necrosis and ASC speck formation induced by Porphyromonas gingivalis in human cells. J. Immunol. 2009, 182:2395-2404.
47. Duncan J.A., et al. Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J. Immunol. 2009, 182:6460-6469.
48. Bauernfeind F.G., et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 2009, 183:787-791.
49. Franchi L., et al. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J. Immunol. 2009, 183:792-796.
50. Juliana C., et al. Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J. Biol. Chem. 2012, 287:36617-36622.
51. Lopez-Castejon G., et al. Deubiquitinases regulate the activity of caspase-1 and interleukin-1beta secretion via assembly of the inflammasome. J. Biol. Chem. 2013, 288:2721-2733.
52. Py B.F., et al. Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol. Cell 2013, 49:331-338.
53. Dostert C., et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008, 320:674-677.
54. Bauernfeind F., et al. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J. Immunol. 2011, 187:613-617.
55. Nakahira K., et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 2011, 12:222-230.
56. Zhou R., et al. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
57. Shimada K., et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012, 36:401-414.
58. Dostert C., et al. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE 2009, 4:e6510.
59. Duewell P., et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010, 464:1357-1361.
60. Bruchard M., et al. Chemotherapy-triggered cathepsin B release in myeloid-derived suppressor cells activates the Nlrp3 inflammasome and promotes tumor growth. Nat. Med. 2013, 19:57-64.
61. Murakami T., et al. Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11282-11287.
62. 2+ and cAMP. Nature 2012, 492:123-127.
63. 2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat. Commun. 2012, 3:1329.
64. Broz P., et al. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 2012, 490:288-291.
65. Rathinam V.A., et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012, 150:606-619.
66. Sander L.E., et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011, 474:385-389.
67. Aachoui Y., et al. Caspase-11 protects against bacteria that escape the vacuole. Science 2013, 339:975-978.
68. Harris J., et al. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J. Biol. Chem. 2011, 286:9587-9597.
69. Shi C.S., et al. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 2012, 13:255-263.
70. Hernandez-Cuellar E., et al. Cutting edge: nitric oxide inhibits the NLRP3 inflammasome. J. Immunol. 2012, 189:5113-5117.
71. Mishra B.B., et al. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat. Immunol. 2013, 14:52-60.
72. Guarda G., et al. T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature 2009, 460:269-273.
73. Jones J.W., 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.
74. Rathinam V.A., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 2010, 11:395-402.
75. Sauer J.D., et al. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 2010, 7:412-419.
76. Warren S.E., et al. Cutting edge: cytosolic bacterial DNA activates the inflammasome via Aim2. J. Immunol. 2010, 185:818-821.
77. Saiga H., et al. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int. Immunol. 2012, 24:637-644.
78. Ge J., et al. Preventing bacterial DNA release and absent in melanoma 2 inflammasome activation by a Legionella effector functioning in membrane trafficking. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6193-6198.
79. Eriksson S., et al. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 2003, 47:103-118.
80. Miao E.A., et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 2010, 11:1136-1142.
81. Shimada T., et al. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 2010, 7:38-49.
82. Taxman D.J., et al. Inflammasome inhibition as a pathogenic stealth mechanism. Cell Host Microbe 2010, 8:7-11.
83. Best S.M. Viral subversion of apoptotic enzymes: escape from death row. Annu. Rev. Microbiol. 2008, 62:171-192.
84. Gregory S.M., et al. Discovery of a viral NLR homolog that inhibits the inflammasome. Science 2011, 331:330-334.
85. Komune N., et al. Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1beta secretion. J. Virol. 2011, 85:13019-13026.
86. Johnston J.B., 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.
87. Dorfleutner A., et al. A Shope Fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 2007, 35:685-694.
88. 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.
89. Schotte P., et al. 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.
90. Sutterwala F.S., et al. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 2007, 204:3235-3245.
91. Ulland T.K., et al. Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence. J. Immunol. 2010, 185:2670-2674.
92. Huang M.T., et al. Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J. Immunol. 2010, 185:5476-5485.
93. Master S.S., et al. Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 2008, 3:224-232.
94. Abdelaziz D.H., et al. Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J. Biol. Chem. 2011, 286:3203-3208.
95. Higa N., et al. Vibrio parahaemolyticus effector proteins suppress inflammasome activation by interfering with host autophagy signaling. PLoS Pathog. 2013, 9:e1003142.
96. Wen H., et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 2011, 12:408-415.
97. Mariathasan S., et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004, 430:213-218.
98. Suzuki T., et al. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 2007, 3:e111.