1932

Abstract

Cell death is a common outcome of virus infection. In some cases, cell death curbs virus replication. In others, cell death enhances virus dissemination and contributes to tissue injury, exacerbating viral disease. Three forms of cell death are observed following virus infection—apoptosis, necroptosis, and pyroptosis. In this review, I describe the core machinery needed for each of these forms of cell death. Using representative viruses, I highlight how distinct stages of virus replication initiate signaling pathways that elicit these forms of cell death. I also discuss viral strategies to overcome the deleterious effects of cell death on virus propagation and the consequences of cell death for host physiology.

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2016-09-29
2024-03-28
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Literature Cited

  1. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH. 1.  et al. 2012. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19:107–20 [Google Scholar]
  2. Lennemann NJ, Coyne CB. 2.  2015. Catch me if you can: the link between autophagy and viruses. PLOS Pathog. 11:e1004685 [Google Scholar]
  3. Salvesen GS, Riedl SJ. 3.  2008. Caspase mechanisms. Adv. Exp. Med. Biol. 615:13–23 [Google Scholar]
  4. Oberst A, Pop C, Tremblay AG, Blais V, Denault JB. 4.  et al. 2010. Inducible dimerization and inducible cleavage reveal a requirement for both processes in caspase-8 activation. J. Biol. Chem. 285:16632–42 [Google Scholar]
  5. Wilson NS, Dixit V, Ashkenazi A. 5.  2009. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat. Immunol. 10:348–55 [Google Scholar]
  6. Tait SW, Green DR. 6.  2010. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11:621–32 [Google Scholar]
  7. Czabotar PE, Lessene G, Strasser A, Adams JM. 7.  2014. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15:49–63 [Google Scholar]
  8. Riedl SJ, Salvesen GS. 8.  2007. The apoptosome: signalling platform of cell death. Nat. Rev. Mol. Cell Biol. 8:405–13 [Google Scholar]
  9. Eckelman BP, Salvesen GS, Scott FL. 9.  2006. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 7:988–94 [Google Scholar]
  10. Brojatsch J, Naughton J, Rolls MM, Zingler K, Young JA. 10.  1996. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845–55 [Google Scholar]
  11. Hanon E, Meyer G, Vanderplasschen A, Dessy-Doize C, Thiry E, Pastoret PP. 11.  1998. Attachment but not penetration of bovine herpesvirus 1 is necessary to induce apoptosis in target cells. J. Virol. 72:7638–41 [Google Scholar]
  12. Gosselin AS, Simonin Y, Guivel-Benhassine F, Rincheval V, Vayssiere JL. 12.  et al. 2003. Poliovirus-induced apoptosis is reduced in cells expressing a mutant CD155 selected during persistent poliovirus infection in neuroblastoma cells. J. Virol. 77:790–98 [Google Scholar]
  13. Autret A, Martin-Latil S, Mousson L, Wirotius A, Petit F. 13.  et al. 2007. Poliovirus induces Bax-dependent cell death mediated by c-Jun NH2-terminal kinase. J. Virol. 81:7504–16 [Google Scholar]
  14. Jan JT, Chatterjee S, Griffin DE. 14.  2000. Sindbis virus entry into cells triggers apoptosis by activating sphingomyelinase, leading to the release of ceramide. J. Virol. 74:6425–32 [Google Scholar]
  15. Pettus BJ, Chalfant CE, Hannun YA. 15.  2002. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585:114–25 [Google Scholar]
  16. Connolly JL, Dermody TS. 16.  2002. Virion disassembly is required for apoptosis induced by reovirus. J. Virol. 76:1632–41 [Google Scholar]
  17. Danthi P, Kobayashi T, Holm GH, Hansberger MW, Abel TW, Dermody TS. 17.  2008. Reovirus apoptosis and virulence are regulated by host cell membrane penetration efficiency. J. Virol. 82:161–72 [Google Scholar]
  18. Danthi P, Coffey CM, Parker JS, Abel TW, Dermody TS. 18.  2008. Independent regulation of reovirus membrane penetration and apoptosis by the μ1 ϕ domain. PLOS Pathog. 4:e1000248 [Google Scholar]
  19. Hansberger MW, Campbell JA, Danthi P, Arrate P, Pennington KN. 19.  et al. 2007. IκB kinase subunits α and γ are required for activation of NF-κB and induction of apoptosis by mammalian reovirus. J. Virol. 81:1360–71 [Google Scholar]
  20. Connolly JL, Rodgers SE, Clarke P, Ballard DW, Kerr LD. 20.  et al. 2000. Reovirus-induced apoptosis requires activation of transcription factor NF-κB. J. Virol. 74:2981–89 [Google Scholar]
  21. Clarke P, Debiasi RL, Meintzer SM, Robinson BA, Tyler KL. 21.  2005. Inhibition of NF-κB activity and cFLIP expression contribute to viral-induced apoptosis. Apoptosis 10:513–24 [Google Scholar]
  22. Danthi P, Pruijssers AJ, Berger AK, Holm GH, Zinkel SS, Dermody TS. 22.  2010. Bid regulates the pathogenesis of neurotropic reovirus. PLOS Pathog. 6:e1000980 [Google Scholar]
  23. Clarke P, Meintzer SM, Gibson S, Widmann C, Garrington TP. 23.  et al. 2000. Reovirus-induced apoptosis is mediated by TRAIL. J. Virol. 74:8135–39 [Google Scholar]
  24. Kominsky DJ, Bickel RJ, Tyler KL. 24.  2002. Reovirus-induced apoptosis requires both death receptor- and mitochondrial-mediated caspase-dependent pathways of cell death. Cell Death Differ. 9:926–33 [Google Scholar]
  25. Alonso C, Miskin J, Hernaez B, Fernandez-Zapatero P, Soto L. 25.  et al. 2001. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J. Virol. 75:9819–27 [Google Scholar]
  26. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A. 26.  1999. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3:287–96 [Google Scholar]
  27. Goubau D, Deddouche S, Reis e Sousa C. 27.  2013. Cytosolic sensing of viruses. Immunity 38:855–69 [Google Scholar]
  28. Estornes Y, Toscano F, Virard F, Jacquemin G, Pierrot A. 28.  et al. 2012. dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ. 19:1482–94 [Google Scholar]
  29. Lei Y, Moore CB, Liesman RM, O'Connor BP, Bergstralh DT. 29.  et al. 2009. MAVS-mediated apoptosis and its inhibition by viral proteins. PLOS ONE 4:e5466 [Google Scholar]
  30. El Maadidi S, Faletti L, Berg B, Wenzl C, Wieland K. 30.  et al. 2014. A novel mitochondrial MAVS/Caspase-8 platform links RNA virus-induced innate antiviral signaling to Bax/Bak-independent apoptosis. J. Immunol. 192:1171–83 [Google Scholar]
  31. Yu CY, Chiang RL, Chang TH, Liao CL, Lin YL. 31.  2010. The interferon stimulator mitochondrial antiviral signaling protein facilitates cell death by disrupting the mitochondrial membrane potential and by activating caspases. J. Virol. 84:2421–31 [Google Scholar]
  32. Guan K, Zheng Z, Song T, He X, Xu C. 32.  et al. 2013. MAVS regulates apoptotic cell death by decreasing K48-linked ubiquitination of voltage-dependent anion channel 1. Mol. Cell. Biol. 33:3137–49 [Google Scholar]
  33. Chattopadhyay S, Marques JT, Yamashita M, Peters KL, Smith K. 33.  et al. 2010. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J. 29:1762–73 [Google Scholar]
  34. Sze A, Belgnaoui SM, Olagnier D, Lin R, Hiscott J, van Grevenynghe J. 34.  2013. Host restriction factor SAMHD1 limits human T cell leukemia virus type 1 infection of monocytes via STING-mediated apoptosis. Cell Host Microbe 14:422–34 [Google Scholar]
  35. Holm GH, Zurney J, Tumilasci V, Leveille S, Danthi P. 35.  et al. 2007. Retinoic acid-inducible gene-I and interferon-β promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J. Biol. Chem. 282:21953–61 [Google Scholar]
  36. Knowlton JJ, Dermody TS, Holm GH. 36.  2012. Apoptosis induced by mammalian reovirus is beta interferon (IFN) independent and enhanced by IFN regulatory factor 3- and NF-κB-dependent expression of Noxa. J. Virol. 86:1650–60 [Google Scholar]
  37. Kirshner JR, Karpova AY, Kops M, Howley PM. 37.  2005. Identification of TRAIL as an interferon regulatory factor 3 transcriptional target. J. Virol. 79:9320–24 [Google Scholar]
  38. Peters K, Chattopadhyay S, Sen GC. 38.  2008. IRF-3 activation by Sendai virus infection is required for cellular apoptosis and avoidance of persistence. J. Virol. 82:3500–8 [Google Scholar]
  39. Ivashkiv LB, Donlin LT. 39.  2014. Regulation of type I interferon responses. Nat. Rev. Immunol. 14:36–49 [Google Scholar]
  40. Barber GN. 40.  2005. The dsRNA-dependent protein kinase, PKR and cell death. Cell Death Differ. 12:563–70 [Google Scholar]
  41. Kibler KV, Shors T, Perkins KB, Zeman CC, Banaszak MP. 41.  et al. 1997. Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells. J. Virol. 71:1992–2003 [Google Scholar]
  42. Balachandran S, Kim CN, Yeh WC, Mak TW, Bhalla K, Barber GN. 42.  1998. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 17:6888–902 [Google Scholar]
  43. Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK. 43.  et al. 2000. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13:129–41 [Google Scholar]
  44. Donze O, Dostie J, Sonenberg N. 44.  1999. Regulatable expression of the interferon-induced double-stranded RNA dependent protein kinase PKR induces apoptosis and Fas receptor expression. Virology 256:322–29 [Google Scholar]
  45. Gil J, Esteban M. 45.  2000. The interferon-induced protein kinase (PKR), triggers apoptosis through FADD-mediated activation of caspase 8 in a manner independent of Fas and TNF-α receptors. Oncogene 19:3665–74 [Google Scholar]
  46. Gil J, Alcami J, Esteban M. 46.  1999. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the α subunit of eukaryotic translation initiation factor 2 and NF-κB. Mol. Cell. Biol. 19:4653–63 [Google Scholar]
  47. Castelli JC, Hassel BA, Wood KA, Li XL, Amemiya K. 47.  et al. 1997. A study of the interferon antiviral mechanism: apoptosis activation by the 2-5A system. J. Exp. Med. 186:967–72 [Google Scholar]
  48. Maitra RK, Silverman RH. 48.  1998. Regulation of human immunodeficiency virus replication by 2′,5′-oligoadenylate-dependent RNase L. J. Virol. 72:1146–52 [Google Scholar]
  49. Silverman RH. 49.  2007. Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81:12720–29 [Google Scholar]
  50. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC. 50.  et al. 2003. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237–49 [Google Scholar]
  51. Takizawa T, Fukuda R, Miyawaki T, Ohashi K, Nakanishi Y. 51.  1995. Activation of the apoptotic Fas antigen-encoding gene upon influenza virus infection involving spontaneously produced beta-interferon. Virology 209:288–96 [Google Scholar]
  52. Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H. 52.  et al. 2003. Integration of interferon-α/ββ signalling to p53 responses in tumour suppression and antiviral defence. Nature 424:516–23 [Google Scholar]
  53. Haupt S, Berger M, Goldberg Z, Haupt Y. 53.  2003. Apoptosis—the p53 network. J. Cell Sci. 116:4077–85 [Google Scholar]
  54. Toyoda H, Nicklin MJ, Murray MG, Anderson CW, Dunn JJ. 54.  et al. 1986. A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein. Cell 45:761–70 [Google Scholar]
  55. Hanecak R, Semler BL, Anderson CW, Wimmer E. 55.  1982. Proteolytic processing of poliovirus polypeptides: antibodies to polypeptide P3-7c inhibit cleavage at glutamine-glycine pairs. PNAS 79:3973–77 [Google Scholar]
  56. Krausslich HG, Nicklin MJ, Toyoda H, Etchison D, Wimmer E. 56.  1987. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220. J. Virol. 61:2711–18 [Google Scholar]
  57. Goldstaub D, Gradi A, Bercovitch Z, Grosmann Z, Nophar Y. 57.  et al. 2000. Poliovirus 2A protease induces apoptotic cell death. Mol. Cell. Biol. 20:1271–77 [Google Scholar]
  58. Barco A, Feduchi E, Carrasco L. 58.  2000. Poliovirus protease 3Cpro kills cells by apoptosis. Virology 266:352–60 [Google Scholar]
  59. Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE. 59.  2000. The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol. Cell. Biol. 20:8590–601 [Google Scholar]
  60. Rajani KR, Pettit Kneller EL, McKenzie MO, Horita DA, Chou JW, Lyles DS. 60.  2012. Complexes of vesicular stomatitis virus matrix protein with host Rae1 and Nup98 involved in inhibition of host transcription. PLOS Pathog. 8:e1002929 [Google Scholar]
  61. Kopecky SA, Willingham MC, Lyles DS. 61.  2001. Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J. Virol. 75:12169–81 [Google Scholar]
  62. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR. 62.  1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053–61 [Google Scholar]
  63. Grossman SR, Perez M, Kung AL, Joseph M, Mansur C. 63.  et al. 1998. p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol. Cell 2:405–15 [Google Scholar]
  64. Lowe SW, Ruley HE. 64.  1993. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev. 7:535–45 [Google Scholar]
  65. Debbas M, White E. 65.  1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546–54 [Google Scholar]
  66. Cuconati A, Mukherjee C, Perez D, White E. 66.  2003. DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev. 17:2922–32 [Google Scholar]
  67. Mitchell JK, Friesen PD. 67.  2012. Baculoviruses modulate a proapoptotic DNA damage response to promote virus multiplication. J. Virol. 86:13542–53 [Google Scholar]
  68. Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P. 68.  2005. Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLOS Pathog. 1:e4 [Google Scholar]
  69. McAuley JL, Chipuk JE, Boyd KL, Van De Velde N, Green DR, McCullers JA. 69.  2010. PB1-F2 proteins from H5N1 and 20th century pandemic influenza viruses cause immunopathology. PLOS Pathog. 6:e1001014 [Google Scholar]
  70. Jacotot E, Ferri KF, El Hamel C, Brenner C, Druillennec S. 70.  et al. 2001. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J. Exp. Med. 193:509–19 [Google Scholar]
  71. Coffey CM, Sheh A, Kim IS, Chandran K, Nibert ML, Parker JS. 71.  2006. Reovirus outer capsid protein μ1 induces apoptosis and associates with lipid droplets, endoplasmic reticulum, and mitochondria. J. Virol. 80:8422–38 [Google Scholar]
  72. Wisniewski ML, Werner BG, Hom LG, Anguish LJ, Coffey CM, Parker JS. 72.  2011. Reovirus infection or ectopic expression of outer capsid protein μ1 induces apoptosis independently of the cellular proapoptotic proteins Bax and Bak. J. Virol. 85:296–304 [Google Scholar]
  73. Kim JW, Lyi SM, Parrish CR, Parker JS. 73.  2011. A proapoptotic peptide derived from reovirus outer capsid protein μ1 has membrane-destabilizing activity. J. Virol. 85:1507–16 [Google Scholar]
  74. Prikhod'ko GG, Prikhod'ko EA, Pletnev AG, Cohen JI. 74.  2002. Langat flavivirus protease NS3 binds caspase-8 and induces apoptosis. J. Virol. 76:5701–10 [Google Scholar]
  75. Prikhod'ko EA, Prikhod'ko GG, Siegel RM, Thompson P, Major ME, Cohen JI. 75.  2004. The NS3 protein of hepatitis C virus induces caspase-8-mediated apoptosis independent of its protease or helicase activities. Virology 329:53–67 [Google Scholar]
  76. Kamita SG, Majima K, Maeda S. 76.  1993. Identification and characterization of the p35 gene of Bombyx mori nuclear polyhedrosis virus that prevents virus-induced apoptosis. J. Virol. 67:455–63 [Google Scholar]
  77. Gagliardini V, Fernandez PA, Lee RK, Drexler HC, Rotello RJ. 77.  et al. 1994. Prevention of vertebrate neuronal death by the crmA gene. Science 263:826–28 [Google Scholar]
  78. Saraiva M, Alcami A. 78.  2001. CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. J. Virol. 75:226–33 [Google Scholar]
  79. Skaletskaya A, Bartle LM, Chittenden T, McCormick AL, Mocarski ES, Goldmacher VS. 79.  2001. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. PNAS 98:7829–34 [Google Scholar]
  80. Bertin J, Armstrong RC, Ottilie S, Martin DA, Wang Y. 80.  et al. 1997. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. PNAS 94:1172–76 [Google Scholar]
  81. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E. 81.  et al. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517–21 [Google Scholar]
  82. Cheng EH, Nicholas J, Bellows DS, Hayward GS, Guo HG. 82.  et al. 1997. A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. PNAS 94:690–94 [Google Scholar]
  83. Dawson CW, Eliopoulos AG, Dawson J, Young LS. 83.  1995. BHRF1, a viral homologue of the Bcl-2 oncogene, disturbs epithelial cell differentiation. Oncogene 10:69–77 [Google Scholar]
  84. Wasilenko ST, Stewart TL, Meyers AF, Barry M. 84.  2003. Vaccinia virus encodes a previously uncharacterized mitochondrial-associated inhibitor of apoptosis. PNAS 100:14345–50 [Google Scholar]
  85. Arnoult D, Bartle LM, Skaletskaya A, Poncet D, Zamzami N. 85.  et al. 2004. Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. PNAS 101:7988–93 [Google Scholar]
  86. Han J, Sabbatini P, Perez D, Rao L, Modha D, White E. 86.  1996. The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10:461–77 [Google Scholar]
  87. Clem RJ, Miller LK. 87.  1994. Control of programmed cell death by the baculovirus genes p35 and iap. Mol. Cell. Biol. 14:5212–22 [Google Scholar]
  88. Seshagiri S, Vucic D, Lee J, Dixit VM. 88.  1999. Baculovirus-based genetic screen for antiapoptotic genes identifies a novel IAP. J. Biol. Chem. 274:36769–73 [Google Scholar]
  89. Silke J, Meier P. 89.  2013. Inhibitor of apoptosis (IAP) proteins—modulators of cell death and inflammation. Cold Spring Harb. Perspect. Biol. 5:a008730 [Google Scholar]
  90. Byers NM, Vandergaast RL, Friesen PD. 90.  2015. Baculovirus inhibitor-of-apoptosis Op-IAP3 blocks apoptosis by interaction with and stabilization of a host insect cellular IAP. J. Virol. 90:533–44 [Google Scholar]
  91. Hay S, Kannourakis G. 91.  2002. A time to kill: viral manipulation of the cell death program. J. Gen. Virol. 83:1547–64 [Google Scholar]
  92. Cuconati A, White E. 92.  2002. Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev. 16:2465–78 [Google Scholar]
  93. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G. 93.  2008. Viral control of mitochondrial apoptosis. PLOS Pathog. 4:e1000018 [Google Scholar]
  94. Mocarski ES, Upton JW, Kaiser WJ. 94.  2012. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12:79–88 [Google Scholar]
  95. Upton JW, Chan FK. 95.  2014. Staying alive: cell death in antiviral immunity. Mol. Cell 54:273–80 [Google Scholar]
  96. Devireddy LR, Jones CJ. 96.  1999. Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J. Virol. 73:3778–88 [Google Scholar]
  97. Wurzer WJ, Planz O, Ehrhardt C, Giner M, Silberzahn T. 97.  et al. 2003. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J. 22:2717–28 [Google Scholar]
  98. Jackson AC, Rossiter JP. 98.  1997. Apoptosis plays an important role in experimental rabies virus infection. J. Virol. 71:5603–7 [Google Scholar]
  99. Despres P, Frenkiel MP, Ceccaldi PE, Duarte Dos Santos C, Deubel V. 99.  1998. Apoptosis in the mouse central nervous system in response to infection with mouse-neurovirulent dengue viruses. J. Virol. 72:823–29 [Google Scholar]
  100. DeBiasi RL, Robinson BA, Sherry B, Bouchard R, Brown RD. 100.  et al. 2004. Caspase inhibition protects against reovirus-induced myocardial injury in vitro and in vivo. J. Virol. 78:11040–50 [Google Scholar]
  101. DeBiasi RL, Kleinschmidt-DeMasters BK, Richardson-Burns S, Tyler KL. 101.  2002. Central nervous system apoptosis in human herpes simplex virus and cytomegalovirus encephalitis. J. Infect. Dis. 186:1547–57 [Google Scholar]
  102. Clarke P, Tyler KL. 102.  2009. Apoptosis in animal models of virus-induced disease. Nat. Rev. Microbiol. 7:144–55 [Google Scholar]
  103. Rajput A, Kovalenko A, Bogdanov K, Yang SH, Kang TB. 103.  et al. 2011. RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein. Immunity 34:340–51 [Google Scholar]
  104. Silke J, Rickard JA, Gerlic M. 104.  2015. The diverse role of RIP kinases in necroptosis and inflammation. Nat. Immunol. 16:689–97 [Google Scholar]
  105. Galluzzi L, Kepp O, Kroemer G. 105.  2014. MLKL regulates necrotic plasma membrane permeabilization. Cell Res. 24:139–40 [Google Scholar]
  106. Pasparakis M, Vandenabeele P. 106.  2015. Necroptosis and its role in inflammation. Nature 517:311–20 [Google Scholar]
  107. Cho YS, Challa S, Moquin D, Genga R, Ray TD. 107.  et al. 2009. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112–23 [Google Scholar]
  108. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A. 108.  et al. 2008. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30:689–700 [Google Scholar]
  109. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C. 109.  et al. 2011. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43:449–63 [Google Scholar]
  110. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. 110.  2012. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat. Immunol. 13:954–62 [Google Scholar]
  111. Thapa RJ, Nogusa S, Chen P, Maki JL, Lerro A. 111.  et al. 2013. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. PNAS 110:E3109–18 [Google Scholar]
  112. McComb S, Cessford E, Alturki NA, Joseph J, Shutinoski B. 112.  et al. 2014. Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. PNAS 111:E3206–13 [Google Scholar]
  113. He S, Liang Y, Shao F, Wang X. 113.  2011. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. PNAS 108:20054–59 [Google Scholar]
  114. Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW. 114.  et al. 2013. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288:31268–79 [Google Scholar]
  115. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP. 115.  et al. 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471:368–72 [Google Scholar]
  116. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P. 116.  et al. 2011. Catalytic activity of the caspase-8–FLIPL complex inhibits RIPK3-dependent necrosis. Nature 471:363–67 [Google Scholar]
  117. Upton JW, Kaiser WJ, Mocarski ES. 117.  2012. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11:290–97 [Google Scholar]
  118. Huang Z, Wu SQ, Liang Y, Zhou X, Chen W. 118.  et al. 2015. RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host Microbe 17:229–42 [Google Scholar]
  119. Wang X, Li Y, Liu S, Yu X, Li L. 119.  et al. 2014. Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. PNAS 111:15438–43 [Google Scholar]
  120. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L. 120.  et al. 2003. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 278:51613–21 [Google Scholar]
  121. Dobbelstein M, Shenk T. 121.  1996. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J. Virol. 70:6479–85 [Google Scholar]
  122. Berger AK, Danthi P. 122.  2013. Reovirus activates a caspase-independent cell death pathway. mBio 4:e00178–13 [Google Scholar]
  123. Son KN, Lipton HL. 123.  2015. Inhibition of Theiler's virus-induced apoptosis in infected murine macrophages results in necroptosis. Virus Res. 195:177–82 [Google Scholar]
  124. Chu JJ, Ng ML. 124.  2003. The mechanism of cell death during West Nile virus infection is dependent on initial infectious dose. J. Gen. Virol. 84:3305–14 [Google Scholar]
  125. Bozym RA, Patel K, White C, Cheung KH, Bergelson JM. 125.  et al. 2011. Calcium signals and calpain-dependent necrosis are essential for release of coxsackievirus B from polarized intestinal epithelial cells. Mol. Biol. Cell 22:3010–21 [Google Scholar]
  126. Hiller BE, Berger AK, Danthi P. 126.  2015. Viral gene expression potentiates reovirus-induced necrosis. Virology 484:386–94 [Google Scholar]
  127. Upton JW, Kaiser WJ, Mocarski ES. 127.  2010. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7:302–13 [Google Scholar]
  128. Omoto S, Guo H, Talekar GR, Roback L, Kaiser WJ, Mocarski ES. 128.  2015. Suppression of RIP3-dependent necroptosis by human cytomegalovirus. J. Biol. Chem. 290:11635–48 [Google Scholar]
  129. Guo H, Omoto S, Harris PA, Finger JN, Bertin J. 129.  et al. 2015. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe 17:243–51 [Google Scholar]
  130. Harris KG, Morosky SA, Drummond CG, Patel M, Kim C. 130.  et al. 2015. RIP3 regulates autophagy and promotes coxsackievirus B3 infection of intestinal epithelial cells. Cell Host Microbe 18:221–32 [Google Scholar]
  131. Rodrigue-Gervais IG, Labbe K, Dagenais M, Dupaul-Chicoine J, Champagne C. 131.  et al. 2014. Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15:23–35 [Google Scholar]
  132. Martinon F, Tschopp J. 132.  2007. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 14:10–22 [Google Scholar]
  133. Guo H, Callaway JB, Ting JP. 133.  2015. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat. Med. 21:677–87 [Google Scholar]
  134. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE. 134.  et al. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11:395–402 [Google Scholar]
  135. Chen G, Shaw MH, Kim YG, Nunez G. 135.  2009. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 4:365–98 [Google Scholar]
  136. Poeck H, Bscheider M, Gross O, Finger K, Roth S. 136.  et al. 2010. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production. Nat. Immunol. 11:63–69 [Google Scholar]
  137. Hagar JA, Aachoui Y, Miao EA. 137.  2015. WildCARDs: Inflammatory caspases directly detect LPS. Cell Res. 25:149–50 [Google Scholar]
  138. He WT, Wan H, Hu L, Chen P, Wang X. 138.  et al. 2015. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 25:1285–98 [Google Scholar]
  139. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K. 139.  et al. 2015. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526:666–71 [Google Scholar]
  140. Monroe KM, Yang Z, Johnson JR, Geng X, Doitsh G. 140.  et al. 2014. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343:428–32 [Google Scholar]
  141. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM. 141.  et al. 2014. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505:509–14 [Google Scholar]
  142. Galloway NL, Doitsh G, Monroe KM, Yang Z, Munoz-Arias I. 142.  et al. 2015. Cell-to-cell transmission of HIV-1 is required to trigger pyroptotic death of lymphoid-tissue-derived CD4 T cells. Cell Rep. 12:1555–63 [Google Scholar]
  143. Tan TY, Chu JJ. 143.  2013. Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J. Gen. Virol. 94:2215–20 [Google Scholar]
  144. Amsler L, Malouli D, DeFilippis V. 144.  2013. The inflammasome as a target of modulation by DNA viruses. Future Virol. 8:357–70 [Google Scholar]
  145. Ashida H, Mimuro H, Ogawa M, Kobayashi T, Sanada T. 145.  et al. 2011. Cell death and infection: a double-edged sword for host and pathogen survival. J. Cell Biol. 195:931–42 [Google Scholar]
  146. Golstein P, Kroemer G. 146.  2005. Redundant cell death mechanisms as relics and backups. Cell Death Differ. 12:Suppl. 21490–96 [Google Scholar]
  147. Han J, Zhong CQ, Zhang DW. 147.  2011. Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat. Immunol. 12:1143–49 [Google Scholar]
  148. Taylor JM, Barry M. 148.  2006. Near death experiences: poxvirus regulation of apoptotic death. Virology 344:139–50 [Google Scholar]
  149. Draper SJ, Heeney JL. 149.  2010. Viruses as vaccine vectors for infectious diseases and cancer. Nat. Rev. Microbiol. 8:62–73 [Google Scholar]
  150. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. 150.  2000. Consequences of cell death: Exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191:423–34 [Google Scholar]
  151. Albert ML. 151.  2004. Death-defying immunity: Do apoptotic cells influence antigen processing and presentation?. Nat. Rev. Immunol. 4:223–31 [Google Scholar]
  152. Albert ML, Sauter B, Bhardwaj N. 152.  1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392:86–89 [Google Scholar]
  153. Yatim N, Jusforgues-Saklani H, Orozco S, Schulz O, Barreira da Silva R. 153.  et al. 2015. RIPK1 and NF-κB signaling in dying cells determines cross-priming of CD8+ T cells. Science 350:328–34 [Google Scholar]
  154. Chiocca EA. 154.  2002. Oncolytic viruses. Nat. Rev. Cancer 2:938–50 [Google Scholar]
  155. Igney FH, Krammer PH. 155.  2002. Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2:277–88 [Google Scholar]
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