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

Abstract

Host control over infectious disease relies on the ability of cells in multicellular organisms to detect and defend against pathogens to prevent disease. Evolution affords mammals with a wide variety of independent immune mechanisms to control or eliminate invading infectious agents. Many pathogens acquire functions to deflect these immune mechanisms and promote infection. Following successful invasion of a host, cell autonomous signaling pathways drive the production of inflammatory cytokines, deployment of restriction factors and induction of cell death. Combined, these innate immune mechanisms attract dendritic cells, neutrophils and macrophages as well as innate lymphoid cells such as natural killer cells that all help control infection. Eventually, the development of adaptive pathogen-specific immunity clears infection and provides immune memory of the encounter. For obligate intracellular pathogens such as viruses, diverse cell death pathways make a pivotal contribution to early control by eliminating host cells before progeny are produced. Pro-apoptotic caspase-8 activity (along with caspase-10 in humans) executes extrinsic apoptosis, a nonlytic form of cell death triggered by TNF family death receptors (DRs). Over the past two decades, alternate extrinsic apoptosis and necroptosis outcomes have been described. Programmed necrosis, or necroptosis, occurs when receptor interacting protein kinase 3 (RIPK3) activates mixed lineage kinase-like (MLKL), causing cell leakage. Thus, activation of DRs, toll-like receptors (TLRs) or pathogen sensor Z-nucleic acid binding protein 1 (ZBP1) initiates apoptosis as well as necroptosis if not blocked by virus-encoded inhibitors. Mammalian cell death pathways are blocked by herpesvirus- and poxvirus-encoded cell death suppressors. Growing evidence has revealed the importance of Z-nucleic acid sensor, ZBP1, in the cell autonomous recognition of both DNA and RNA virus infection. This volume will explore the detente between viruses and cells to manage death machinery and avoid elimination to support dissemination within the host animal.

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Abbreviations

ADAR:

Adenosine deaminase acting on RNA genes

BCL:

B-cell lymphoma

CASP:

Caspase

cFLIP:

Cellular FLICE inhibitory protein

DD:

Death domain

DRs:

Death receptors

DNA:

Deoxy-ribonucleic acid

DAI:

DNA-dependent activator of IFN regulatory factors

dsRNA:

Double-stranded RNA

FADD:

FAS-associated death domain

HSV:

Herpes simplex virus

HCMV:

Human cytomegalovirus

IFN:

Interferon

IFN:

Type-I interferon

IRF:

IFN-regulatory factor

ISG:

IFN-stimulated gene

MLKL:

Mixed lineage kinase-like

MCMV:

Murine cytomegalovirus

NK:

Natural killer

NLR:

NOD-like receptor

NF-κB:

Nuclear factor kappa B

PAMP:

Pathogen associated molecular pattern

PRR:

Pattern recognition receptor

PCD:

Programmed cell death

PKR:

Protein kinase R

RIPK:

Receptor interacting protein kinase

RHIM:

Receptor interacting protein homotypic interaction motif

ssRNA:

Ribonucleic acid

TLRs:

Toll-like receptors

TNF:

Tumor necrosis factor

TNFR:

TNF receptor

VACV:

Vaccinia virus

wt:

Wild type

Z-NA:

Z-form nucleic acid

Zα:

Z-nucleic acid binding

ZBP1:

Z-nucleic acid binding protein 1

References

  • Águeda-Pinto A, Alves LQ, Neves F, McFadden G, Jacobs BL, Castro LFC, Rahman MM, Esteves PJ (2021) Convergent loss of the necroptosis pathway in disparate mammalian lineages shapes viruses countermeasures. Front Immunol 12:747737

    Article  PubMed  PubMed Central  Google Scholar 

  • Albert ML (2004) Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol 4(3):223–231

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Diaz S, Dillon CP, Lalaoui N, Tanzer MC, Rodriguez DA, Lin A, Lebois M, Hakem R, Josefsson EC, O’Reilly LA, Silke J, Alexander WS, Green DR, Strasser A (2016) The pseudokinase MLKL and the kinase RIPK3 have distinct roles in autoimmune disease caused by loss of death-receptor-induced apoptosis. Immunity 45(3):513–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Athanasiadis A (2012) Zalpha-domains: at the intersection between RNA editing and innate immunity. Semin Cell Dev Biol 23(3):275–280

    Article  CAS  PubMed  Google Scholar 

  • Balachandran S, Mocarski ES (2021) Viral Z-RNA triggers ZBP1-dependent cell death. Curr Opin Virol 51:134–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber GN (2001) Host defense, viruses and apoptosis. Cell Death Differ 8(2):113–126

    Article  CAS  PubMed  Google Scholar 

  • Bedoui S, Herold MJ, Strasser A (2020) Emerging connectivity of programmed cell death pathways and its physiological implications. Nat Rev Mol Cell Biol 21(11):678–695

    Article  CAS  PubMed  Google Scholar 

  • Beg AA, Sha WC, Bronson RT, Ghosh S, Baltimore D (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376(6536):167–170

    Article  CAS  PubMed  Google Scholar 

  • Berger SB, Kasparcova V, Hoffman S, Swift B, Dare L, Schaeffer M, Capriotti C, Cook M, Finger J, Hughes-Earle A, Harris PA, Kaiser WJ, Mocarski ES, Bertin J, Gough PJ (2014) Cutting edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J Immunol 192:5476–5480

    Article  CAS  PubMed  Google Scholar 

  • Berry R, Watson GM, Jonjic S, Degli-Esposti MA, Rossjohn J (2020) Modulation of innate and adaptive immunity by cytomegaloviruses. Nat Rev Immunol 20(2):113–127

    Article  CAS  PubMed  Google Scholar 

  • Bidere N, Su HC, Lenardo MJ (2006) Genetic disorders of programmed cell death in the immune system. Annu Rev Immunol 24:321–352

    Article  CAS  PubMed  Google Scholar 

  • Bonnet MC, Preukschat D, Welz PS, van Loo G, Ermolaeva MA, Bloch W, Haase I, Pasparakis M (2011) The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 35(4):572–582

    Article  CAS  PubMed  Google Scholar 

  • Brandt T, Heck MC, Vijaysri S, Jentarra GM, Cameron JM, Jacobs BL (2005) The N-terminal domain of the vaccinia virus E3L-protein is required for neurovirulence, but not induction of a protective immune response. Virology 333(2):263–270

    Article  CAS  PubMed  Google Scholar 

  • Brune W, Andoniou CE (2017) Die another day: inhibition of cell death pathways by cytomegalovirus. Viruses 9(9):249

    Google Scholar 

  • Brune W, Menard C, Heesemann J, Koszinowski UH (2001) A ribonucleotide reductase homolog of cytomegalovirus and endothelial cell tropism. Science 291(5502):303–305

    Article  CAS  PubMed  Google Scholar 

  • Ch’en IL, Hedrick SM, Hoffmann A (2008) NF-κB as a determinant of distinct cell death pathways. Methods Enzymol 446:175–187

    Article  PubMed  Google Scholar 

  • Ch’en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM (2011) Mechanisms of necroptosis in T cells. J Exp Med 208(4):633–641

    Article  PubMed  PubMed Central  Google Scholar 

  • Chan FK, Luz NF, Moriwaki K (2015) Programmed necrosis in the cross talk of cell death and inflammation. Annu Rev Immunol 33:79–106

    Article  CAS  PubMed  Google Scholar 

  • Chan YK, Gack MU (2016) Viral evasion of intracellular DNA and RNA sensing. Nat Rev Microbiol 14(6):360–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao DT, Korsmeyer SJ (1998) BCL-2 family: regulators of cell death. Annu Rev Immunol 16:395–419

    Article  CAS  PubMed  Google Scholar 

  • Chaudhry MZ, Casalegno-Garduno R, Sitnik KM, Kasmapour B, Pulm AK, Brizic I, Eiz-Vesper B, Moosmann A, Jonjic S, Mocarski ES, Cicin-Sain L (2020) Cytomegalovirus inhibition of extrinsic apoptosis determines fitness and resistance to cytotoxic CD8 T cells. Proc Natl Acad Sci U S A 117(23):12961–12968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chauhan D, Vande Walle L, Lamkanfi M (2020) Therapeutic modulation of inflammasome pathways. Immunol Rev 297(1):123–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen KW, Brodsky IE (2023) Yersinia interactions with regulated cell death pathways. Curr Opin Microbiol 71:102256

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Gullett JM, Tweedell RE, Kanneganti TD (2023) Innate immune inflammatory cell death: PANoptosis and PANoptosomes in host defense and disease. Eur J Immunol:e2250235

    Google Scholar 

  • Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137(6):1112–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christgen S, Zheng M, Kesavardhana S, Karki R, Malireddi RKS, Banoth B, Place DE, Briard B, Sharma BR, Tuladhar S, Samir P, Burton A, Kanneganti TD (2020) Identification of the PANoptosome: a molecular platform triggering pyroptosis, apoptosis, and necroptosis (PANoptosis). Front Cell Infect Microbiol 10:237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cicin-Sain L, Ruzsics Z, Podlech J, Bubic I, Menard C, Jonjic S, Reddehase MJ, Koszinowski UH (2008) Dominant-negative FADD rescues the in vivo fitness of a cytomegalovirus lacking an antiapoptotic viral gene. J Virol 82(5):2056–2064

    Article  CAS  PubMed  Google Scholar 

  • Clarke P, Tyler KL (2009) Apoptosis in animal models of virus-induced disease. Nat Rev Microbiol 7(2):144–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM (1995) Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 270(27):15974–15978

    Article  CAS  PubMed  Google Scholar 

  • Conos SA, Chen KW, De Nardo D, Hara H, Whitehead L, Núñez G, Masters SL, Murphy JM, Schroder K, Vaux DL, Lawlor KE, Lindqvist LM, Vince JE (2017) Active MLKL triggers the NLRP3 inflammasome in a cell-intrinsic manner. Proc Natl Acad Sci U S A 114(6):E961-e969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Consonni F, Gambineri E, Favre C (2022) ALPS, FAS, and beyond: from inborn errors of immunity to acquired immunodeficiencies. Ann Hematol 101(3):469–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cronk JM, Fafoutis E, Brown MG (2021) Licensing natural killers for antiviral immunity. Pathogens (Basel, Switzerland) 10(7):908

    Google Scholar 

  • Daley-Bauer LP, Roback L, Crosby LN, McCormick AL, Feng Y, Kaiser WJ, Mocarski ES (2017) Mouse cytomegalovirus M36 and M45 death suppressors cooperate to prevent inflammation resulting from antiviral programmed cell death pathways. Proc Natl Acad Sci U S A 114(13):E2786–E2795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116(2):205–219

    Article  CAS  PubMed  Google Scholar 

  • Daniels BP, Snyder AG, Olsen TM, Orozco S, Oguin TH 3rd, Tait SW, Martinez J, Gale M Jr, Loo YM, Oberst A (2017) RIPK3 restricts viral pathogenesis via cell death-independent neuroinflammation. Cell 169(2):301-313.e311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C, Wachsmuth L, Eftychi C, Lin J, Corona T, Hermance N, Zelic M, Kirsch P, Basic M, Bleich A, Kelliher M, Pasparakis M (2014) RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 513(7516):90–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BR (2001) Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol 69(6):912–920

    Article  PubMed  Google Scholar 

  • DeAntoneo C, Danthi P, Balachandran S (2022) Reovirus activated cell death pathways. Cells 11(11):1757

    Google Scholar 

  • DeFilippis VR, Alvarado D, Sali T, Rothenburg S, Fruh K (2010) Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 84(1):585–598

    Article  CAS  PubMed  Google Scholar 

  • Degterev A, Yuan J (2008) Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9(5):378–390

    Article  CAS  PubMed  Google Scholar 

  • Demarco B, Chen KW, Broz P (2020a) Cross talk between intracellular pathogens and cell death. Immunol Rev 297(1):174–193

    Article  CAS  PubMed  Google Scholar 

  • Demarco B, Grayczyk JP, Bjanes E, Le Roy D, Tonnus W, Assenmacher CA, Radaelli E, Fettrelet T, Mack V, Linkermann A, Roger T, Brodsky IE, Chen KW, Broz P (2020b) Caspase-8-dependent gasdermin D cleavage promotes antimicrobial defense but confers susceptibility to TNF-induced lethality. Sci Adv 6(47):eabc3465

    Google Scholar 

  • Dillon CP, Oberst A, Weinlich R, Janke LJ, Kang TB, Ben-Moshe T, Mak TW, Wallach D, Green DR (2012) Survival function of the FADD-Caspase-8-cFLIP(L) complex. Cell Rep 1:401–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dillon CP, Weinlich R, Rodriguez DA, Cripps JG, Quarato G, Gurung P, Verbist KC, Brewer TL, Llambi F, Gong YN, Janke LJ, Kelliher MA, Kanneganti TD, Green DR (2014) RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 157(5):1189–1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doerflinger M, Deng Y, Whitney P, Salvamoser R, Engel S, Kueh AJ, Tai L, Bachem A, Gressier E, Geoghegan ND, Wilcox S, Rogers KL, Garnham AL, Dengler MA, Bader SM, Ebert G, Pearson JS, De Nardo D, Wang N, Yang C, Pereira M, Bryant CE, Strugnell RA, Vince JE, Pellegrini M, Strasser A, Bedoui S, Herold MJ (2020) Flexible usage and interconnectivity of diverse cell death pathways protect against intracellular infection. Immunity 53(3):533-547.e537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dubin G, Fishman NO, Eisenberg RJ, Cohen GH, Friedman HM (1992) The role of herpes simplex virus glycoproteins in immune evasion. Curr Top Microbiol Immunol 179:111–120

    CAS  PubMed  Google Scholar 

  • Ellis RE, Yuan JY, Horvitz HR (1991) Mechanisms and functions of cell death. Annu Rev Cell Biol 7:663–698

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Yang Y, Mei Y, Ma L, Zhu DE, Hoti N, Castanares M, Wu M (2007) Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 19(10):2056–2067

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Daley-Bauer LP, Mocarski ES (2019a) Caspase-8-dependent control of NK- and T cell responses during cytomegalovirus infection. Med Microbiol Immunol 208:555–571

    Google Scholar 

  • Feng Y, Daley-Bauer LP, Roback L, Guo H, Koehler HS, Potempa M, Lanier LL, Mocarski ES (2019b) Caspase-8 restricts antiviral CD8 T cell hyperaccumulation. Proc Natl Acad Sci U S A 116(30):15170–15177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Daley-Bauer LP, Roback L, Potempa M, Lanier LL, Mocarski ES (2019c) Caspase-8 restricts natural killer cell accumulation during MCMV Infection. Med Microbiol Immunol 208(3–4):543–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Livingston-Rosanoff D, Roback L, Sundararajan A, Speck SH, Mocarski ES, Daley-Bauer LP (2018) Remarkably robust antiviral immune response despite combined deficiency in caspase-8 and RIPK3. J Immunol 201(8):2244–2255

    Article  CAS  PubMed  Google Scholar 

  • Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, Hupe M, Cain K, Macfarlane M, Hacker G, Leverkus M (2011) cIAPs block ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 43:449–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finlay BB, McFadden G (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124(4):767–782

    Article  CAS  PubMed  Google Scholar 

  • Fletcher-Etherington A, Nobre L, Nightingale K, Antrobus R, Nichols J, Davison AJ, Stanton RJ, Weekes MP (2020) Human cytomegalovirus protein pUL36: a dual cell death pathway inhibitor. Proc Natl Acad Sci U S A 117(31):18771–18779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritsch M, Günther SD, Schwarzer R, Albert MC, Schorn F, Werthenbach JP, Schiffmann LM, Stair N, Stocks H, Seeger JM, Lamkanfi M, Krönke M, Pasparakis M, Kashkar H (2019) Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis. Nature 575(7784):683–687

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Comella N, Tognazzi K, Brown LF, Dvorak HF, Kocher O (1999) Cloning of DLM-1, a novel gene that is up-regulated in activated macrophages, using RNA differential display. Gene 240(1):157–163

    Article  CAS  PubMed  Google Scholar 

  • Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G (2008) Viral control of mitochondrial apoptosis. PLoS Pathog 4(5):e1000018

    Article  PubMed  PubMed Central  Google Scholar 

  • Galluzzi L, Kepp O, Chan FK, Kroemer G (2017) Necroptosis: mechanisms and relevance to disease. Annu Rev Pathol 12:103–130

    Article  CAS  PubMed  Google Scholar 

  • Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, Annicchiarico-Petruzzelli M, Antonov AV, Arama E, Baehrecke EH, Barlev NA, Bazan NG, Bernassola F, Bertrand MJM, Bianchi K, Blagosklonny MV, Blomgren K, Borner C, Boya P, Brenner C, Campanella M, Candi E, Carmona-Gutierrez D, Cecconi F, Chan FK, Chandel NS, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Cohen GM, Conrad M, Cubillos-Ruiz JR, Czabotar PE, D'Angiolella V, Dawson TM, Dawson VL, De Laurenzi V, De Maria R, Debatin KM, DeBerardinis RJ, Deshmukh M, Di Daniele N, Di Virgilio F, Dixit VM, Dixon SJ, Duckett CS, Dynlacht BD, El-Deiry WS, Elrod JW, Fimia GM, Fulda S, García-Sáez AJ, Garg AD, Garrido C, Gavathiotis E, Golstein P, Gottlieb E, Green DR, Greene LA, Gronemeyer H, Gross A, Hajnoczky G, Hardwick JM, Harris IS, Hengartner MO, Hetz C, Ichijo H, Jäättelä M, Joseph B, Jost PJ, Juin PP, Kaiser WJ, Karin M, Kaufmann T, Kepp O, Kimchi A, Kitsis RN, Klionsky DJ, Knight RA, Kumar S, Lee SW, Lemasters JJ, Levine B, Linkermann A, Lipton SA, Lockshin RA, López-Otín C, Lowe SW, Luedde T, Lugli E, MacFarlane M, Madeo F, Malewicz M, Malorni W, Manic G, Marine JC, Martin SJ, Martinou JC, Medema JP, Mehlen P, Meier P, Melino S, Miao EA, Molkentin JD, Moll UM, Muñoz-Pinedo C, Nagata S, Nuñez G, Oberst A, Oren M, Overholtzer M, Pagano M, Panaretakis T, Pasparakis M, Penninger JM, Pereira DM, Pervaiz S, Peter ME, Piacentini M, Pinton P, Prehn JHM, Puthalakath H, Rabinovich GA, Rehm M, Rizzuto R, Rodrigues CMP, Rubinsztein DC, Rudel T, Ryan KM, Sayan E, Scorrano L, Shao F, Shi Y, Silke J, Simon HU, Sistigu A, Stockwell BR, Strasser A, Szabadkai G, Tait SWG, Tang D, Tavernarakis N, Thorburn A, Tsujimoto Y, Turk B, Vanden Berghe T, Vandenabeele P, Vander Heiden MG, Villunger A, Virgin HW, Vousden KH, Vucic D, Wagner EF, Walczak H, Wallach D, Wang Y, Wells JA, Wood W, Yuan J, Zakeri Z, Zhivotovsky B, Zitvogel L, Melino G, Kroemer G (2018) Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death. Cell Death Differ 25(3):486–541

    Google Scholar 

  • Goldstein ME, Scull MA (2021) Modeling innate antiviral immunity in physiological context. J Mol Biol:167374

    Google Scholar 

  • Gooding LR (1992) Virus proteins that counteract host immune defenses. Cell 71(1):5–7

    Article  CAS  PubMed  Google Scholar 

  • Gooding LR, Elmore LW, Tollefson AE, Brady HA, Wold WS (1988) A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. Cell 53(3):341–346

    Article  CAS  PubMed  Google Scholar 

  • Goodrum F, Britt W, Mocarski ES (2021) Cytomegalovirus. In: Knipe DM, Howley PM (eds) Fields virology, 7th edn. Wolters Kluwer Inc., Philadelphia, pp 389–444

    Google Scholar 

  • Green DR (2022) Cell death in development. Cold Spring Harb Perspect Biol 14(4)

    Google Scholar 

  • Guicciardi ME, Malhi H, Mott JL, Gores GJ (2013) Apoptosis and necrosis in the liver. Compr Physiol 3(2):977–1010

    Article  PubMed  Google Scholar 

  • Guo H, Gilley RP, Fisher A, Lane R, Landsteiner VJ, Ragan KB, Dovey CM, Carette JE, Upton JW, Mocarski ES, Kaiser WJ (2018) Species-independent contribution of ZBP1/DAI/DLM-1-triggered necroptosis in host defense against HSV1. Cell Death Dis 9(8):816

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo H, Kaiser WJ, Mocarski ES (2015a) Manipulation of apoptosis and necroptosis signaling by herpesviruses. Med Microbiol Immunol 204(3):439–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Koehler HS, Dix RD, Mocarski ES (2022a) Programmed cell death-dependent host defense in ocular herpes simplex virus infection. Front Microbiol 13:869064

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo H, Koehler HS, Mocarski ES, Dix RD (2022b) RIPK3 and caspase 8 collaborate to limit herpes simplex encephalitis. PLoS Pathog 18(9):e1010857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Omoto S, Harris PA, Finger JN, Bertin J, Gough PJ, Kaiser WJ, Mocarski ES (2015b) Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe 17(2):243–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardwick JM, Chen YB, Jonas EA (2012) Multipolar functions of BCL-2 proteins link energetics to apoptosis. Trends Cell Biol 22(6):318–328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann BM, Albrecht RA, Zaslavsky E, Nudelman G, Pincas H, Marjanovic N, Schotsaert M, Martinez-Romero C, Fenutria R, Ingram JP, Ramos I, Fernandez-Sesma A, Balachandran S, Garcia-Sastre A, Sealfon SC (2017) Pandemic H1N1 influenza A viruses suppress immunogenic RIPK3-driven dendritic cell death. Nat Commun 8(1):1931

    Google Scholar 

  • He S, Liang Y, Shao F, Wang X (2011) Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci U S A 108(50):20054–20059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137(6):1100–1111

    Article  CAS  PubMed  Google Scholar 

  • Hedrick SM, Ch’en IL, Alves BN (2010) Intertwined pathways of programmed cell death in immunity. Immunol Rev 236:41–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hengartner MO, Horvitz HR (1994) The ins and outs of programmed cell death during C. elegans development. Philos Trans R Soc Lond B Biol Sci 345(1313):243–246

    Google Scholar 

  • Herbert A (2019) Z-DNA and Z-RNA in human disease. Commun Biol 2:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Herzer K, Sprinzl MF, Galle PR (2007) Hepatitis viruses: live and let die. Liver Int 27(3):293–301

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Wu SQ, Liang Y, Zhou X, Chen W, Li L, Wu J, Zhuang Q, Chen C, Li J, Zhong CQ, **a W, Zhou R, Zheng C, Han J (2015) RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host Microbe 17(2):229–242

    Article  CAS  PubMed  Google Scholar 

  • Huttmann J, Krause E, Schommartz T, Brune W (2015) Functional comparison of molluscum contagiosum virus vFLIP MC159 with murine cytomegalovirus M36/vICA and M45/vIRA proteins. J Virol 90(6):2895–2905

    Article  PubMed  Google Scholar 

  • Ingram JP, Thapa RJ, Fisher A, Tummers B, Zhang T, Yin C, Rodriguez DA, Guo H, Lane R, Williams R, Slifker MJ, Basagoudanavar SH, Rall GF, Dillon CP, Green DR, Kaiser WJ, Balachandran S (2019) ZBP1/DAI drives RIPK3-mediated cell death induced by IFNs in the absence of RIPK1. J Immunol 203(5):1348–1355

    Article  CAS  PubMed  Google Scholar 

  • Ishii KJ, Kawagoe T, Koyama S, Matsui K, Kumar H, Kawai T, Uematsu S, Takeuchi O, Takeshita F, Coban C, Akira S (2008) TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451(7179):725–729

    Article  CAS  PubMed  Google Scholar 

  • James ER, Green DR (2002) Infection and the origins of apoptosis. Cell Death Differ 9(4):355–357

    Article  CAS  PubMed  Google Scholar 

  • Johnston JB, McFadden G (2004) Technical knockout: understanding poxvirus pathogenesis by selectively deleting viral immunomodulatory genes. Cell Microbiol 6(8):695–705

    Article  CAS  PubMed  Google Scholar 

  • Jones TR, Wiertz EJ, Sun L, Fish KN, Nelson JA, Ploegh HL (1996) Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci U S A 93(21):11327–11333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Justice JL, Cristea IM (2022) Nuclear antiviral innate responses at the intersection of DNA sensing and DNA repair. Trends Microbiol 30(11):1056–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WJ, Daley-Bauer LP, Thapa RJ, Mandal P, Berger SB, Huang C, Sundararajan A, Guo H, Roback L, Speck SH, Bertin J, Gough PJ, Balachandran S, Mocarski ES (2014) RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition. Proc Natl Acad Sci U S A 111:7753–7758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WJ, Offermann MK (2005) Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J Immunol 174(8):4942–4952

    Article  CAS  PubMed  Google Scholar 

  • Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW, Gough PJ, Sehon CA, Marquis RW, Bertin J, Mocarski ES (2013a) Toll-like receptor 3-mediated necrosis via TRIF, RIP3 and MLKL. J Biol Chem 288:31268–31279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, Caspary T, Mocarski ES (2011) RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471(7338):368–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WJ, Upton JW, Mocarski ES (2008) Receptor-interacting protein homotypic interaction motif-dependent control of NF-κ B activation via the DNA-dependent activator of IFN regulatory factors. J Immunol 181(9):6427–6434

    Article  CAS  PubMed  Google Scholar 

  • Kaiser WJ, Upton JW, Mocarski ES (2013b) Viral modulation of programmed necrosis. Curr Opin Virol 3(3):296–306

    Article  CAS  PubMed  Google Scholar 

  • Kang TB, Ben-Moshe T, Varfolomeev EE, Pewzner-Jung Y, Yogev N, Jurewicz A, Waisman A, Brenner O, Haffner R, Gustafsson E, Ramakrishnan P, Lapidot T, Wallach D (2004) Caspase-8 serves both apoptotic and nonapoptotic roles. J Immunol 173(5):2976–2984

    Article  CAS  PubMed  Google Scholar 

  • Kang TB, Jeong JS, Yang SH, Kovalenko A, Wallach D (2018) Caspase-8 deficiency in mouse embryos triggers chronic RIPK1-dependent activation of inflammatory genes, independently of RIPK3. Cell Death Differ 25(6):1107–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karki R, Sharma BR, Tuladhar S, Williams EP, Zalduondo L, Samir P, Zheng M, Sundaram B, Banoth B, Malireddi RKS, Schreiner P, Neale G, Vogel P, Webby R, Jonsson CB, Kanneganti TD (2021) Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell 184(1):149-168.e117

    Article  CAS  PubMed  Google Scholar 

  • Katze MG, He Y, Gale M Jr (2002) Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2(9):675–687

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann SH, Hengartner MO (2001) Programmed cell death: alive and well in the new millennium. Trends Cell Biol 11(12):526–534

    Article  CAS  PubMed  Google Scholar 

  • Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S (1998) Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol 143(5):1353–1360

    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, Vande Walle L, 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 

  • Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P (1998) The death domain kinase RIP mediates the TNF-induced NF-κB signal. Immunity 8(3):297–303

    Article  CAS  PubMed  Google Scholar 

  • Kennedy NJ, Kataoka T, Tschopp J, Budd RC (1999) Caspase activation is required for T cell proliferation. J Exp Med 190(12):1891–1896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257

    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 

  • Kesavardhana S, Malireddi RKS, Burton AR, Porter SN, Vogel P, Pruett-Miller SM, Kanneganti TD (2020a) The Zα2 domain of ZBP1 is a molecular switch regulating influenza-induced PANoptosis and perinatal lethality during development. J Biol Chem 295(24):8325–8330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kesavardhana S, Malireddi RKS, Kanneganti TD (2020b) Caspases in cell death, inflammation, and pyroptosis. Annu Rev Immunol 38:567–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YG, Muralinath M, Brandt T, Pearcy M, Hauns K, Lowenhaupt K, Jacobs BL, Rich A (2003) A role for Z-DNA binding in vaccinia virus pathogenesis. Proc Natl Acad Sci U S A 100(12):6974–6979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koehler H, Cotsmire S, Langland J, Kibler KV, Kalman D, Upton JW, Mocarski ES, Jacobs BL (2017) Inhibition of DAI-dependent necroptosis by the Z-DNA binding domain of the vaccinia virus innate immune evasion protein, E3. Proc Natl Acad Sci U S A 114(43):11506–11511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koehler H, Cotsmire S, Zhang T, Balachandran S, Upton JW, Langland J, Kalman D, Jacobs BL, Mocarski ES (2021) Vaccinia virus E3 prevents sensing of Z-RNA to block ZBP1-dependent necroptosis. Cell Host Microbe 29(8):1266–1276 e1265

    Google Scholar 

  • Krause E, de Graaf M, Fliss PM, Dolken L, Brune W (2014) Murine cytomegalovirus virion-associated protein M45 mediates rapid NF-κB activation after infection. J Virol 88(17):9963–9975

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267(5206):2000–2003

    Article  CAS  PubMed  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, Kanneganti TD (2018) ZBP1: Innate sensor regulating cell death and inflammation. Trends Immunol 39(2):123–134

    Article  CAS  PubMed  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 

  • Kuriakose T, Zheng M, Neale G, Kanneganti TD (2018) IRF1 is a transcriptional regulator of ZBP1 promoting NLRP3 inflammasome activation and cell death during influenza virus infection. J Immunol 200(4):1489–1495

    Article  CAS  PubMed  Google Scholar 

  • Kurt-Jones EA, Orzalli MH, Knipe DM (2017) Innate immune mechanisms and herpes simplex virus infection and disease. Adv Anat Embryol Cell Biol 223:49–75

    Article  PubMed  PubMed Central  Google Scholar 

  • Lalaoui N, Boyden SE, Oda H, Wood GM, Stone DL, Chau D, Liu L, Stoffels M, Kratina T, Lawlor KE, Zaal KJM, Hoffmann PM, Etemadi N, Shield-Artin K, Biben C, Tsai WL, Blake MD, Kuehn HS, Yang D, Anderton H, Silke N, Wachsmuth L, Zheng L, Moura NS, Beck DB, Gutierrez-Cruz G, Ombrello AK, Pinto-Patarroyo GP, Kueh AJ, Herold MJ, Hall C, Wang H, Chae JJ, Dmitrieva NI, McKenzie M, Light A, Barham BK, Jones A, Romeo TM, Zhou Q, Aksentijevich I, Mullikin JC, Gross AJ, Shum AK, Hawkins ED, Masters SL, Lenardo MJ, Boehm M, Rosenzweig SD, Pasparakis M, Voss AK, Gadina M, Kastner DL, Silke J (2020) Mutations that prevent caspase cleavage of RIPK1 cause autoinflammatory disease. Nature 577(7788):103–108

    Article  CAS  PubMed  Google Scholar 

  • Lamkanfi M, Dixit VM (2010) Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8(1):44–54

    Article  CAS  PubMed  Google Scholar 

  • Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157(5):1013–1022

    Article  CAS  PubMed  Google Scholar 

  • Langelier Y, Bergeron S, Chabaud S, Lippens J, Guilbault C, Sasseville AM, Denis S, Mosser DD, Massie B (2002) The R1 subunit of herpes simplex virus ribonucleotide reductase protects cells against apoptosis at, or upstream of, caspase-8 activation. J Gen Virol 83(Pt 11):2779–2789

    Article  CAS  PubMed  Google Scholar 

  • Langelier Y, Champoux L, Hamel M, Guilbault C, Lamarche N, Gaudreau P, Massie B (1998) The R1 subunit of herpes simplex virus ribonucleotide reductase is a good substrate for host cell protein kinases but is not itself a protein kinase. J Biol Chem 273(3):1435–1443

    Article  CAS  PubMed  Google Scholar 

  • Lawlor KE, Khan N, Mildenhall A, Gerlic M, Croker BA, D’Cruz AA, Hall C, Kaur Spall S, Anderton H, Masters SL, Rashidi M, Wicks IP, Alexander WS, Mitsuuchi Y, Benetatos CA, Condon SM, Wong WW, Silke J, Vaux DL, Vince JE (2015) RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat Commun 6:6282

    Article  CAS  PubMed  Google Scholar 

  • Le T, Reeves RK, McKinnon LR (2022) The functional diversity of tissue-resident natural killer cells against infection. Immunology 167:28–39

    Google Scholar 

  • Lee S, Karki R, Wang Y, Nguyen LN, Kalathur RC, Kanneganti TD (2021) AIM2 forms a complex with pyrin and ZBP1 to drive PANoptosis and host defence. Nature 597:415–419

    Google Scholar 

  • Lei X, Chen Y, Lien E, Fitzgerald KA (2023) MLKL-driven inflammasome activation and caspase-8 mediate inflammatory cell death in influenza A virus infection. mBio 14(2):e0011023

    Google Scholar 

  • Lettre G, Hengartner MO (2006) Developmental apoptosis in C. elegans: a complex CEDnario. Nat Rev Mol Cell Biol 7(2):97–108

    Google Scholar 

  • Li P, Allen H, Banerjee S, Franklin S, Herzog L, Johnston C, McDowell J, Paskind M, Rodman L, Salfeld J et al (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80(3):401–411

    Article  CAS  PubMed  Google Scholar 

  • Li S, Cao L, Zhang Z, Kuang M, Chen L, Zhao Y, Luo Y, Yin Z, You F (2021) Cytosolic and nuclear recognition of virus and viral evasion. Mol Biomed 2(1):30

    Article  PubMed  PubMed Central  Google Scholar 

  • Li W, Yuan J (2023) Targeting RIPK1 kinase for modulating inflammation in human diseases. Front Immunol 14:1159743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Garcia Reino EJ, Harschnitz O, Guo H, Chan YH, Khobrekar NV, Hasek ML, Dobbs K, Rinchai D, Materna M, Matuozzo D, Lee D, Bastard P, Chen J, Lee YS, Kim SK, Zhao S, Amin P, Lorenzo L, Seeleuthner Y, Chevalier R, Mazzola L, Gay C, Stephan JL, Milisavljevic B, Boucherit S, Rozenberg F, Perez de Diego R, Dix RD, Marr N, Béziat V, Cobat A, Aubart M, Abel L, Chabrier S, Smith GA, Notarangelo LD, Mocarski ES, Studer L, Casanova JL, Zhang SY (2023) Encephalitis and poor neuronal death-mediated control of herpes simplex virus in human inherited RIPK3 deficiency. Sci Immunol 8(82):eade2860

    Google Scholar 

  • Liu Z, Nailwal H, Rector J, Rahman MM, Sam R, McFadden G, Chan FK (2021) A class of viral inducer of degradation of the necroptosis adaptor RIPK3 regulates virus-induced inflammation. Immunity 54(2):247-258.e247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu JV, Walsh CM (2012) Programmed necrosis and autophagy in immune function. Immunol Rev 249(1):205–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu JV, Weist BM, van Raam BJ, Marro BS, Nguyen LV, Srinivas P, Bell BD, Luhrs KA, Lane TE, Salvesen GS, Walsh CM (2011) Complementary roles of Fas-associated death domain (FADD) and receptor interacting protein kinase-3 (RIPK3) in T-cell homeostasis and antiviral immunity. Proc Natl Acad Sci U S A 108(37):15312–15317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macen JL, Graham KA, Lee SF, Schreiber M, Boshkov LK, McFadden G (1996) Expression of the myxoma virus tumor necrosis factor receptor homologue and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology 218(1):232–237

    Article  CAS  PubMed  Google Scholar 

  • Madiraju C, Novack JP, Reed JC, Matsuzawa SI (2022) K63 ubiquitination in immune signaling. Trends Immunol 43(2):148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maelfait J, Liverpool L, Bridgeman A, Ragan KB, Upton JW, Rehwinkel J (2017) Sensing of viral and endogenous RNA by ZBP1/DAI induces necroptosis. EMBO J 36(17):2529–2543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maelfait J, Liverpool L, Rehwinkel J (2020) Nucleic acid sensors and programmed cell death. J Mol Biol 432(2):552–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mancini M, Vidal SM (2020) Mechanisms of natural killer cell evasion through viral adaptation. Annu Rev Immunol 38:511–539

    Article  CAS  PubMed  Google Scholar 

  • Mandal P, Berger SB, Pillay S, Moriwaki K, Huang C, Guo H, Lich JD, Finger J, Kasparcova V, Votta B, Ouellette M, King BW, Wisnoski D, Lakdawala AS, DeMartino MP, Casillas LN, Haile PA, Sehon CA, Marquis RW, Upton J, Daley-Bauer LP, Roback L, Ramia N, Dovey CM, Carette JE, Chan FK, Bertin J, Gough PJ, Mocarski ES, Kaiser WJ (2014) RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol Cell 56(4):481–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandal P, Feng Y, Lyons JD, Berger SB, Otani S, DeLaney A, Tharp GK, Maner-Smith K, Burd EM, Schaeffer M, Hoffman S, Capriotti C, Roback L, Young CB, Liang Z, Ortlund EA, DiPaolo NC, Bosinger S, Bertin J, Gough PJ, Brodsky IE, Coopersmith CM, Shayakhmetov DM, Mocarski ES (2018) Caspase-8 collaborates with caspase-11 to drive tissue damage and execution of endotoxic shock. Immunity 49(1):42-55.e46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandal P, McCormick AL, Mocarski ES (2020) TNF signaling dictates myeloid and non-myeloid cell crosstalk to execute MCMV-induced extrinsic apoptosis. Viruses 12(11):1221

    Google Scholar 

  • Mandal P, Nagrani LN, Hernandez L, McCormick AL, Dillon CP, Koehler HS, Roback L, Alnemri ES, Green DR, Mocarski ES (2021) Multiple autonomous cell death suppression strategies ensure cytomegalovirus fitness. Viruses 13:1707

    Google Scholar 

  • McCormick AL, Mocarski ES (2013) Cell death pathways controlled by cytomegaloviruses. In: Reddehase MJ (ed) Cytomegaloviruses: from molecular pathogenesis to intervention, vol I. Caister Scientific Press, Norfolk, United Kingdom, pp 263–276

    Google Scholar 

  • McCormick AL, Mocarski Jr ES (2007) Viral modulation of the host response to infection. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. 2011/02/25 edn. Cambridge Press, Cambridge, pp 324–337. NBK47417 [bookaccession]

    Google Scholar 

  • McCormick AL, Roback L, Livingston-Rosanoff D, St Clair C (2010) The human cytomegalovirus UL36 gene controls caspase-dependent and -independent cell death programs activated by infection of monocytes differentiating to macrophages. J Virol 84(10):5108–5123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormick AL, Roback L, Mocarski ES (2008) HtrA2/Omi terminates cytomegalovirus infection and is controlled by the viral mitochondrial inhibitor of apoptosis (vMIA). PLoS Pathog 4(5):e1000063

    Article  PubMed  PubMed Central  Google Scholar 

  • McCormick AL, Roback L, Wynn G, Mocarski ES (2013) Multiplicity-dependent activation of a serine protease-dependent cytomegalovirus-associated programmed cell death pathway. Virology 435(2):250–257

    Article  CAS  PubMed  Google Scholar 

  • McCormick AL, Skaletskaya A, Barry PA, Mocarski ES, Goldmacher VS (2003) Differential function and expression of the viral inhibitor of caspase 8-induced apoptosis (vICA) and the viral mitochondria-localized inhibitor of apoptosis (vMIA) cell death suppressors conserved in primate and rodent cytomegaloviruses. Virology 316(2):221–233

    Article  CAS  PubMed  Google Scholar 

  • Means RE, Lang SM, Jung JU (2007) Human gammaherpesvirus immune evasion strategies

    Google Scholar 

  • Menard C, Wagner M, Ruzsics Z, Holak K, Brune W, Campbell AE, Koszinowski UH (2003) Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J Virol 77(10):5557–5570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyts I, Casanova JL (2021) Viral infections in humans and mice with genetic deficiencies of the type I IFN response pathway. Eur J Immunol 51(5):1039–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A, Warren SE, Wewers MD, Aderem A (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11(12):1136–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller LK (1999) An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol 9(8):323–328

    Article  CAS  PubMed  Google Scholar 

  • Mocarski ES, Guo H, Kaiser WJ (2015) Necroptosis: The Trojan horse in cell autonomous antiviral host defense. Virology 479–480:160–166

    Article  PubMed  Google Scholar 

  • Mocarski ES Jr (2002) Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends Microbiol 10(7):332–339

    Article  CAS  PubMed  Google Scholar 

  • Mocarski ES, Kaiser WJ, Livingston-Rosanoff D, Upton JW, Daley-Bauer LP (2014) True grit: programmed necrosis in antiviral host defense, inflammation, and immunogenicity. J Immunol 192(5):2019–2026

    Article  CAS  PubMed  Google Scholar 

  • Mocarski ES, Upton JW, Kaiser WJ (2011) Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat Rev Immunol 12(2):79–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriwaki K, Balaji S, Bertin J, Gough PJ, Chan FK (2017) Distinct kinase-independent role of RIPK3 in CD11c(+) mononuclear phagocytes in cytokine-induced tissue repair. Cell Rep 18(10):2441–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moriwaki K, Chan FK (2017) The inflammatory signal adaptor RIPK3: functions beyond necroptosis. Int Rev Cell Mol Biol 328:253–275

    Article  CAS  PubMed  Google Scholar 

  • Motwani M, Pesiridis S, Fitzgerald KA (2019) DNA sensing by the cGAS-STING pathway in health and disease. Nat Rev Genet 20(11):657–674

    Article  CAS  PubMed  Google Scholar 

  • Mujal AM, Delconte RB, Sun JC (2021) Natural killer cells: from innate to adaptive features. Annu Rev Immunol 39:417–447

    Article  CAS  PubMed  Google Scholar 

  • Müller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M (1994) Functional role of type I and type II interferons in antiviral defense. Science 264(5167):1918–1921

    Article  PubMed  Google Scholar 

  • Muscolino E, Castiglioni C, Brixel R, Frascaroli G, Brune W (2021) Species-specific inhibition of necroptosis by HCMV UL36. Viruses 13:2134

    Google Scholar 

  • Nagata S (2018) Apoptosis and clearance of apoptotic cells. Annu Rev Immunol 36:489–517

    Article  CAS  PubMed  Google Scholar 

  • Nailwal H, Chan FK (2019) Necroptosis in anti-viral inflammation. Cell Death Differ 26(1):4–13

    Article  CAS  PubMed  Google Scholar 

  • Newton K (2015) RIPK1 and RIPK3: critical regulators of inflammation and cell death. Trends Cell Biol 25(6):347–353

    Article  CAS  PubMed  Google Scholar 

  • Newton K, Dugger DL, Wickliffe KE, Kapoor N, Cristina de-Almagro M, Vucic D, Komuves L, Ferrando RE, French DM, Webster J, Roose-Girma M, Warming S, Dixit VM (2014) Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343:1357–1360

    Google Scholar 

  • Newton K, Wickliffe KE, Dugger DL, Maltzman A, Roose-Girma M, Dohse M, Komuves L, Webster JD, Dixit VM (2019a) Cleavage of RIPK1 by caspase-8 is crucial for limiting apoptosis and necroptosis. Nature 574(7778):428–431

    Article  CAS  PubMed  Google Scholar 

  • Newton K, Wickliffe KE, Maltzman A, Dugger DL, Reja R, Zhang Y, Roose-Girma M, Modrusan Z, Sagolla MS, Webster JD, Dixit VM (2019b) Activity of caspase-8 determines plasticity between cell death pathways. Nature 575(7784):679–682

    Article  CAS  PubMed  Google Scholar 

  • Newton K, Wickliffe KE, Maltzman A, Dugger DL, Strasser A, Pham VC, Lill JR, Roose-Girma M, Warming S, Solon M, Ngu H, Webster JD, Dixit VM (2016) RIPK1 inhibits ZBP1-driven necroptosis during development. Nature 540(7631):129–133

    Article  CAS  PubMed  Google Scholar 

  • Nishikura K (2016) A-to-I editing of coding and non-coding RNAs by ADARs. Nat Rev Mol Cell Biol 17(2):83–96

    Article  CAS  PubMed  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-driven 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 

  • Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, Hakem R, Salvesen GS, Green DR (2011) Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471(7338):363–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omoto S, Guo H, Talekar GR, Roback L, Kaiser WJ, Mocarski ES (2015) Suppression of RIP3-dependent necroptosis by human cytomegalovirus. J Biol Chem 290(18):11635–11648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orning P, Lien E (2021) Multiple roles of caspase-8 in cell death, inflammation, and innate immunity. J Leukoc Biol 109(1):121–141

    Article  CAS  PubMed  Google Scholar 

  • Patton T, Zhao Z, Lim XY, Eddy E, Wang H, Nelson AG, Ennis B, Eckle SBG, Souter MNT, Pediongco TJ, Koay HF, Zhang JG, Djajawi TM, Louis C, Lalaoui N, Jacquelot N, Lew AM, Pellicci DG, McCluskey J, Zhan Y, Chen Z, Lawlor KE, Corbett AJ (2023) RIPK3 controls MAIT cell accumulation during development but not during infection. Cell Death Dis 14(2):111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson JS, Giogha C, Muhlen S, Nachbur U, Pham CL, Zhang Y, Hildebrand JM, Oates CV, Lung TW, Ingle D, Dagley LF, Bankovacki A, Petrie EJ, Schroeder GN, Crepin VF, Frankel G, Masters SL, Vince J, Murphy JM, Sunde M, Webb AI, Silke J, Hartland EL (2017) EspL is a bacterial cysteine protease effector that cleaves RHIM proteins to block necroptosis and inflammation. Nat Microbiol 2:16258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrie EJ, Sandow JJ, Lehmann WIL, Liang LY, Coursier D, Young SN, Kersten WJA, Fitzgibbon C, Samson AL, Jacobsen AV, Lowes KN, Au AE, Jousset Sabroux H, Lalaoui N, Webb AI, Lessene G, Manning G, Lucet IS, Murphy JM (2019) Viral MLKL homologs subvert necroptotic cell death by sequestering cellular RIPK3. Cell Rep 28(13):3309-3319.e3305

    Article  CAS  PubMed  Google Scholar 

  • Pham TH, Kwon KM, Kim YE, Kim KK, Ahn JH (2013) DNA sensing-independent inhibition of herpes simplex virus 1 replication by DAI/ZBP1. J Virol 87(6):3076–3086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piersma SJ, Brizić I (2021) Natural killer cell effector functions in antiviral defense. FEBS J

    Google Scholar 

  • Ranger AM, Malynn BA, Korsmeyer SJ (2001) Mouse models of cell death. Nat Genet 28(2):113–118

    Article  CAS  PubMed  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 

  • Rebsamen M, Heinz LX, Meylan E, Michallet MC, Schroder K, Hofmann K, Vazquez J, Benedict CA, Tschopp J (2009) DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-κB. EMBO Rep 10(8):916–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddien PW, Horvitz HR (2004) The engulfment process of programmed cell death in caenorhabditis elegans. Annu Rev Cell Dev Biol 20:193–221

    Article  CAS  PubMed  Google Scholar 

  • Rickard JA, O’Donnell JA, Evans JM, Lalaoui N, Poh AR, Rogers T, Vince JE, Lawlor KE, Ninnis RL, Anderton H, Hall C, Spall SK, Phesse TJ, Abud HE, Cengia LH, Corbin J, Mifsud S, Di Rago L, Metcalf D, Ernst M, Dewson G, Roberts AW, Alexander WS, Murphy JM, Ekert PG, Masters SL, Vaux DL, Croker BA, Gerlic M, Silke J (2014) RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell 157(5):1175–1188

    Article  CAS  PubMed  Google Scholar 

  • Roizman B, Taddeo B (2007) The strategy of herpes simplex virus replication and takeover of the host cell. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge

    Google Scholar 

  • Roy CR, Mocarski ES (2007) Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol 8(11):1179–1187

    Article  CAS  PubMed  Google Scholar 

  • Rucker AJ, Chan FK (2022) Tumor-intrinsic and immune modulatory roles of receptor-interacting protein kinases. Trends Biochem Sci 47(4):342–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamaki K, Inoue T, Asano M, Sudo K, Kazama H, Sakagami J, Sakata S, Ozaki M, Nakamura S, Toyokuni S, Osumi N, Iwakura Y, Yonehara S (2002) Ex vivo whole-embryo culture of caspase-8-deficient embryos normalize their aberrant phenotypes in the develo** neural tube and heart. Cell Death Differ 9(11):1196–1206

    Article  CAS  PubMed  Google Scholar 

  • Salvesen GS, Riedl SJ (2008) Caspase mechanisms. Adv Exp Med Biol 615:13–23

    Article  CAS  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 U S A 115(46):E10888-e10897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauer JD, Witte CE, Zemansky J, Hanson B, Lauer P, Portnoy DA (2010) Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7(5):412–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, Cameron C, Sypula J, Nazarian SH, Lucas A, McFadden G (2003) Poxviruses and immune evasion. Annu Rev Immunol 21:377–423

    Article  CAS  PubMed  Google Scholar 

  • Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22(4):526–539

    Article  CAS  PubMed  Google Scholar 

  • Shisler JL, Gooding LR (1998) Adenoviral inhibitors of the apoptotic cascade. Trends Microbiol 6(9):337–339

    Article  CAS  PubMed  Google Scholar 

  • Shubina M, Tummers B, Boyd DF, Zhang T, Yin C, Gautam A, Guo XJ, Rodriguez DA, Kaiser WJ, Vogel P, Green DR, Thomas PG, Balachandran S (2020) Necroptosis restricts influenza A virus as a stand-alone cell death mechanism. J Exp Med 217(11):e20191259

    Google Scholar 

  • Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, Goldmacher VS (2001) A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci U S A 98(14):7829–7834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith GL (1996) Virus proteins that bind cytokines, chemokines or interferons. Curr Opin Immunol 8(4):467–471

    Article  CAS  PubMed  Google Scholar 

  • Song B, Shiromoto Y, Minakuchi M, Nishikura K (2022) The role of RNA editing enzyme ADAR1 in human disease. Wiley Interdiscip Rev RNA 13(1):e1665

    Article  CAS  PubMed  Google Scholar 

  • Sridharan H, Ragan KB, Guo H, Gilley RP, Landsteiner VJ, Kaiser WJ, Upton JW (2017) Murine cytomegalovirus IE3-dependent transcription is required for DAI/ZBP1-mediated necroptosis. EMBO Rep 18(8):1429–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steain M, Baker M, Pham CLL, Shanmugam N, Gambin Y, Sierecki E, McSharry BP, Avdic S, Slobedman B, Sunde M, Abendroth A (2020) Varicella zoster virus encodes a viral decoy RHIM to inhibit cell death. PLoS Pathog 16(7):e1008473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strasser A, Vaux DL (2018) Viewing BCL2 and cell death control from an evolutionary perspective. Cell Death Differ 25(1):13–20

    Article  CAS  PubMed  Google Scholar 

  • Su H, Bidere N, Zheng L, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M (2005) Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 307(5714):1465–1468

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, Wang X (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148(1–2):213–227

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Wang X (2014) A new kind of cell suicide: mechanisms and functions of programmed necrosis. Trends Biochem Sci 39(12):587–593

    Article  CAS  PubMed  Google Scholar 

  • Suraweera CD, Hinds MG, Kvansakul M (2020) Poxviral strategies to overcome host cell apoptosis. Pathogens (Basel, Switzerland) 10(1):6

    Google Scholar 

  • Szczerba M, Subramanian S, Trainor K, McCaughan M, Kibler KV, Jacobs BL (2022) Small hero with great powers: vaccinia virus E3 protein and evasion of the type I IFN response. Biomedicines 10(2):235

    Google Scholar 

  • Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K, Ohba Y, Taniguchi T (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448(7152):501–505

    Article  CAS  PubMed  Google Scholar 

  • Tang D, Wang H, Billiar TR, Kroemer G, Kang R (2021a) Emerging mechanisms of immunocoagulation in sepsis and septic shock. Trends Immunol 42(6):508–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Q, Rigby RE, Young GR, Hvidt AK, Davis T, Tan TK, Bridgeman A, Townsend AR, Kassiotis G, Rehwinkel J (2021b) Adenosine-to-inosine editing of endogenous Z-form RNA by the deaminase ADAR1 prevents spontaneous MAVS-dependent type I interferon responses. Immunity 54(9):1961-1975.e1965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, Zachariou A, Lopez J, Macfarlane M, Cain K, Meier P (2011) The ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell 43:432–448

    Article  CAS  PubMed  Google Scholar 

  • Terra JK, Cote CK, France B, Jenkins AL, Bozue JA, Welkos SL, LeVine SM, Bradley KA (2010) Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J Immunol 184(1):17–20

    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 

  • Thapa RJ, Nogusa S, Balachandran S (2018) Analysis of cytokine- and influenza A virus-driven RIPK3 necrosome formation. Methods Mol Biol 1857:93–99

    Google Scholar 

  • Tummers B, Green DR (2022a) The evolution of regulated cell death pathways in animals and their evasion by pathogens. Physiol Rev 102(1):411–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tummers B, Green DR (2022b) Mechanisms of TNF-independent RIPK3-mediated cell death. Biochem J 479(19):2049–2062

    Article  CAS  PubMed  Google Scholar 

  • Udawatte DJ, Rothman AL (2021) Viral suppression of RIPK1-mediated signaling. mBio 12(4):e0172321

    Google Scholar 

  • Upton JW, Chan FK (2014) Staying alive: cell death in antiviral immunity. Mol Cell 54(2):273–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upton JW, Kaiser WJ, Mocarski ES (2008) Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J Biol Chem 283(25):16966–16970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upton JW, Kaiser WJ, Mocarski ES (2010) Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7(4):302–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upton JW, Kaiser WJ, Mocarski ES (2012) DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11(3):290–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upton JW, Shubina M, Balachandran S (2017) RIPK3-driven cell death during virus infections. Immunol Rev 277(1):90–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van den Berg SPH, Pardieck IN, Lanfermeijer J, Sauce D, Klenerman P, van Baarle D, Arens R (2019) The hallmarks of CMV-specific CD8 T-cell differentiation. Med Microbiol Immunol

    Google Scholar 

  • van den Broek MF, Muller U, Huang S, Zinkernagel RM, Aguet M (1995) Immune defence in mice lacking type I and/or type II interferon receptors. Immunol Rev 148:5–18

    Article  PubMed  Google Scholar 

  • Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, Lapidot T, Soffer D, Sobe T, Avraham KB, Goncharov T, Holtmann H, Lonai P, Wallach D (1998) Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9(2):267–276

    Article  CAS  PubMed  Google Scholar 

  • Vaux DL, Korsmeyer SJ (1999) Cell death in development. Cell 96(2):245–254

    Article  CAS  PubMed  Google Scholar 

  • Verburg SG, Lelievre RM, Westerveld MJ, Inkol JM, Sun YL, Workenhe ST (2022) Viral-mediated activation and inhibition of programmed cell death. PLoS Pathog 18(8):e1010718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P (1998) Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187(9):1477–1485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verdonck S, Nemegeer J, Vandenabeele P, Maelfait J (2021) Viral manipulation of host cell necroptosis and pyroptosis. Trends Microbiol 30:593–605

    Google Scholar 

  • Veyer DL, Carrara G, Maluquer de Motes C, Smith GL (2017) Vaccinia virus evasion of regulated cell death. Immunol Lett 186:68–80

    Article  CAS  PubMed  Google Scholar 

  • Vince JE, Wong WW, Gentle I, Lawlor KE, Allam R, O’Reilly L, Mason K, Gross O, Ma S, Guarda G, Anderton H, Castillo R, Hacker G, Silke J, Tschopp J (2012) Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36(2):215–227

    Article  CAS  PubMed  Google Scholar 

  • Vitale I, Pietrocola F, Guilbaud E, Aaronson SA, Abrams JM, Adam D, Agostini M, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, Aqeilan RI, Arama E, Baehrecke EH, Balachandran S, Bano D, Barlev NA, Bartek J, Bazan NG, Becker C, Bernassola F, Bertrand MJM, Bianchi ME, Blagosklonny MV, Blander JM, Blandino G, Blomgren K, Borner C, Bortner CD, Bove P, Boya P, Brenner C, Broz P, Brunner T, Damgaard RB, Calin GA, Campanella M, Candi E, Carbone M, Carmona-Gutierrez D, Cecconi F, Chan FK, Chen GQ, Chen Q, Chen YH, Cheng EH, Chipuk JE, Cidlowski JA, Ciechanover A, Ciliberto G, Conrad M, Cubillos-Ruiz JR, Czabotar PE, D'Angiolella V, Daugaard M, Dawson TM, Dawson VL, De Maria R, De Strooper B, Debatin KM, Deberardinis RJ, Degterev A, Del Sal G, Deshmukh M, Di Virgilio F, Diederich M, Dixon SJ, Dynlacht BD, El-Deiry WS, Elrod JW, Engeland K, Fimia GM, Galassi C, Ganini C, Garcia-Saez AJ, Garg AD, Garrido C, Gavathiotis E, Gerlic M, Ghosh S, Green DR, Greene LA, Gronemeyer H, Häcker G, Hajnóczky G, Hardwick JM, Haupt Y, He S, Heery DM, Hengartner MO, Hetz C, Hildeman DA, Ichijo H, Inoue S, Jäättelä M, Janic A, Joseph B, Jost PJ, Kanneganti TD, Karin M, Kashkar H, Kaufmann T, Kelly GL, Kepp O, Kimchi A, Kitsis RN, Klionsky DJ, Kluck R, Krysko DV, Kulms D, Kumar S, Lavandero S, Lavrik IN, Lemasters JJ, Liccardi G, Linkermann A, Lipton SA, Lockshin RA, López-Otín C, Luedde T, MacFarlane M, Madeo F, Malorni W, Manic G, Mantovani R, Marchi S, Marine JC, Martin SJ, Martinou JC, Mastroberardino PG, Medema JP, Mehlen P, Meier P, Melino G, Melino S, Miao EA, Moll UM, Muñoz-Pinedo C, Murphy DJ, Niklison-Chirou MV, Novelli F, Núñez G, Oberst A, Ofengeim D, Opferman JT, Oren M, Pagano M, Panaretakis T, Pasparakis M, Penninger JM, Pentimalli F, Pereira DM, Pervaiz S, Peter ME, Pinton P, Porta G, Prehn JHM, Puthalakath H, Rabinovich GA, Rajalingam K, Ravichandran KS, Rehm M, Ricci JE, Rizzuto R, Robinson N, Rodrigues CMP, Rotblat B, Rothlin CV, Rubinsztein DC, Rudel T, Rufini A, Ryan KM, Sarosiek KA, Sawa A, Sayan E, Schroder K, Scorrano L, Sesti F, Shao F, Shi Y, Sica GS, Silke J, Simon HU, Sistigu A, Stephanou A, Stockwell BR, Strapazzon F, Strasser A, Sun L, Sun E, Sun Q, Szabadkai G, Tait SWG, Tang D, Tavernarakis N, Troy CM, Turk B, Urbano N, Vandenabeele P, Vanden Berghe T, Vander Heiden MG, Vanderluit JL, Verkhratsky A, Villunger A, von Karstedt S, Voss AK, Vousden KH, Vucic D, Vuri D, Wagner EF, Walczak H, Wallach D, Wang R, Wang Y, Weber A, Wood W, Yamazaki T, Yang HT, Zakeri Z, Zawacka-Pankau JE, Zhang L, Zhang H, Zhivotovsky B, Zhou W, Piacentini M, Kroemer G, Galluzzi L (2023) Apoptotic cell death in disease-current understanding of the NCCD 2023. Cell Death Differ 30(5):1097–1154

    Google Scholar 

  • Vlantis K, Wullaert A, Polykratis A, Kondylis V, Dannappel M, Schwarzer R, Welz P, Corona T, Walczak H, Weih F, Klein U, Kelliher M, Pasparakis M (2016) NEMO prevents RIP kinase 1-mediated epithelial cell death and chronic intestinal inflammation by NF-κB-dependent and -independent functions. Immunity 44(3):553–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallach D, Kang TB, Dillon CP, Green DR (2016) Programmed necrosis in inflammation: toward identification of the effector molecules. Science 352(6281):aaf2154

    Google Scholar 

  • Wang G, Zhang D, Orchard RC, Hancks DC, Reese TA (2023) Norovirus MLKL-like protein initiates cell death to induce viral egress. Nature 616(7955):152–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Du F, Wang X (2008) TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133(4):693–703

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Li Y, Liu S, Yu X, Li L, Shi C, He W, Li J, Xu L, Hu Z, Yu L, Yang Z, Chen Q, Ge L, Zhang Z, Zhou B, Jiang X, Chen S, He S (2014) Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc Natl Acad Sci U S A 111:15438–15443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward-Kavanagh LK, Lin WW, Sedy JR, Ware CF (2016) The TNF receptor superfamily in co-stimulating and co-inhibitory responses. Immunity 44(5):1005–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welz PS, Wullaert A, Vlantis K, Kondylis V, Fernandez-Majada V, Ermolaeva M, Kirsch P, Sterner-Kock A, van Loo G, Pasparakis M (2011) FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 477(7364):330–334

    Article  CAS  PubMed  Google Scholar 

  • Wold WS, Hermiston TW, Tollefson AE (1994) Adenovirus proteins that subvert host defenses. Trends Microbiol 2(11):437–443

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Huang Z, Ren J, Zhang Z, He P, Li Y, Ma J, Chen W, Zhang Y, Zhou X, Yang Z, Wu SQ, Chen L, Han J (2013) Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res 23:994–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Wu X, Zhang X, **e Q, Fan C, Zhang H (2018) Embryonic lethality and host immunity of RelA-deficient mice are mediated by both apoptosis and necroptosis. J Immunol 200(1):271–285

    Article  CAS  PubMed  Google Scholar 

  • Yatim N, Albert ML (2011) Dying to replicate: the orchestration of the viral life cycle, cell death pathways, and immunity. Immunity 35(4):478–490

    Article  CAS  PubMed  Google Scholar 

  • Yeh WC, Itie A, Elia AJ, Ng M, Shu HB, Wakeham A, Mirtsos C, Suzuki N, Bonnard M, Goeddel DV, Mak TW (2000) Requirement for casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12(6):633–642

    Article  CAS  PubMed  Google Scholar 

  • Yoon S, Kovalenko A, Bogdanov K, Wallach D (2017) MLKL, the protein that mediates necroptosis, also regulates endosomal trafficking and extracellular vesicle generation. Immunity 47(1):51-65.e57

    Article  CAS  PubMed  Google Scholar 

  • Zangger N, Oxenius A (2022) T cell immunity to cytomegalovirus infection. Curr Opin Immunol 77:102185

    Article  CAS  PubMed  Google Scholar 

  • Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325:332–336

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhou X, McQuade T, Li J, Chan FK, Zhang J (2011a) Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471(7338):373–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Cado D, Chen A, Kabra NH, Winoto A (1998) Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 392(6673):296–300

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang H, Li J, Rosenberg S, Zhang EC, Zhou X, Qin F, Farabaugh M (2011b) RIP1-mediated regulation of lymphocyte survival and death responses. Immunol Res 51(2–3):227–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Yin C, Boyd DF, Quarato G, Ingram JP, Shubina M, Ragan KB, Ishizuka T, Crawford JC, Tummers B, Rodriguez DA, Xue J, Peri S, Kaiser WJ, Lopez CB, Xu Y, Upton JW, Thomas PG, Green DR, Balachandran S (2020) Influenza virus Z-RNAs induce ZBP1-mediated necroptosis. Cell 180(6):1115-1129.e1113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng M, Kanneganti TD (2020) The regulation of the ZBP1-NLRP3 inflammasome and its implications in pyroptosis, apoptosis, and necroptosis (PANoptosis). Immunol Rev 297(1):26–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Mocarski, E.S. (2023). Programmed Necrosis in Host Defense. 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_2023_264

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