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Pyroptosis in Antiviral Immunity

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Alternate Programmed Cell Death Signaling in Antiviral Host Defense

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 442))

Abstract

Pyroptosis is a form of lytic, programmed cell death that functions as an innate immune effector mechanism to facilitate host defense against pathogenic microorganisms, including viruses. This type of proinflammatory cell death is orchestrated by proteolytic activation of human or mouse caspase-1, mouse caspase-11 and human caspase-4 and caspase-5 in response to infectious and inflammatory stimuli. Induction of pyroptosis requires either a canonical inflammasome responsible for caspase-1 activation or a noncanonical complex composed of caspase-11 in mice or caspase-4 or caspase-5 in humans. Recent studies have identified the pore-forming protein gasdermin D, a substrate of these inflammatory caspases, as an executioner of pyroptosis. The membrane pores formed by gasdermin D facilitate release of proinflammatory cytokines IL-1β and IL-18 and consequent biologic effects of these cytokines together with other released components. Pyroptosis, like other forms of programmed cell death, helps eliminate infected cells and thereby restricts the replicative niche, undermining survival and proliferation of intracellular pathogens. This includes viruses as well as bacteria, where ample evidence supports a critical role for inflammasome effector functions and cell death in host defense. Viruses have evolved their own mechanisms to modulate inflammasome signaling and pyroptosis. Here, we review the current literature regarding the role of pyroptosis in antiviral immune responses.

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References

  • Aachoui Y, Leaf IA, Hagar JA, Fontana MF, Campos CG, Zak DE, Tan MH, Cotter PA, Vance RE, Aderem A, Miao EA (2013) Caspase-11 protects against bacteria that escape the vacuole. Science 339(6122):975–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aarreberg LD, Wilkins C, Ramos HJ, Green R, Davis MA, Chow K, Gale M, Jr (2018) Interleukin-1beta signaling in dendritic cells induces antiviral interferon responses. MBio 9(2)

    Google Scholar 

  • Aglietti RA, Estevez A, Gupta A, Ramirez MG, Liu PS, Kayagaki N, Ciferri C, Dixit VM, Dueber EC (2016) GsdmD p 30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc Natl Acad Sci USA 113(28):7858–7863

    Google Scholar 

  • Akhter A, Gavrilin MA, Frantz L, Washington S, Ditty C, Limoli D, Day C, Sarkar A, Newland C, Butchar J, Marsh CB, Wewers MD, Tridandapani S, Kanneganti TD, Amer AO (2009) Caspase-7 activation by the Nlrc4/Ipaf inflammasome restricts Legionella pneumophila infection. PLoS Pathog 5(4):e1000361

    Article  PubMed  PubMed Central  Google Scholar 

  • Ansari MA, Singh VV, Dutta S, Veettil MV, Dutta D, Chikoti L, Lu J, Everly D, Chandran B (2013) Constitutive interferon-inducible protein 16-inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J Virol 87(15):8606–8623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonopoulos C, Russo HM, El Sanadi C, Martin BN, Li X, Kaiser WJ, Mocarski ES, Dubyak GR (2015) Caspase-8 as an effector and regulator of NLRP3 inflammasome signaling. J Biol Chem 290(33):20167–20184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basil MC, Levy BD (2016) Specialized pro-resolving mediators: endogenous regulators of infection and inflammation. Nat Rev Immunol 16(1):51–67

    Article  CAS  PubMed  Google Scholar 

  • Boise LH, Collins CM (2001) Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol 9(2):64–67

    Article  CAS  PubMed  Google Scholar 

  • Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38(1):31–40

    Article  CAS  PubMed  Google Scholar 

  • Broz P, Dixit VM (2016) Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol 16(7):407–420

    Article  CAS  PubMed  Google Scholar 

  • Broz P, von Moltke J, Jones JW, Vance RE, Monack DM (2010) Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8(6):471–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen LM, Kaniga K, Galan JE (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21(5):1101–1115

    Article  CAS  PubMed  Google Scholar 

  • Chien H, Dix RD (2012) Evidence for multiple cell death pathways during development of experimental cytomegalovirus retinitis in mice with retrovirus-induced immunosuppression: apoptosis, necroptosis, and pyroptosis. J Virol 86(20):10961–10978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chirathaworn C, Rianthavorn P, Wuttirattanakowit N, Poovorawan Y (2010) Serum IL-18 and IL-18BP levels in patients with Chikungunya virus infection. Viral Immunol 23(1):113–117

    Article  CAS  PubMed  Google Scholar 

  • Chung WC, Kang HR, Yoon H, Kang SJ, Ting JP, Song MJ (2015) Influenza A virus NS1 protein inhibits the NLRP3 inflammasome. PLoS ONE 10(5):e0126456

    Article  PubMed  Google Scholar 

  • Cieniewicz B, Dong Q, Li G, Forrest JC, Mounce BC, Tarakanova VL, van der Velden A, Krug LT (2015) Murine gammaherpesvirus 68 pathogenesis is independent of caspase-1 and caspase-11 in mice and impairs interleukin-1β production upon extrinsic stimulation in culture. J Virol 89(13):6562–6574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cookson BT, Brennan MA (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9(3):113–114

    Article  CAS  PubMed  Google Scholar 

  • Davis MA, Fairgrieve MR, Den Hartigh A, Yakovenko O, Duvvuri B, Lood C, Thomas WE, Fink SL, Gale M, Jr (2019) Calpain drives pyroptotic vimentin cleavage, intermediate filament loss, and cell rupture that mediates immunostimulation. Proc Natl Acad Sci USA 116(11):5061–5070

    Google Scholar 

  • Denton AE, Doherty PC, Turner SJ, La Gruta NL (2007) IL-18, but not IL-12, is required for optimal cytokine production by influenza virus-specific CD8+ T cells. Eur J Immunol 37(2):368–375

    Article  CAS  PubMed  Google Scholar 

  • Diner BA, Lum KK, Cristea IM (2015) The emerging role of nuclear viral DNA sensors. J Biol Chem 290(44):26412–26421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, Sun H, Wang DC, Shao F (2016) Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535(7610):111–116

    Article  CAS  PubMed  Google Scholar 

  • Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, Hunt PW, Hatano H, Sowinski S, Munoz-Arias I, Greene WC (2014) Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505(7484):509–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doitsh G, Greene WC (2016) Dissecting how CD4 T cells are lost during HIV infection. Cell Host Microbe 19(3):280–291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dondelinger Y, Hulpiau P, Saeys Y, Bertrand MJM, Vandenabeele P (2016) An evolutionary perspective on the necroptotic pathway. Trends Cell Biol 26(10):721–732

    Article  CAS  PubMed  Google Scholar 

  • Dondelinger Y, Jouan-Lanhouet S, Divert T, Theatre E, Bertin J, Gough PJ, Giansanti P, Heck AJ, Dejardin E, Vandenabeele P, Bertrand MJ (2015) NF-kappaB-independent role of IKKalpha/IKKbeta in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol Cell 60(1):63–76

    Article  CAS  PubMed  Google Scholar 

  • Dorfleutner A, Talbott SJ, Bryan NB, Funya KN, Rellick SL, Reed JC, Shi X, Rojanasakul Y, Flynn DC, Stehlik C (2007) A shope fibroma virus PYRIN-only protein modulates the host immune response. Virus Genes 35(3):685–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichholz K, Bru T, Tran TT, Fernandes P, Welles H, Mennechet FJ, Manel N, Alves P, Perreau M, Kremer EJ (2016) Immune-complexed adenovirus induce AIM2-mediated pyroptosis in human dendritic cells. PLoS Pathog 12(9):e1005871

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458(7237):509–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fink SL, Cookson BT (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8(11):1812–1825

    Article  CAS  PubMed  Google Scholar 

  • Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, Monks C, Baba TW, Ruprecht RM, Kupfer A (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1(2):129–134

    Article  CAS  PubMed  Google Scholar 

  • Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, Farzan M, Inoue S, Jung JU, Garcia-Sastre A (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5(5):439–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galloway NL, Doitsh G, Monroe KM, Yang Z, Munoz-Arias I, Levy DN, Greene WC (2015) Cell-to-cell transmission of HIV-1 is required to trigger pyroptotic death of lymphoid-tissue-derived CD4 T cells. Cell Rep 12(10):1555–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerlic M, Faustin B, Postigo A, Yu EC, Proell M, Gombosuren N, Krajewska M, Flynn R, Croft M, Way M, Satterthwait A, Liddington RC, Salek-Ardakani S, Matsuzawa S, Reed JC (2013) Vaccinia virus F1L protein promotes virulence by inhibiting inflammasome activation. Proc Natl Acad Sci USA 110(19):7808–7813

    Google Scholar 

  • Gregory SM, Davis BK, West JA, Taxman DJ, Matsuzawa S, Reed JC, Ting JP, Damania B (2011) Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331(6015):330–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA (2013) Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341(6151):1250–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hale BG, Randall RE, Ortin J, Jackson D (2008) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89(Pt 10):2359–2376

    Article  CAS  PubMed  Google Scholar 

  • He WT, Wan H, Hu L, Chen P, Wang X, Huang Z, Yang ZH, Zhong CQ, Han J (2015) Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res 25(12):1285–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Z, Chen J, Zhu X, An S, Dong X, Yu J, Zhang S, Wu Y, Li G, Zhang Y, Wu J, Li M (2018) NLRP3 inflammasome activation mediates zika virus-associated inflammation. J Infect Dis 217(12):1942–1951

    Article  CAS  PubMed  Google Scholar 

  • Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A (1999) The salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96(5):2396–2401

    Google Scholar 

  • Hilbi H, Moss JE, Hersh D, Chen Y, Arondel J, Banerjee S, Flavell RA, Yuan J, Sansonetti PJ, Zychlinsky A (1998) Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273(49):32895–32900

    Article  CAS  PubMed  Google Scholar 

  • Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A (2009) Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206(1):79–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson KE, Chikoti L, Chandran B (2013) Herpes simplex virus 1 infection induces activation and subsequent inhibition of the IFI16 and NLRP3 inflammasomes. J Virol 87(9):5005–5018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston JB, Barrett JW, Nazarian SH, Goodwin M, Ricciuto D, Wang G, McFadden G (2005) A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23(6):587–598

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen I, Miao EA (2015) Pyroptotic cell death defends against intracellular pathogens. Immunol Rev 265(1):130–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jorgensen I, Rayamajhi M, Miao EA (2017) Programmed cell death as a defence against infection. Nat Rev Immunol 17(3):151–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jureka AS, Kleinpeter AB, Cornilescu G, Cornilescu CC, Petit CM (2015) Structural basis for a novel interaction between the NS1 protein derived from the 1918 Influenza virus and RIG-I. Structure (London, England: 1993) 23(11):2001–2010

    Google Scholar 

  • Kanneganti TD (2010) Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10(10):688–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaushik DK, Gupta M, Kumawat KL, Basu A (2012) NLRP3 inflammasome: key mediator of neuroinflammation in murine Japanese encephalitis. PLoS ONE 7(2):e32270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526(7575):666–671

    Article  CAS  PubMed  Google Scholar 

  • Kayagaki N, Warming S, Lamkanfi M, Walle L Vande, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479(7371):117–121

    Article  CAS  PubMed  Google Scholar 

  • Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341(6151):1246–1249

    Article  CAS  PubMed  Google Scholar 

  • Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, Chandran B (2011) IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9(5):363–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kesavardhana S, Kuriakose T, Guy CS, Samir P, Malireddi RKS, Mishra A, Kanneganti TD (2017) ZBP1/DAI ubiquitination and sensing of influenza vRNPs activate programmed cell death. J Exp Med 214(8):2217–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kip E, Naze F, Suin V, Berghe T Vanden, Francart A, Lamoral S, Vandenabeele P, Beyaert R, Van Gucht S, Kalai M (2017) Impact of caspase-1/11, -3, -7, or IL-1beta/IL-18 deficiency on rabies virus-induced macrophage cell death and onset of disease. Cell death Discov 3:17012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochs G, Garcia-Sastre A, Martinez-Sobrido L (2007) Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81(13):7011–7021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kofahi HM, Taylor NG, Hirasawa K, Grant MD, Russell RS (2016) Hepatitis C virus infection of cultured human hepatoma cells causes apoptosis and pyroptosis in both infected and bystander cells. Sci Rep 6:37433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komune N, Ichinohe T, Ito M, Yanagi Y (2011) Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1beta secretion. J Virol 85(24):13019–13026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuriakose T, Kanneganti TD (2017) Regulation and functions of NLRP3 inflammasome during influenza virus infection. Mol Immunol 86:56–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuriakose T, Man SM, Malireddi RK, Karki R, Kesavardhana S, Place DE, Neale G, Vogel P, Kanneganti TD (2016) ZBP1/DAI is an innate sensor of influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways. Sci Immunol 1(2):aag2045

    Google Scholar 

  • Lamkanfi M, Dixit VM (2011) Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 187(2):597–602

    Article  CAS  PubMed  Google Scholar 

  • Lamkanfi M, Kanneganti TD, Van Damme P, Vanden Berghe T, Vanoverberghe I, Vandekerckhove J, Vandenabeele P, Gevaert K, Nunez G (2008) Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol Cell Proteomics 7(12):2350–2363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei X, Zhang Z, Xiao X, Qi J, He B, Wang J (2017) Enterovirus 71 inhibits pyroptosis through cleavage of gasdermin D. J Virol 91(18):e01069-17

    Google Scholar 

  • Liu T, Tang L, Tang H, Pu J, Gong S, Fang D, Zhang H, Li YP, Zhu X, Wang W, Wu M, Liao Y, Li C, Zhou H, Huang X (2019) Zika virus infection induces acute kidney injury through activating NLRP3 inflammasome via suppressing Bcl-2. Front Immunol 10:1925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J (2016) Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535(7610):153–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lupfer C, Kanneganti TD (2013) The expanding role of NLRs in antiviral immunity. Immunol Rev 255(1):13–24

    Article  PubMed  PubMed Central  Google Scholar 

  • Lupfer C, Malik A, Kanneganti TD (2015) Inflammasome control of viral infection. Curr Opin Virol 12:38–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lupfer C, Thomas PG, Anand PK, Vogel P, Milasta S, Martinez J, Huang G, Green M, Kundu M, Chi H, Xavier RJ, Green DR, Lamkanfi M, Dinarello CA, Doherty PC, Kanneganti TD (2013) Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat Immunol 14(5):480–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malireddi RKS, Kesavardhana S, Kanneganti TD (2019) ZBP1 and TAK1: master regulators of NLRP3 inflammasome/pyroptosis, apoptosis, and necroptosis (PAN-optosis). Front Cell Infect Microbiol 9:406

    Google Scholar 

  • Man SM, Kanneganti TD (2015) Regulation of inflammasome activation. Immunol Rev 265(1):6–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Man SM, Karki R, Kanneganti TD (2017) Molecular mechanisms and functions of pyroptosis, inflammatory caspases and inflammasomes in infectious diseases. Immunol Rev 277(1):61–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10(2):417–426

    Article  CAS  PubMed  Google Scholar 

  • Masters SL, Gerlic M, Metcalf D, Preston S, Pellegrini M, O’Donnell JA, McArthur K, Baldwin TM, Chevrier S, Nowell CJ, Cengia LH, Henley KJ, Collinge JE, Kastner DL, Feigenbaum L, Hilton DJ, Alexander WS, Kile BT, Croker BA (2012) NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity 37(6):1009–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monack DM, Navarre WW, Falkow S (2001) Salmonella-induced macrophage death: the role of caspase-1 in death and inflammation. Microbes Infect 3(14–15):1201–1212

    Article  CAS  PubMed  Google Scholar 

  • Monack DM, Raupach B, Hromockyj AE, Falkow S (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93(18):9833–9838

    Google Scholar 

  • Monroe KM, Yang Z, Johnson JR, Geng X, Doitsh G, Krogan NJ, Greene WC (2014) IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343(6169):428–432

    Article  CAS  PubMed  Google Scholar 

  • Moriyama M, Chen IY, Kawaguchi A, Koshiba T, Nagata K, Takeyama H, Hasegawa H, Ichinohe T (2016) The RNA- and TRIM25-binding domains of influenza virus NS1 protein are essential for suppression of NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol 90(8):4105–4114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogusa S, Thapa RJ, Dillon CP, Liedmann S, Oguin TH 3rd, Ingram JP, Rodriguez DA, Kosoff R, Sharma S, Sturm O, Verbist K, Gough PJ, Bertin J, Hartmann BM, Sealfon SC, Kaiser WJ, Mocarski ES, Lopez CB, Thomas PG, Oberst A, Green DR, Balachandran S (2016) RIPK3 activates parallel pathways of MLKL-criven necroptosis and FADD-mediated apoptosis to protect against Influenza A virus. Cell Host Microbe 20(1):13–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orning P, Weng D, Starheim K, Ratner D, Best Z, Lee B, Brooks A, Xia S, Wu H, Kelliher MA, Berger SB, Gough PJ, Bertin J, Proulx MM, Goguen JD, Kayagaki N, Fitzgerald KA, Lien E (2018) Pathogen blockade of TAK1 triggers caspase-8-dependent cleavage of gasdermin D and cell death. Science 362(6418):1064–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pang IK, Ichinohe T, Iwasaki A (2013) IL-1R signaling in dendritic cells replaces pattern-recognition receptors in promoting CD8(+) T cell responses to influenza A virus. Nat Immunol 14(3):246–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park HS, Liu G, Thulasi Raman SN, Landreth SL, Liu Q, Zhou Y (2018) NS1 protein of 2009 pandemic influenza a virus inhibits porcine NLRP3 inflammasome-mediated interleukin-1β production by suppressing ASC ubiquitination. J Virol 92(8):e00022-18

    Google Scholar 

  • Pelegrin P, Barroso-Gutierrez C, Surprenant A (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J Immunol 180(11):7147–7157

    Article  CAS  PubMed  Google Scholar 

  • Poeck H, Bscheider M, Gross O, Finger K, Roth S, Rebsamen M, Hannesschlager N, Schlee M, Rothenfusser S, Barchet W, Kato H, Akira S, Inoue S, Endres S, Peschel C, Hartmann G, Hornung V, Ruland J (2010) Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production. Nat Immunol 11(1):63–69

    Article  CAS  PubMed  Google Scholar 

  • Pothlichet J, Meunier I, Davis BK, Ting JP, Skamene E, von Messling V, Vidal SM (2013) Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 9(4):e1003256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan LT, Caputo A, Bleackley RC, Pickup DJ, Salvesen GS (1995) Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J Biol Chem 270(18):10377–10379

    Article  CAS  PubMed  Google Scholar 

  • Rajan JV, Rodriguez D, Miao EA, Aderem A (2011) The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J Virol 85(9):4167–4172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajsbaum R, Albrecht RA, Wang MK, Maharaj NP, Versteeg GA, Nistal-Villan E, Garcia-Sastre A, Gack MU (2012) Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog 8(11):e1003059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos HJ, Lanteri MC, Blahnik G, Negash A, Suthar MS, Brassil MM, Sodhi K, Treuting PM, Busch MP, Norris PJ, Gale M Jr (2012) IL-1β signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog 8(11):e1003039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, Waggoner L, Vanaja SK, Monks BG, Ganesan S, Latz E, Hornung V, Vogel SN, Szomolanyi-Tsuda E, Fitzgerald KA (2010) The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11(5):395–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray CA, Black RA, Kronheim SR, Greenstreet TA, Sleath PR, Salvesen GS, Pickup DJ (1992) Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 69(4):597–604

    Article  CAS  PubMed  Google Scholar 

  • Rogers C, Fernandes-Alnemri T, Mayes L, Alnemri D, Cingolani G, Alnemri ES (2017) Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death. Nat Commun 8:14128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruhl S, Broz P (2015) Caspase-11 activates a canonical NLRP3 inflammasome by promoting K(+) efflux. Eur J Immunol 45(10):2927–2936

    Article  PubMed  Google Scholar 

  • Sarhan J, Liu BC, Muendlein HI, Li P, Nilson R, Tang AY, Rongvaux A, Bunnell SC, Shao F, Green DR, Poltorak A (2018) Caspase-8 induces cleavage of gasdermin D to elicit pyroptosis during Yersinia infection. Proc Natl Acad Sci USA 115(46):E10888–E10897

    Google Scholar 

  • Sborgi L, Ruhl S, Mulvihill E, Pipercevic J, Heilig R, Stahlberg H, Farady CJ, Muller DJ, Broz P, Hiller S (2016) GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J 35(16):1766–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitz N, Kurrer M, Bachmann MF, Kopf M (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 79(10):6441–6448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider KS, Gross CJ, Dreier RF, Saller BS, Mishra R, Gorka O, Heilig R, Meunier E, Dick MS, Cikovic T, Sodenkamp J, Medard G, Naumann R, Ruland J, Kuster B, Broz P, Gross O (2017) The inflammasome drives GSDMD-independent secondary pyroptosis and IL-1 release in the absence of caspase-1 protease activity. Cell Rep 21(13):3846–3859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma D, Kanneganti TD (2016) The cell biology of inflammasomes: mechanisms of inflammasome activation and regulation. J Cell Biol 213(6):617–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Gao W, Shao F (2017) Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci 42(4):245–254

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526(7575):660–665

    Article  CAS  PubMed  Google Scholar 

  • Shrivastava S, Mukherjee A, Ray R, Ray RB (2013) Hepatitis C virus induces interleukin-1β (IL-1β)/IL-18 in circulatory and resident liver macrophages. J Virol 87(22):12284–12290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh VV, Kerur N, Bottero V, Dutta S, Chakraborty S, Ansari MA, Paudel N, Chikoti L, Chandran B (2013) Kaposi’s sarcoma-associated herpesvirus latency in endothelial and B cells activates gamma interferon-inducible protein 16-mediated inflammasomes. J Virol 87(8):4417–4431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stasakova J, Ferko B, Kittel C, Sereinig S, Romanova J, Katinger H, Egorov A (2005) 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 1β and 18. J Gen Virol 86(Pt 1):185–195

    Article  CAS  PubMed  Google Scholar 

  • Stewart MK, Cookson BT (2016) Evasion and interference: intracellular pathogens modulate caspase-dependent inflammatory responses. Nat Rev Microbiol 14(6):346–359

    Article  CAS  PubMed  Google Scholar 

  • Stewart TL, Wasilenko ST, Barry M (2005) Vaccinia virus F1L protein is a tail-anchored protein that functions at the mitochondria to inhibit apoptosis. J Virol 79(2):1084–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suwanmanee S, Luplertlop N (2017) Immunopathogenesis of dengue virus-induced redundant cell death: apoptosis and pyroptosis. Viral Immunol 30(1):13–19

    Article  CAS  PubMed  Google Scholar 

  • Taabazuing CY, Okondo MC, Bachovchin DA (2017) Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in monocytes and macrophages. Cell Chem Biol 24(4):507–514

    Google Scholar 

  • Tan TY, Chu JJ (2013) Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol 94(Pt 10):2215–2220

    Article  CAS  PubMed  Google Scholar 

  • Tate MD, Mansell A (2018) An update on the NLRP3 inflammasome and influenza: the road to redemption or perdition? Curr Opin Immunol 54:80–85

    Article  CAS  PubMed  Google Scholar 

  • Tate MD, Ong JD, Dowling JK, McAuley JL, Robertson AB, Latz E, Drummond GR, Cooper MA, Hertzog PJ, Mansell A (2016) Reassessing the role of the NLRP3 inflammasome during pathogenic influenza A virus infection via temporal inhibition. Sci Rep 6:27912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tewari M, Telford WG, Miller RA, Dixit VM (1995) CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J Biol Chem 270(39):22705–22708

    Article  CAS  PubMed  Google Scholar 

  • Thapa RJ, Ingram JP, Ragan KB, Nogusa S, Boyd DF, Benitez AA, Sridharan H, Kosoff R, Shubina M, Landsteiner VJ, Andrake M, Vogel P, Sigal LJ, tenOever BR, Thomas PG, Upton JW, Balachandran S (2016) DAI senses influenza A virus genomic RNA and activates RIPK3-dependent cell death. Cell Host Microbe 20(5):674–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas PG, Dash P, Aldridge JR Jr, Ellebedy AH, Reynolds C, Funk AJ, Martin WJ, Lamkanfi M, Webby RJ, Boyd KL, Doherty PC, Kanneganti TD (2009) The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30(4):566–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torii Y, Kawada JI, Murata T, Yoshiyama H, Kimura H, Ito Y (2017) Epstein-Barr virus infection-induced inflammasome activation in human monocytes. PLoS One 12(4):e0175053

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Gao W, Shi X, Ding J, Liu W, He H, Wang K, Shao F (2017) Chemotherapy drugs induce pyroptosis through caspase-3 cleavage of a gasdermin. Nature 547:99–103

    Google Scholar 

  • Watson PR, Gautier AV, Paulin SM, Bland AP, Jones PW, Wallis TS (2000) Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect Immun 68(6):3744–3747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Ding S, Wang P, Wei Z, Pan W, Palm NW, Yang Y, Yu H, Li HB, Wang G, Lei X, de Zoete MR, Zhao J, Zheng Y, Chen H, Zhao Y, Jurado KA, Feng N, Shan L, Kluger Y, Lu J, Abraham C, Fikrig E, Greenberg HB, Flavell RA (2017) Nlrp9b inflammasome restricts rotavirus infection in intestinal epithelial cells. Nature 546(7660):667–670

    Google Scholar 

  • Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358(6382):167–169

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Research studies from our laboratory are supported by the US National Institutes of Health (AI101935, AI124346, AR056296 and CA163507 to T.-D.K.) and the American Lebanese Syrian Associated Charities (to T.-D.K.).

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The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Department of Immunology, St. Jude Children’s Research Hospital, MS #351, 262 Danny Thomas Place, 38105-3678, Memphis, TN, USA

    Teneema Kuriakose & Thirumala-Devi Kanneganti

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  1. Teneema Kuriakose
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  2. Thirumala-Devi Kanneganti
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Correspondence to Thirumala-Devi Kanneganti .

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  1. Department of Microbiology and Immunology, Emory University, Atlanta, GA, USA

    Edward S. Mocarski

  2. Department of Biological Sciences, Lehman College, Biology and Biochemistry Programs, The Graduate Center, City University of New York, Bronx, NY, USA

    Pratyusha Mandal

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Kuriakose, T., Kanneganti, TD. (2019). Pyroptosis in Antiviral Immunity. In: Mocarski, E.S., Mandal, P. (eds) Alternate Programmed Cell Death Signaling in Antiviral Host Defense. Current Topics in Microbiology and Immunology, vol 442. Springer, Cham. https://doi.org/10.1007/82_2019_189

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