Immunology in clinic review series; focus on autoinflammatory diseases: Inflammasomes: Mechanisms of activation

Clinical and Experimental Immunology

Volumn 167, Issue 3, 2012, Pages 369-381

  Mankan, A K ^a   Kubarenko, A ^a   Hornung, V ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

Caspase 1; IL 1 ; Inflammasome

Indexed keywords

ADENOSINE TRIPHOSPHATE; AIM2 PROTEIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CRYOPYRIN; FLAGELLIN; GRAMICIDIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; LEUCINE RICH REPEAT KINASE 2; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NIGERICIN; NLRC4 PROTEIN; NLRP1 PROTEIN; NLRP6 PROTEIN; POTASSIUM; PURINERGIC P2X7 RECEPTOR; PYRIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; URIC ACID; VALINOMYCIN;

AMINO TERMINAL SEQUENCE; ANTHRAX; AUTOINFLAMMATORY DISEASE; BACTERIAL INFECTION; CELL DEATH; CYTOKINE RELEASE; ENZYME ACTIVATION; FAMILIAL MEDITERRANEAN FEVER; GENE MUTATION; HUMAN; IMMUNE RESPONSE; LEGIONELLA PNEUMOPHILA; MACROPHAGE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTE; PORPHYROMONAS GINGIVALIS; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA; SALMONELLA TYPHIMURIUM; SHIGELLA FLEXNERI;

ANIMALS; AUTOIMMUNE DISEASES; CASPASE 1; CELL DEATH; HEREDITARY AUTOINFLAMMATORY DISEASES; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; MODELS, IMMUNOLOGICAL; MODELS, MOLECULAR; SIGNAL TRANSDUCTION;

EID: 84856368969     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2011.04534.x     Document Type: Review

References (100)

1. Masters SL, Simon A, Aksentijevich I, Kastner DL. Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease (*). Annu Rev Immunol 2009; 27:621-68.
2. Ozkurede VU, Franchi L. Immunology in the clinic review series; focus on autoinflammatory diseases: role of inflammasomes in autoinflammatory syndromes. Clin Exp Immun 2012; 167:382-90.
3. Goldbach-Mansky R. Immunology in clinic review series; focus on autoinflammatory diseases: update on monogenic autoinflammatory diseases: the role of interleukin (IL)-1 and an emerging role for cytokines beyond IL-1. Clin Exp Immun 2012; 167:391-404.
4. Keller M, Ruegg A, Werner S, Beer HD. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008; 132:818-31.
5. Cookson BT, Brennan MA. Pro-inflammatory programmed cell death. Trends Microbiol 2001; 9:113-4.
6. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 2000; 38:31-40.
7. Miao EA, Leaf IA, Treuting PM etal. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 2010; 11:1136-42.
8. Manji GA, Wang L, Geddes BJ etal. PYPAF1, a PYRIN-containing Apaf1-like protein that assembles with ASC and regulates activation of NF-kappa B. J Biol Chem 2002; 277:11570-5.
9. Wang L, Manji GA, Grenier JM etal. PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing. J Biol Chem 2002; 277:29874-80.
10. Grenier JM, Wang L, Manji GA etal. 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.
11. Hornung V, Ablasser A, Charrel-Dennis M etal. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009; 458:514-8.
12. Yamamoto M, Yaginuma K, Tsutsui H etal. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules. Genes Cells 2004; 9:1055-67.
13. Mariathasan S, Newton K, Monack DM etal. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004; 430:213-8.
14. Taxman DJ, Zhang J, Champagne C etal. Cutting edge: ASC mediates the induction of multiple cytokines by Porphyromonas gingivalis via caspase-1-dependent and -independent pathways. J Immunol 2006; 177:4252-6.
15. Taxman DJ, Holley-Guthrie EA, Huang MT etal. The NLR adaptor ASC/PYCARD regulates DUSP10, mitogen-activated protein kinase (MAPK), and chemokine induction independent of the inflammasome. J Biol Chem 2011; 286:19605-16.
16. Tschopp J, Martinon F, Burns K. NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 2003; 4:95-104.
17. Ting JP, Lovering RC, Alnemri ES etal. The NLR gene family: a standard nomenclature. Immunity 2008; 28:285-7.
18. Masumoto J, Taniguchi S, Ayukawa K etal. ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J Biol Chem 1999; 274:33835-8.
19. Richards N, Schaner P, Diaz A etal. Interaction between pyrin and the apoptotic speck protein (ASC) modulates ASC-induced apoptosis. J Biol Chem 2001; 276:39320-9.
20. Srinivasula SM, Poyet JL, Razmara M, Datta P, Zhang Z, Alnemri ES. The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J Biol Chem 2002; 277:21119-22.
21. Broz P, von Moltke J, Jones JW, Vance RE, Monack DM. Differential requirement for caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 2010; 8:471-83.
22. Leipe DD, Koonin EV, Aravind L. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 2004; 343:1-28.
23. Martinon F, Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004; 117:561-74.
24. Koonin EV, Aravind L. The NACHT family-a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci 2000; 25:223-4.
25. Inohara N, Nunez G. NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 2003; 3:371-82.
26. DeLaBarre B, Brunger AT. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nat Struct Biol 2003; 10:856-63.
27. Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 2009; 17:172-82.
28. Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 2005; 434:926-33.
29. Reubold TF, Wohlgemuth S, Eschenburg S. Crystal structure of full-length apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. Structure 2011; 19:1074-83.
30. Yuan S, Yu X, Topf M, Ludtke SJ, Wang X, Akey CW. Structure of an apoptosome-procaspase-9 CARD complex. Structure 2010; 18:571-83.
31. Yuan S, Yu X, Topf M etal. Structure of the Drosophila apoptosome at 6·9 a resolution. Structure 2011; 19:128-40.
32. Qi S, Pang Y, Hu Q etal. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 2010; 141:446-57.
33. Faustin B, Lartigue L, Bruey JM etal. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell 2007; 25:713-24.
34. Duncan JA, Bergstralh DT, Wang Y etal. Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. Proc Natl Acad Sci USA 2007; 104:8041-6.
35. Truhlar SM, Komives EA. LRR domain folding: just put a cap on it! Structure 2008; 16:655-7.
36. Liao KC, Mogridge J. Expression of Nlrp1b inflammasome components in human fibroblasts confers susceptibility to anthrax lethal toxin. Infect Immun 2009; 77:4455-62.
37. Mayor A, Martinon F, De Smedt T, Petrilli V, Tschopp J. A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat Immunol 2007; 8:497-503.
38. Shirasu K. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 2009; 60:139-64.
39. Kadota Y, Shirasu K, Guerois R. NLR sensors meet at the SGT1-HSP90 crossroad. Trends Biochem Sci 2009; 35:199-207.
40. Yuan S, Yu X, Asara JM, Heuser JE, Ludtke SJ, Akey CW. The holo-apoptosome: activation of procaspase-9 and interactions with caspase-3. Structure 2011; 19:1084-96.
41. Ting JP, Duncan JA, Lei Y. How the noninflammasome NLRs function in the innate immune system. Science 2010; 327:286-90.
42. Jha S, Ting JP. Inflammasome-associated nucleotide-binding domain, leucine-rich repeat proteins and inflammatory diseases. J Immunol 2009; 183:7623-9.
43. Bauernfeind F, Ablasser A, Bartok E etal. Inflammasomes: current understanding and open questions. Cell Mol Life Sci 2011; 68:765-83.
44. Bauernfeind FG, Horvath G, Stutz A etal. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 2009; 183:787-91.
45. 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.
46. Kahlenberg JM, Lundberg KC, Kertesy SB, Qu Y, Dubyak GR. Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-kappaB-driven protein synthesis. J Immunol 2005; 175:7611-22.
47. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003; 425:516-21.
48. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440:237-41.
49. Hornung V, Bauernfeind F, Halle A etal. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008; 9:847-56.
50. 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.
51. Halle A, Hornung V, Petzold GC etal. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008; 9:857-65.
52. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003; 552:335-44.
53. 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.
54. 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.
55. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010; 11:136-40.
56. Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010; 116:1570-3.
57. van Bruggen R, Koker MY, Jansen M etal. Human NLRP3 inflammasome activation is Nox1-4 independent. Blood 2010; 115:5398-400.
58. van de Veerdonk FL, Smeekens SP, Joosten LA etal. Reactive oxygen species-independent activation of the IL-1beta inflammasome in cells from patients with chronic granulomatous disease. Proc Natl Acad Sci USA 2010; 107:3030-3.
59. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469:221-5.
60. Nakahira K, Haspel JA, Rathinam VA etal. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-30.
61. Bulua AC, Simon A, Maddipati R etal. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 2011; 208:519-33.
62. Solle M, Labasi J, Perregaux DG etal. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 2001; 276:125-32.
63. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 2006; 25:5071-82.
64. Kanneganti TD, Lamkanfi M, Kim YG etal. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007; 26:433-43.
65. Marina-Garcia N, Franchi L, Kim YG etal. Pannexin-1-mediated intracellular delivery of muramyl dipeptide induces caspase-1 activation via cryopyrin/NLRP3 independently of Nod2. J Immunol 2008; 180:4050-7.
66. Qu Y, Misaghi S, Newton K etal. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 2011; 186:6553-61.
67. Fink SL, Bergsbaken T, Cookson BT. Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 2008; 105:4312-7.
68. Arlehamn CS, Petrilli V, Gross O, Tschopp J, Evans TJ. The role of potassium in inflammasome activation by bacteria. J Biol Chem 2010; 285:10508-18.
69. Muruve DA, Petrilli V, Zaiss AK etal. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008; 452:103-7.
70. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002; 10:417-26.
71. Hsu LC, Ali SR, McGillivray S etal. A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc Natl Acad Sci USA 2008; 105:7803-8.
72. Girardin SE, Boneca IG, Viala J etal. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 2003; 278:8869-72.
73. Ferwerda G, Kramer M, de Jong D etal. Engagement of NOD2 has a dual effect on proIL-1beta mRNA transcription and secretion of bioactive IL-1beta. Eur J Immunol 2008; 38:184-91.
74. Squires RC, Muehlbauer SM, Brojatsch J. Proteasomes control caspase-1 activation in anthrax lethal toxin-mediated cell killing. J Biol Chem 2007; 282:34260-7.
75. Wickliffe KE, Leppla SH, Moayeri M. Anthrax lethal toxin-induced inflammasome formation and caspase-1 activation are late events dependent on ion fluxes and the proteasome. Cell Microbiol 2008; 10:332-43.
76. Witola WH, Mui E, Hargrave A etal. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells. Infect Immun 2011; 79:756-66.
77. Zamboni DS, Kobayashi KS, Kohlsdorf T etal. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 2006; 7:318-25.
78. Suzuki T, Franchi L, Toma C etal. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 2007; 3:e111.
79. Miao EA, Ernst RK, Dors M, Mao DP, Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc Natl Acad Sci USA 2008; 105:2562-7.
80. Franchi L, Amer A, Body-Malapel M etal. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 2006; 7:576-82.
81. Miao EA, Andersen-Nissen E, Warren SE, Aderem A. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol 2007; 29:275-88.
82. Warren SE, Mao DP, Rodriguez AE, Miao EA, Aderem A. Multiple Nod-like receptors activate caspase 1 during Listeria monocytogenes infection. J Immunol 2008; 180:7558-64.
83. Miao EA, Mao DP, Yudkovsky N etal. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 2010; 107:3076-80.
84. Lightfield KL, Persson J, Brubaker SW etal. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 2008; 9:1171-8.
85. Lightfield KL, Persson J, Trinidad NJ etal. Differential requirements for NAIP5 in activation of the NLRC4 inflammasome. Infect Immun 2011; 79:1606-14.
86. Kofoed EM, Vance RE. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011; 477:592-5.
87. Hornung V, Latz E. Intracellular DNA recognition. Nat Rev Immunol 2010; 10:123-30.
88. Roberts TL, Idris A, Dunn JA etal. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009; 323:1057-60.
89. Panchanathan R, Shen H, Duan X etal. Aim2 deficiency in mice suppresses the expression of the inhibitory Fcgamma receptor (FcgammaRIIB) through the induction of the IFN-inducible p202, a lupus susceptibility protein. J Immunol 2011; 186:6762-70.
90. Kempster SL, Belteki G, Forhead AJ etal. Developmental control of the Nlrp6 inflammasome and a substrate, IL-18, in mammalian intestine. Am J Physiol Gastrointest Liver Physiol 2011; 300:G253-63.
91. Elinav E, Strowig T, Kau AL etal. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-57.
92. Normand S, Delanoye-Crespin A, Bressenot A etal. Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury. Proc Natl Acad Sci USA 2011; 108:9601-6.
93. Touitou I, Lesage S, McDermott M etal. Infevers: an evolving mutation database for auto-inflammatory syndromes. Hum Mutat 2004; 24:194-8.
94. Centola M, Wood G, Frucht DM etal. The gene for familial Mediterranean fever, MEFV, is expressed in early leukocyte development and is regulated in response to inflammatory mediators. Blood 2000; 95:3223-31.
95. Diaz A, Hu C, Kastner DL etal. Lipopolysaccharide-induced expression of multiple alternatively spliced MEFV transcripts in human synovial fibroblasts: a prominent splice isoform lacks the C-terminal domain that is highly mutated in familial Mediterranean fever. Arthritis Rheum 2004; 50:3679-89.
96. Yu JW, Wu J, Zhang Z etal. Cryopyrin and pyrin activate caspase-1, but not NF-kappaB, via ASC oligomerization. Cell Death Differ 2006; 13:236-49.
97. Chae JJ, Wood G, Masters SL etal. The B30·2 domain of pyrin, the familial Mediterranean fever protein, interacts directly with caspase-1 to modulate IL-1beta production. Proc Natl Acad Sci USA 2006; 103:9982-7.
98. Chae JJ, Komarow HD, Cheng J etal. Targeted disruption of pyrin, the FMF protein, causes heightened sensitivity to endotoxin and a defect in macrophage apoptosis. Mol Cell 2003; 11:591-604.
99. Chae JJ, Cho YH, Lee GS etal. Gain-of-function pyrin mutations induce NLRP3 protein-independent interleukin-1beta activation and severe autoinflammation in mice. Immunity 2011; 34:755-68.
100. Chae JJ, Wood G, Richard K etal. The familial Mediterranean fever protein, pyrin, is cleaved by caspase-1 and activates NF-kappaB through its N-terminal fragment. Blood 2008; 112:1794-803.