NLRP3 inflammasome and host protection against bacterial infection

Journal of Korean Medical Science

Volumn 28, Issue 10, 2013, Pages 1415-1423

  Kim, Jwa Jin ^a   Jo, Eun Kyeong ^a  

^a Chungnam National University   (South Korea)

Author keywords

Bacteria; Host defense; Infection; Inflammation; NLRP3 protein, human; Pathology

Indexed keywords

CARRIER PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRP3 PROTEIN, HUMAN;

BACTERIAL INFECTION; BACTERIUM; HOST RESISTANCE; HUMAN; IMMUNOLOGY; INFECTION; INFLAMMATION; METABOLISM; PATHOLOGY; REVIEW; SIGNAL TRANSDUCTION;

BACTERIA; HOST DEFENSE; INFECTION; INFLAMMATION; NLRP3 PROTEIN, HUMAN; PATHOLOGY;

BACTERIAL INFECTIONS; CARRIER PROTEINS; CASPASE 1; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; SIGNAL TRANSDUCTION;

EID: 84885705098     PISSN: 10118934     EISSN: 15986357     Source Type: Journal    
DOI: 10.3346/jkms.2013.28.10.1415     Document Type: Review

References (71)

1. Cassel SL, Joly S, Sutterwala FS. The NLRP3 inflammasome: a sensor of immune danger signals. Semin Immunol 2009; 21: 194-8.
2. Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 2009; 10: 241-7.
3. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009; 27: 229-65.
4. Latz E. The inflammasomes: mechanisms of activation and function. Curr Opin Immunol 2010; 22: 28-33.
5. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 2004; 20: 319-25.
6. LamkanfiM, Dixit VM. Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 2009; 227: 95-105.
7. Tschopp J, Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 2010; 10: 210-5.
8. Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, Brown GD, Fitzgerald KA. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 2009; 5: 487-97.
9. Yang CS, Shin DM, Jo EK. The role of NLR-related protein 3 inflammasome in host defense and inflammatory diseases. Int Neurourol J 2012; 16: 2-12.
10. Bae JY, Park HH. Crystal structure of NALP3 protein pyrin domain (PYD) and its implications in inflammasome assembly. J Biol Chem 2011; 286: 39528-36.
11. Vajjhala PR, Mirams RE, Hill JM. Multiple binding sites on the pyrin domain of ASC protein allow self-association and interaction with NLRP3 protein. J Biol Chem 2012; 287: 41732-43.
12. Gombault A, Baron L, Couillin I. ATP release and purinergic signaling in NLRP3 inflammasome activation. Front Immunol 2012; 3: 414.
13. Pelegrin P, Surprenant A. Pannexin-1 couples to maitotoxin- and nigericin-induced interleukin-1beta release through a dye uptake-independent pathway. J Biol Chem 2007; 282: 2386-94.
14. Zhong Z, Zhai Y, Liang S, Mori Y, Han R, Sutterwala FS, Qiao L. TRPM2 links oxidative stress to NLRP3 inflammasome activation. Nat Commun 2013; 4: 1611.
15. Vladimer GI, Marty-Roix R, Ghosh S, Weng D, Lien E. Inflammasomes and host defenses against bacterial infections. Curr Opin Microbiol 2013; 16: 23-31.
16. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, van der Meer JH, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I, et al. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 2009; 113: 2324-35.
17. Lu B, Nakamura T, Inouye K, Li J, Tang Y, Lundbäck P, Valdes-Ferrer SI, Olofsson PS, Kalb T, Roth J, et al. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 2012; 488: 670-4.
18. Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, Cresswell P, MacMicking JD. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 2012; 336: 481-5.
19. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469: 221-5.
20. Misawa T, Takahama M, Kozaki T, Lee H, Zou J, Saitoh T, Akira S. Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome. Nat Immunol 2013; 14: 454-60.
21. Subramanian N, Natarajan K, Clatworthy MR, Wang Z, Germain RN. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 2013; 153: 348-61.
22. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6: 981-8.
23. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437: 1167-72.
24. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006; 440: 228-32.
25. Willingham SB, Bergstralh DT, O'Connor W, Morrison AC, Taxman DJ, Duncan JA, Barnoy S, Venkatesan MM, Flavell RA, Deshmukh M, et al. Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2007; 2: 147-59.
26. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, Leong JM, Fitzgerald KA. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012; 150: 606-19.
27. Duncan JA, Gao X, Huang MT, O'Connor BP, Thomas CE, Willingham SB, Bergstralh DT, Jarvis GA, Sparling PF, Ting JP. Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J Immunol 2009; 182: 6460-9.
28. Master SS, Rampini SK, Davis AS, Keller C, Ehlers S, Springer B, Timmins GS, Sander P, Deretic V. Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 2008; 3: 224-32.
29. Lee HM, Yuk JM, Kim KH, Jang J, Kang G, Park JB, Son JW, Jo EK. Mycobacterium abscessus activates the NLRP3 inflammasome via Dectin-1-Syk and p62/SQSTM1. Immunol Cell Biol 2012; 90: 601-10.
30. Mishra BB, Moura-Alves P, Sonawane A, Hacohen N, Griffiths G, Moita LF, Anes E. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol 2010; 12: 1046-63.
31. Lee HM, Kang J, Lee SJ, Jo EK. Microglial activation of the NLRP3 inflammasome by the priming signals derived from macrophages infected with mycobacteria. Glia 2013; 61: 441-52.
32. Koo JE, Hong HJ, Dearth A, Kobayashi KS, Koh YS. Intracellular invasion of Orientia tsutsugamushi activates inflammasome in asc-dependent manner. PLoS One 2012; 7: e39042.
33. He X, Mekasha S, Mavrogiorgos N, Fitzgerald KA, Lien E, Ingalls RR. Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J Immunol 2010; 184: 5743-54.
34. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 2006; 126: 1135-45.
35. Costa A, Gupta R, Signorino G, Malara A, Cardile F, Biondo C, Midiri A, Galbo R, Trieu-Cuot P, Papasergi S, et al. Activation of the NLRP3 inflammasome by group B streptococci. J Immunol 2012; 188: 1953-60.
36. McNeela EA, Burke A, Neill DR, Baxter C, Fernandes VE, Ferreira D, Smeaton S, El-Rachkidy R, McLoughlin RM, Mori A, et al. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cy tokines independently of TLR4. PLoS Pathog 2010; 6: e1001191.
37. Kebaier C, Chamberland RR, Allen IC, Gao X, Broglie PM, Hall JD, Jania C, Doerschuk CM, Tilley SL, Duncan JA. Staphylococcus aureus a- hemolysin mediates virulence in a murine model of severe pneumonia through activation of the NLRP3 inflammasome. J Infect Dis 2012; 205: 807-17.
38. Holzinger D, Gieldon L, Mysore V, Nippe N, Taxman DJ, Duncan JA, Broglie PM, Marketon K, Austermann J, Vogl T, et al. Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 2012; 92: 1069-81.
39. Jun HK, Lee SH, Lee HR, Choi BK. Integrin a5ß1 activates the NLRP3 inflammasome by direct interaction with a bacterial surface protein. Immunity 2012; 36: 755-68.
40. Kayagaki N, Warming S, LamkanfiM, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, et al. Non-canonical inflammasome activation targets caspase-11. Nature 2011; 479: 117-21.
41. Zheng Y, Lilo S, Brodsky IE, Zhang Y, Medzhitov R, Marcu KB, Bliska JB. A Yersinia effector with enhanced inhibitory activity on the NF-?B pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages. PLoS Pathog 2011; 7: e1002026.
42. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, Ryffel B, Swanson JA, Müller M, Blander JM. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011; 474: 385-9.
43. Ceballos-Olvera I, Sahoo M, Miller MA, Del Barrio L, Re F. Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1ß is deleterious. PLoS Pathog 2011; 7: e1002452.
44. Liu Z, Zaki MH, Vogel P, Gurung P, Finlay BB, Deng W, LamkanfiM, Kanneganti TD. Role of inflammasomes in host defense against Citrobacter rodentium infection. J Biol Chem 2012; 287: 16955-64.
45. Broz P, Newton K, LamkanfiM, Mariathasan S, Dixit VM, Monack DM. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med 2010; 207: 1745-55.
46. Aachoui Y, Leaf IA, Hagar JA, Fontana MF, Campos CG, Zak DE, Tan MH, Cotter PA, Vance RE, Aderem A, et al. Caspase-11 protects against bacteria that escape the vacuole. Science 2013; 339: 975-8.
47. Saiga H, Kitada S, Shimada Y, Kamiyama N, Okuyama M, Makino M, Yamamoto M, Takeda K. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int Immunol 2012; 24: 637-44.
48. Carlsson F, Kim J, Dumitru C, Barck KH, Carano RA, Sun M, Diehl L, Brown EJ. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog 2010; 6: e1000895.
49. Mishra BB, Rathinam VA, Martens GW, Martinot AJ, Kornfeld H, Fitzgerald KA, Sassetti CM. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1ß. Nat Immunol 2013; 14: 52-60.
50. Chen CC, Tsai SH, Lu CC, Hu ST, Wu TS, Huang TT, Saïd-Sadier N, Ojcius DM, Lai HC. Activation of an NLRP3 inflammasome restricts Mycobacterium kansasii infection. PLoS One 2012; 7: e36292.
51. Kastenmüller W, Torabi-Parizi P, Subramanian N, Lämmermann T, Germain RN. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 2012; 150: 1235-48.
52. Chilton PM, Embry CA, Mitchell TC. Effects of differences in lipid A structure on TLR4 pro-inflammatory signaling and inflammasome activation. Front Immunol 2012; 3: 154.
53. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A, Warren SE, Wewers MD, Aderem A. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 2010; 11: 1136-42.
54. Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, Christiansen G, Birkelund S. Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia trachomatis infection. Cell Microbiol 2007; 9: 2795-803.
55. Abdul-Sater AA, Saïd-Sadier N, Padilla EV, Ojcius DM. Chlamydial infection of monocytes stimulates IL-1beta secretion through activation of the NLRP3 inflammasome. Microbes Infect 2010; 12: 652-61.
56. Nagarajan UM, Sikes JD, Yeruva L, Prantner D. Significant role of IL-1 signaling, but limited role of inflammasome activation, in oviduct pathology during Chlamydia muridarum genital infection. J Immunol 2012; 188: 2866-75.
57. Hitzler I, Sayi A, Kohler E, Engler DB, Koch KN, Hardt WD, Müller A. Caspase-1 has both proinflammatory and regulatory properties in Helicobacter infections, which are differentially mediated by its substrates IL-1ß and IL-18. J Immunol 2012; 188: 3594-602.
58. Oosting M, van de Veerdonk FL, Kanneganti TD, Sturm P, Verschueren I, Berende A, van der Meer JW, Kullberg BJ, Netea MG, Joosten LA. Borrelia species induce inflammasome activation and IL-17 production through a caspase-1-dependent mechanism. Eur J Immunol 2011; 41: 172-81.
59. Oosting M, Buffen K, Malireddi SR, Sturm P, Verschueren I, Koenders MI, van de Veerdonk FL, van der Meer JW, Netea MG, Kanneganti TD, et al. Murine Borrelia arthritis is highly dependent on ASC and caspase-1, but independent of NLRP3. Arthritis Res Ther 2012; 14: R247.
60. Liu N, Belperron AA, Booth CJ, Bockenstedt LK. The caspase 1 inflammasome is not required for control of murine Lyme borreliosis. Infect Immun 2009; 77: 3320-7.
61. Cohen TS, Prince AS. Activation of inflammasome signaling mediates pathology of acute P: aeruginosa pneumonia. J Clin Invest 2013; 123: 1630-7.
62. Thakur A, Barrett RP, McClellan S, Hazlett LD. Regulation of Pseudomonas aeruginosa corneal infection in IL-1 beta converting enzyme (ICE, caspase-1) deficient mice. Curr Eye Res 2004; 29: 225-33.
63. Wong KW, Jacobs WR Jr. Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis. Cell Microbiol 2011; 13: 1371-84.
64. McElvania Tekippe E, Allen IC, Hulseberg PD, Sullivan JT, McCann JR, Sandor M, Braunstein M, Ting JP. Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1. PLoS One 2010; 5: e12320.
65. Lalor SJ, Dungan LS, Sutton CE, Basdeo SA, Fletcher JM, Mills KH. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gammadelta and CD4 T cells that mediate autoimmunity. J Immunol 2011; 186: 5738-48.
66. Rathinam VA, Vanaja SK, Fitzgerald KA. Regulation of inflammasome signaling. Nat Immunol 2012; 13: 333-2.
67. Galle M, Schotte P, Haegman M, Wullaert A, Yang HJ, Jin S, Beyaert R. 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: 1767-76.
68. Schotte P, Denecker G, Van Den Broeke A, Vandenabeele P, Cornelis GR, 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: 25134-42.
69. Brodsky IE, Palm NW, Sadanand S, Ryndak MB, Sutterwala FS, Flavell RA, Bliska JB, Medzhitov R. A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 2010; 7: 376-87.
70. Abdelaziz DH, Gavrilin MA, Akhter A, Caution K, Kotrange S, Khweek AA, Abdulrahman BA, Grandhi J, Hassan ZA, Marsh C, et al. Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes. J Biol Chem 2011; 286: 3203-8.
71. Huang MT, Mortensen BL, Taxman DJ, Craven RR, Taft-Benz S, Kijek TM, Fuller JR, Davis BK, Allen IC, Brickey WJ, et al. Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J Immunol 2010; 185: 5476-85.