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Erschienen in: Immunologic Research 5-6/2016

03.10.2016 | Review

Inflammasomes and its importance in viral infections

verfasst von: Gaurav Shrivastava, Moisés León-Juárez, Julio García-Cordero, David Eduardo Meza-Sánchez, Leticia Cedillo-Barrón

Erschienen in: Immunologic Research | Ausgabe 5-6/2016

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Abstract

A complex interplay between pathogen and host determines the immune response during viral infection. A set of cytosolic sensors are expressed by immune cells to detect viral infection. NOD-like receptors (NLRs) comprise a large family of intracellular pattern recognition receptors. Members of the NLR family assemble into large multiprotein complexes, termed inflammasomes, which induce downstream immune responses to specific pathogens, environmental stimuli, and host cell damage. Inflammasomes are composed of cytoplasmic sensor molecules such as NLRP3 or absent in melanoma 2 (AIM2), the adaptor protein ASC (apoptosis-associated speck-like protein containing caspase recruitment domain), and the effector protein procaspase-1. The inflammasome operates as a platform for caspase-1 activation, resulting in caspase-1-dependent proteolytic maturation and secretion of interleukin (IL)-1β and IL-18. This, in turn, activates the expression of other immune genes and facilitates lymphocyte recruitment to the site of primary infection, thereby controlling invading pathogens. Moreover, inflammasomes counter viral replication and remove infected immune cells through an inflammatory cell death, program termed as pyroptosis. As a countermeasure, viral pathogens have evolved virulence factors to antagonise inflammasome pathways. In this review, we discuss the role of inflammasomes in sensing viral infection as well as the evasion strategies that viruses have developed to evade inflammasome-dependent immune responses. This information summarises our understanding of host defence mechanisms against viruses and highlights research areas that can provide new approaches to interfere in the pathogenesis of viral diseases.
Literatur
1.
Zurück zum Zitat Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol. 1997;9(1):4–9.PubMedCrossRef Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol. 1997;9(1):4–9.PubMedCrossRef
10.
Zurück zum Zitat Huang H, Saravia J, You D, Shaw AJ, Cormier SA. Impaired gamma delta T cell-derived IL-17A and inflammasome activation during early respiratory syncytial virus infection in infants. Immunol Cell Biol. 2014;. doi:10.1038/icb.2014.79.PubMedPubMedCentral Huang H, Saravia J, You D, Shaw AJ, Cormier SA. Impaired gamma delta T cell-derived IL-17A and inflammasome activation during early respiratory syncytial virus infection in infants. Immunol Cell Biol. 2014;. doi:10.​1038/​icb.​2014.​79.PubMedPubMedCentral
17.
Zurück zum Zitat 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(2):417–26.PubMedCrossRef 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(2):417–26.PubMedCrossRef
30.
Zurück zum Zitat Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev. 2011;243(1):136–51.PubMedCrossRef Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev. 2011;243(1):136–51.PubMedCrossRef
35.
Zurück zum Zitat 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(5):2871–9. doi:10.1074/jbc.M608083200.PubMedCrossRef 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(5):2871–9. doi:10.​1074/​jbc.​M608083200.PubMedCrossRef
40.
Zurück zum Zitat 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(Pt 13):2903–13. doi:10.1242/jcs.124388.PubMedCrossRef 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(Pt 13):2903–13. doi:10.​1242/​jcs.​124388.PubMedCrossRef
41.
Zurück zum Zitat Rossol M, Pierer M, Raulien N, et al. Extracellular Ca2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat Commun. 2012;3:1329.PubMedPubMedCentralCrossRef Rossol M, Pierer M, Raulien N, et al. Extracellular Ca2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat Commun. 2012;3:1329.PubMedPubMedCentralCrossRef
45.
Zurück zum Zitat Kanneganti TD, Body-Malapel M, Amer A, 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(48):36560–8. doi:10.1074/jbc.M607594200.PubMedCrossRef Kanneganti TD, Body-Malapel M, Amer A, 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(48):36560–8. doi:10.​1074/​jbc.​M607594200.PubMedCrossRef
49.
59.
Zurück zum Zitat McAuley JL, Tate MD, MacKenzie-Kludas CJ, et al. Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog. 2013;. doi:10.1371/journal.ppat.1003392. McAuley JL, Tate MD, MacKenzie-Kludas CJ, et al. Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog. 2013;. doi:10.​1371/​journal.​ppat.​1003392.
60.
Zurück zum Zitat Triantafilou K, Kar S, Vakakis E, Kotecha S, Triantafilou M. Human respiratory syncytial virus viroporin SH: a viral recognition pathway used by the host to signal inflammasome activation. Thorax. 2013;68(1):66–75. doi:10.1136/thoraxjnl-2012-202182.PubMedCrossRef Triantafilou K, Kar S, Vakakis E, Kotecha S, Triantafilou M. Human respiratory syncytial virus viroporin SH: a viral recognition pathway used by the host to signal inflammasome activation. Thorax. 2013;68(1):66–75. doi:10.​1136/​thoraxjnl-2012-202182.PubMedCrossRef
61.
Zurück zum Zitat Pontillo A, Silva LT, Oshiro TM, Finazzo C, Crovella S, Duarte AJS. HIV-1 induces NALP3-inflammasome expression and interleukin-1β secretion in dendritic cells from healthy individuals but not from HIV-positive patients. AIDS. 2012;26(1):11–8. doi:10.1097/QAD.0b013e32834d697f.PubMedCrossRef Pontillo A, Silva LT, Oshiro TM, Finazzo C, Crovella S, Duarte AJS. HIV-1 induces NALP3-inflammasome expression and interleukin-1β secretion in dendritic cells from healthy individuals but not from HIV-positive patients. AIDS. 2012;26(1):11–8. doi:10.​1097/​QAD.​0b013e32834d697f​.PubMedCrossRef
63.
69.
76.
Zurück zum Zitat Burckstummer T, Baumann C, Bluml S, et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol. 2009;10(3):266–72. doi:10.1038/ni.1702.PubMedCrossRef Burckstummer T, Baumann C, Bluml S, et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol. 2009;10(3):266–72. doi:10.​1038/​ni.​1702.PubMedCrossRef
80.
82.
Zurück zum Zitat Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol. 2004;5(7):730–7. doi:10.1038/ni1087.PubMedCrossRef Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol. 2004;5(7):730–7. doi:10.​1038/​ni1087.PubMedCrossRef
86.
Zurück zum Zitat Liu P, Jamaluddin M, Li K, Garofalo RP, Casola A, Brasier AR. Retinoic acid-inducible gene I mediates early antiviral response and Toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J Virol. 2007;81(3):1401–11. doi:10.1128/JVI.01740-06.PubMedCrossRef Liu P, Jamaluddin M, Li K, Garofalo RP, Casola A, Brasier AR. Retinoic acid-inducible gene I mediates early antiviral response and Toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J Virol. 2007;81(3):1401–11. doi:10.​1128/​JVI.​01740-06.PubMedCrossRef
90.
92.
Zurück zum Zitat Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M. Establishment and maintenance of the innate antiviral response to West Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol. 2008;82(2):609–16. doi:10.1128/JVI.01305-07.PubMedCrossRef Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M. Establishment and maintenance of the innate antiviral response to West Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol. 2008;82(2):609–16. doi:10.​1128/​JVI.​01305-07.PubMedCrossRef
95.
Zurück zum Zitat Poeck H, Bscheider M, Gross O, et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat Immunol. 2010;11(1):63–9. doi:10.1038/ni.1824.PubMedCrossRef Poeck H, Bscheider M, Gross O, et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1 beta production. Nat Immunol. 2010;11(1):63–9. doi:10.​1038/​ni.​1824.PubMedCrossRef
98.
102.
Zurück zum Zitat Moore CB, Bergstralh DT, Duncan JA, et al. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature. 2008;451(7178):573–7.PubMedCrossRef Moore CB, Bergstralh DT, Duncan JA, et al. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature. 2008;451(7178):573–7.PubMedCrossRef
104.
Zurück zum Zitat Arnoult D, Soares F, Tattoli I, Castanier C, Philpott DJ, Girardin SE. An N-terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J Cell Sci. 2009;122(Pt 17):3161–8.PubMedPubMedCentralCrossRef Arnoult D, Soares F, Tattoli I, Castanier C, Philpott DJ, Girardin SE. An N-terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J Cell Sci. 2009;122(Pt 17):3161–8.PubMedPubMedCentralCrossRef
105.
Zurück zum Zitat Lei Y, Wen H, Yu Y, et al. The mitochondrial proteins NLRX1 and TUFM form a complex that regulates type I interferon and autophagy. Immunity. 2012;36(6):933–46.PubMedPubMedCentralCrossRef Lei Y, Wen H, Yu Y, et al. The mitochondrial proteins NLRX1 and TUFM form a complex that regulates type I interferon and autophagy. Immunity. 2012;36(6):933–46.PubMedPubMedCentralCrossRef
106.
Zurück zum Zitat Lei Y, Wen H, Ting JPY. The NLR protein, NLRX1, and its partner, TUFM, reduce type I interferon, and enhance autophagy. Autophagy. 2013;9(3):432–3.PubMedPubMedCentralCrossRef Lei Y, Wen H, Ting JPY. The NLR protein, NLRX1, and its partner, TUFM, reduce type I interferon, and enhance autophagy. Autophagy. 2013;9(3):432–3.PubMedPubMedCentralCrossRef
107.
109.
Zurück zum Zitat Guo H, König R, Deng M, et al. NLRX1 sequesters STING to negatively regulate the interferon response, thereby facilitating the replication of HIV-1 and DNA viruses. Cell Host Microbe. 2016;19(4):515–28.PubMedCrossRef Guo H, König R, Deng M, et al. NLRX1 sequesters STING to negatively regulate the interferon response, thereby facilitating the replication of HIV-1 and DNA viruses. Cell Host Microbe. 2016;19(4):515–28.PubMedCrossRef
111.
Zurück zum Zitat Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006;8(11):1812–25.PubMedCrossRef Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006;8(11):1812–25.PubMedCrossRef
115.
Zurück zum Zitat de Gassart A, Martinon F. Pyroptosis: caspase-11 unlocks the gates of death. Immunity. 2015;43(5):835–7.PubMedCrossRef de Gassart A, Martinon F. Pyroptosis: caspase-11 unlocks the gates of death. Immunity. 2015;43(5):835–7.PubMedCrossRef
116.
Zurück zum Zitat Yang D, He Y, Muñoz-Planillo R, Liu Q, Núñez G. Caspase-11 requires the pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity. 2015;. doi:10.1016/j.immuni.2015.10.009. Yang D, He Y, Muñoz-Planillo R, Liu Q, Núñez G. Caspase-11 requires the pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity. 2015;. doi:10.​1016/​j.​immuni.​2015.​10.​009.
124.
Zurück zum Zitat Zamoshnikova A, Groß CJ, Schuster S, et al. NLRP12 is a neutrophil-specific, negative regulator of in vitro cell migration but does not modulate LPS- or infection-induced NF-κB or ERK signalling. Immunobiology. 2016;221(2):341–6. doi:10.1016/j.imbio.2015.10.001. Zamoshnikova A, Groß CJ, Schuster S, et al. NLRP12 is a neutrophil-specific, negative regulator of in vitro cell migration but does not modulate LPS- or infection-induced NF-κB or ERK signalling. Immunobiology. 2016;221(2):341–6. doi:10.​1016/​j.​imbio.​2015.​10.​001.
129.
Zurück zum Zitat Yang Q, Fu S, Wang J. Hepatitis C virus infection decreases the expression of Toll-like receptors 3 and 7 via upregulation of miR-758. Arch Virol. 2014. doi:10.1007/s00705-014-2167-3. Yang Q, Fu S, Wang J. Hepatitis C virus infection decreases the expression of Toll-like receptors 3 and 7 via upregulation of miR-758. Arch Virol. 2014. doi:10.​1007/​s00705-014-2167-3.
146.
Zurück zum Zitat Kettle S, Alcamí A, Khanna A, Ehret R, Jassoy C, Smith GL. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1beta-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1beta-induced fever. J Gen Virol. 1997;78(Pt 3):677–85.PubMedCrossRef Kettle S, Alcamí A, Khanna A, Ehret R, Jassoy C, Smith GL. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1beta-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1beta-induced fever. J Gen Virol. 1997;78(Pt 3):677–85.PubMedCrossRef
147.
Zurück zum Zitat Stasakova J. Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1 and 18. J Gen Virol. 2005;86(1):185–95. doi:10.1099/vir.0.80422-0.PubMedCrossRef Stasakova J. Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1 and 18. J Gen Virol. 2005;86(1):185–95. doi:10.​1099/​vir.​0.​80422-0.PubMedCrossRef
Metadaten
Titel
Inflammasomes and its importance in viral infections
verfasst von
Gaurav Shrivastava
Moisés León-Juárez
Julio García-Cordero
David Eduardo Meza-Sánchez
Leticia Cedillo-Barrón
Publikationsdatum
03.10.2016
Verlag
Springer US
Erschienen in
Immunologic Research / Ausgabe 5-6/2016
Print ISSN: 0257-277X
Elektronische ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-016-8873-z

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