The NLRP3 inflammasome: Role in airway inflammation

Clinical and Experimental Allergy

Volumn 44, Issue 2, 2014, Pages 160-172

  Im, H ^a   Ammit, A J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AIM2 PROTEIN; ASC PROTEIN; CALCIUM ION; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRC4 PROTEIN; PATTERN RECOGNITION RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; ASTHMA; CELL MATURATION; ENZYME ACTIVATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; ION CURRENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; RESPIRATORY TRACT INFLAMMATION;

ANIMALS; ASTHMA; CARRIER PROTEINS; CASPASE 1; CELL DEATH; HUMANS; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; PROTEIN STRUCTURE, TERTIARY;

EID: 84892770825     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12206     Document Type: Article

References (105)

1. Hirota JA, Hirota SA, Warner SM et al. The airway epithelium nucleotide-binding domain and leucine-rich repeat protein 3 inflammasome is activated by urban particulate matter. J Allergy Clin Immunol 2012; 129(1116-25):e6.
2. Tran HB, Lewis MD, Tan LW et al. Immunolocalization of NLRP3 Inflammasome in Normal Murine Airway Epithelium and Changes following Induction of Ovalbumin-Induced Airway Inflammation. J Allergy (Cairo) 2012; 2012:819176.
3. Besnard AG, Guillou N, Tschopp J et al. NLRP3 inflammasome is required in murine asthma in the absence of aluminum adjuvant. Allergy 2011; 66:1047-57.
4. Ather JL, Ckless K, Martin R et al. Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J Immunol 2011; 187:64-73.
5. Cassel SL, Joly S, Sutterwala FS. The NLRP3 inflammasome: a sensor of immune danger signals. Semin Immunol 2009; 21:194-8.
6. Tillack K, Breiden P, Martin R, Sospedra M. T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J Immunol 2012; 188:3150-9.
7. Steinman RM, Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 2006; 311:17-58.
8. Schroder K, Tschopp J. The inflammasomes. Cell 2010; 140:821-32.
9. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature 2012; 481:278-86.
10. Guarda G, So A. Regulation of inflammasome activity Immunology 2010; 130:329-36.
11. Wong CK, Hu S, Leung KM et al. NOD-like receptors mediated activation of eosinophils interacting with bronchial epithelial cells: a link between innate immunity and allergic asthma. Cell Mol Immunol 2013; 10:317-29.
12. Minkiewicz J, de Rivero Vaccari JP, Keane RW. Human astrocytes express a novel NLRP2 inflammasome. Glia 2013; 61:1113-21.
13. Anand PK, Malireddi RK, Lukens JR et al. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature 2012; 488:389-93.
14. Elinav E, Strowig T, Kau AL et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-57.
15. Sun Y, Zhang M, Chen CC et al. Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice. Gastroenterology 2013; 144:1478-87.
16. Davis BK, Roberts RA, Huang MT et al. Cutting edge: NLRC5-dependent activation of the inflammasome. J Immunol 2011; 186:1333-7.
17. Triantafilou K, Kar S, van Kuppeveld FJ, Triantafilou M. Rhinovirus-induced calcium flux triggers NLRP3 and NLRC5 activation in bronchial cells. Am J Respir Cell Mol Biol 2013; 49:923-34.
18. 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.
19. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 2009; 10:241-7.
20. Sagulenko V, Thygesen SJ, Sester DP et al. AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC. Cell Death Differ 2013; 20: 1149-60.
21. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA. Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 2011; 32:110-6.
22. Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death. Immunol Rev 2011; 243:206-14.
23. Wenzel M, Wunderlich M, Besch R et al. Cytosolic DNA triggers mitochondrial apoptosis via DNA damage signaling proteins independently of AIM2 and RNA polymerase III. J Immunol 2012; 188:394-403.
24. Ulland TK, Janowski AM, Buchan BW et al. Francisella tularensis live vaccine strain folate metabolism and pseudouridine synthase gene mutants modulate macrophage caspase-1 activation. Infect Immun 2013; 81:201-8.
25. Witte CE, Archer KA, Rae CS, Sauer JD, Woodward JJ, Portnoy DA. Innate immune pathways triggered by Listeria monocytogenes and their role in the induction of cell-mediated immunity. Adv Immunol 2012; 113:135-56.
26. Dombrowski Y, Peric M, Koglin S et al. Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci Transl Med 2011; 3:82ra38.
27. Kummer JA, Broekhuizen R, Everett H et al. Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J Histochem Cytochem 2007; 55:443-52.
28. Hsu LC, Ali SR, McGillivray S et al. A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc Natl Acad Sci U S A 2008; 105:7803-8.
29. Faustin B, Lartigue L, Bruey JM et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell 2007; 25:713-24.
30. Grenier JM, Wang L, Manji GA et al. Functional screening of five PYPAF family members identifies PYPAF5 as a novel regulator of NF-kappaB and caspase-1. FEBS Lett 2002; 530:73-8.
31. Case CL, Roy CR. Asc modulates the function of NLRC4 in response to infection of macrophages by Legionella pneumophila. MBio 2011; 2:e00117-11.
32. Miao EA, Mao DP, Yudkovsky N et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 2010; 107:3076-80.
33. Cohen TS, Prince AS. Activation of inflammasome signaling mediates pathology of acute P. aeruginosa pneumonia. J Clin Invest 2013; 123:1630-7.
34. Lamkanfi M, Kanneganti TD. Nlrp3: an immune sensor of cellular stress and infection. Int J Biochem Cell Biol 2010; 42:792-5.
35. Lamkanfi M, Dixit VM. Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 2009; 227:95-105.
36. Ahmad I, Muneer KM, Tamimi IA, Chang ME, Ata MO, Yusuf N. Thymoquinone suppresses metastasis of melanoma cells by inhibition of NLRP3 inflammasome. Toxicol Appl Pharmacol 2013; 270:70-6.
37. McCall SH, Sahraei M, Young AB et al. Osteoblasts express NLRP3, a nucleotide-binding domain and leucine-rich repeat region containing receptor implicated in bacterially induced cell death. J Bone Miner Res 2008; 23:30-40.
38. Sandanger O, Ranheim T, Vinge LE et al. The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischemia-reperfusion injury. Cardiovasc Res 2013; 199:164-74.
39. Wang Y, Yang C, Mao K, Chen S, Meng G, Sun B. Cellular localization of NLRP3 inflammasome. Protein Cell 2013; 4:425-31.
40. Franchi L, Eigenbrod T, Nunez G. Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J Immunol 2009; 183:792-6.
41. Kanneganti TD, Ozoren N, Body-Malapel M et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 2006; 440:233-6.
42. Xu P, Wen Z, Shi X et al. Hemorrhagic shock augments Nlrp3 inflammasome activation in the lung through impaired pyrin induction. J Immunol 2013; 190:5247-55.
43. McCoy AJ, Koizumi Y, Higa N, Suzuki T. 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; 185:7077-84.
44. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440:237-41.
45. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 2011; 29:707-35.
46. Hashimoto M, Tanaka H, Abe S. Quantitative analysis of bronchial wall vascularity in the medium and small airways of patients with asthma and COPD. Chest 2005; 127:965-72.
47. Feldmeyer L, Keller M, Niklaus G, Hohl D, Werner S, Beer HD. The inflammasome mediates UVB-induced activation and secretion of interleukin-1beta by keratinocytes. Curr Biol 2007; 17:1140-5.
48. 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; 14:1583-9.
49. Rajamaki K, Nordstrom T, Nurmi K et al. Extracellular acidosis is a novel danger signal alerting innate immunity via the NLRP3 inflammasome. J Biol Chem 2013; 288:13410-9.
50. Riteau N, Gasse P, Fauconnier L et al. Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am J Respir Crit Care Med 2010; 182:774-83.
51. Kanneganti TD, Lamkanfi M, Kim YG et al. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007; 26:433-43.
52. Cruz CM, Rinna A, Forman HJ, Ventura AL, Persechini PM, Ojcius DM. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 2007; 282:2871-9.
53. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008; 320:674-7.
54. Halle A, Hornung V, Petzold GC et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008; 9:857-65.
55. Scharf B, Clement CC, Wu XX et al. Annexin A2 binds to endosomes following organelle destabilization by particulate wear debris. Nat Commun 2012; 3:755.
56. Welin A, Eklund D, Stendahl O, Lerm M. Human macrophages infected with a high burden of ESAT-6-expressing M. tuberculosis undergo caspase-1- and cathepsin B-independent necrosis. PLoS One 2011; 6:e20302.
57. Gammelsrud A, Solhaug A, Dendele B et al. Enniatin B-induced cell death and inflammatory responses in RAW 267.4 murine macrophages. Toxicol Appl Pharmacol 2012;261: 74-87.
58. Liao YH, Lin YC, Tsao ST et al. HMG-CoA reductase inhibitors activate caspase-1 in human monocytes depending on ATP release and P2X7 activation. J Leukoc Biol 2013; 93:289-99.
59. Brickey WJ, Alexis NE, Hernandez ML, Reed W, Ting JP, Peden DB. Sputum inflammatory cells from patients with allergic rhinitis and asthma have decreased inflammasome gene expression. J Allergy Clin Immunol 2011; 128:900-3.
60. Hernandez ML, Herbst M, Lay JC et al. Atopic asthmatic patients have reduced airway inflammatory cell recruitment after inhaled endotoxin challenge compared with healthy volunteers. J Allergy Clin Immunol 2012; 130(869-76):e2.
61. Pauwels RA, Pedersen S, Busse WW et al. Early intervention with budesonide in mild persistent asthma: a randomised, double-blind trial. The Lancet 2003; 361:1071-6.
62. Reddel H, Ware S, Marks G, Salome C, Jenkins C, Woolcock A. Differences between asthma exacerbations and poor asthma control. The Lancet 1999; 353:364-9.
63. Hayden FG. Rhinovirus and the lower respiratory tract. Rev Med Virol 2004; 14:17-31.
64. Edwards MR, Bartlett NW, Hussell T, Openshaw P, Johnston SL. The microbiology of asthma. Nat Rev Micro 2012; 10:459-71.
65. Corne JM, Marshall C, Smith S et al. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. The Lancet 2002; 359:831-4.
66. Bauer RN, Brighton LE, Mueller L et al. Influenza enhances caspase-1 in bronchial epithelial cells from asthmatic volunteers and is associated with pathogenesis. J Allergy Clin Immunol 2012; 130(958-67):e14.
67. Hirota JA, Im H, Rahman MM et al. The NLRP3 Inflammasome is not Activated in Airway Smooth Muscle Upon TLR2 Ligation. Am J Respir Cell Mol Biol 2013; 49:517-24.
68. Segovia J, Sabbah A, Mgbemena V et al. TLR2/MyD88/NF-kappaB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 2012; 7:e29695.
69. Allen IC, Scull MA, Moore CB et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009; 30:556-65.
70. Pothlichet J, Meunier I, Davis BK et al. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 2013; 9:e1003256.
71. Bauernfeind F, Bartok E, Rieger A, Franchi L, Nunez G, Hornung V. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol 2011; 187:613-7.
72. Riteau N, Baron L, Villeret B et al. ATP release and purinergic signaling: a common pathway for particle-mediated inflammasome activation. Cell Death Dis 2012; 3:e403.
73. Peeters PM, Perkins TN, Wouters EF, Mossman BT, Reynaert NL. Silica induces NLRP3 inflammasome activation in human lung epithelial cells. Part Fibre Toxicol 2013; 10:3.
74. Triantafilou K, Hughes TR, Triantafilou M, Morgan BP. The complement membrane attack complex triggers intracellular Ca2+ fluxes leading to NLRP3 inflammasome activation. J Cell Sci 2013; 126:2903-13.
75. Starkey MR, Jarnicki AG, Essilfie AT et al. Murine models of infectious exacerbations of airway inflammation. Curr Opin Pharmacol 2013; 13:337-44.
76. Fukumoto J, Fukumoto I, Parthasarathy PT et al. NLRP3 Deletion Protects from Hyperoxia-Induced Acute Lung Injury. Am J Physiol Cell Physiol 2013; 305:C182-9.
77. Girtsman TA, Beamer CA, Wu N, Buford M, Holian A. IL-1R signalling is critical for regulation of multi-walled carbon nanotubes-induced acute lung inflammation in C57Bl/6 mice. Nanotoxicology 2014; 8:17-27.
78. Feng F, Li Z, Potts-Kant EN et al. Hyaluronan activation of the Nlrp3 inflammasome contributes to the development of airway hyperresponsiveness. Environ Health Perspect 2012; 120:1692-8.
79. Gasse P, Riteau N, Charron S et al. Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am J Respir Crit Care Med 2009; 179:903-13.
80. Idzko M, Hammad H, van Nimwegen M et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat Med 2007;13: 913-9.
81. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008; 453:1122-6.
82. Kool M, Willart MA, van Nimwegen M et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 2011; 34:527-40.
83. Willingham SB, Allen IC, Bergstralh DT et al. NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and -independent pathways. J Immunol 2009; 183:2008-15.
84. Allen IC, Jania CM, Wilson JE et al. Analysis of NLRP3 in the development of allergic airway disease in mice. J Immunol 2012; 188:2884-93.
85. Sawada M, Kawayama T, Imaoka H et al. IL-18 induces airway hyperresponsiveness and pulmonary inflammation via CD4+ T cell and IL-13. PLoS One 2013; 8:e54623.
86. Leung BP, Culshaw S, Gracie JA et al. A role for IL-18 in neutrophil activation. J Immunol 2001; 167:2879-86.
87. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 2005; 32:311-8.
88. Ohbayashi H, Shimokata K. Matrix metalloproteinase-9 and airway remodeling in asthma. Curr Drug Targets Inflamm Allergy 2005; 4:177-81.
89. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007; 8:942-9.
90. Fortin CF, Ear T, McDonald PP. Autocrine role of endogenous interleukin-18 on inflammatory cytokine generation by human neutrophils. FASEB J 2009; 23:194-203.
91. Hoffman HM, Wanderer AA. Inflammasome and IL-1beta-mediated disorders. Curr Allergy Asthma Rep 2010; 10:229-35.
92. Cowan DC, Cowan JO, Palmay R, Williamson A, Taylor DR. Effects of steroid therapy on inflammatory cell subtypes in asthma. Thorax 2010; 65:384-90.
93. ten Brinke A, Zwinderman AH, Sterk PJ, Rabe KF, Bel EH. "Refractory" eosinophilic airway inflammation in severe asthma: effect of parenteral corticosteroids. Am J Respir Crit Care Med 2004; 170:601-5.
94. Milner JD. IL-17 producing cells in host defense and atopy. Curr Opin Immunol 2011; 23:784-8.
95. Wang YH, Wills-Karp M. The potential role of interleukin-17 in severe asthma. Curr Allergy Asthma Rep 2011; 11:388-94.
96. Halwani R, Al-Muhsen S, Hamid Q. T helper 17 cells in airway diseases: from laboratory bench to bedside. Chest 2013; 143:494-501.
97. Linden A. Interleukin-17 and airway remodelling. Pulm Pharmacol Ther 2006; 19:47-50.
98. Mills KHG, Dungan LS, Jones SA, Harris J. The role of inflammasome-derived IL-1 in driving IL-17 responses. J Leukoc Biol 2013; 93:489-97.
99. Besnard A-G, Togbe D, Couillin I et al. Inflammasome-IL-1-Th17 response in allergic lung inflammation. J Mol Cell Biol 2012; 4:3-10.
100. Martin RA, Ather JL, Lundblad LKA et al. Interleukin-1 receptor and caspase-1 are required for the Th17 response in nitrogen dioxide-promoted allergic airway disease. Am J Respir Cell Mol Biol 2013; 48:655-64.
101. Esnault S, Kelly EA, Nettenstrom LM, Cook EB, Seroogy CM, Jarjour NN. Human eosinophils release IL-1ss and increase expression of IL-17A in activated CD4+ T lymphocytes. Clin Exp Allergy 2012; 42:1756-64.
102. Lamkanfi M, Dixit VM. Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 2012; 28:137-61.
103. Reisetter AC, Stebounova LV, Baltrusaitis J et al. Induction of inflammasome-dependent pyroptosis by carbon black nanoparticles. J Biol Chem 2011; 286:21844-52.
104. Kovarova M, Hesker PR, Jania L et al. NLRP1-dependent pyroptosis leads to acute lung injury and morbidity in mice. J Immunol 2012; 189:2006-16.
105. 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-1beta is deleterious. PLoS Pathog 2011; 7:e1002452.