Staying alive: Cell death in antiviral immunity

Molecular Cell

Volumn 54, Issue 2, 2014, Pages 273-280

  Upton, Jason W ^a   Chan, Francis Ka Ming ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSOME; BIM PROTEIN; CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 8; CASPASE 9; EFFECTOR CASPASE; FAS LIGAND; FLICE INHIBITORY PROTEIN; INTERFERON REGULATORY FACTOR; INTERLEUKIN 18; INTERLEUKIN 1BETA; MIXED LINEAGE KINASE; PERFORIN; PROTEIN BAD; PROTEIN BID; REACTIVE OXYGEN METABOLITE; X LINKED INHIBITOR OF APOPTOSIS;

ANTIVIRAL ACTIVITY; APOPTOSIS; AUTOIMMUNITY; AUTOPHAGY; CELL DEATH; CHROMATIN CONDENSATION; CONFORMATIONAL TRANSITION; CYTOTOXIC T LYMPHOCYTE; DNA FRAGMENTATION; EFFECTOR CELL; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGICAL MEMORY; LIGAND BINDING; LYMPHOCYTE; MEMORY T LYMPHOCYTE; MITOCHONDRION; NATURAL KILLER CELL; NECROSIS; NONHUMAN; PATHOGENESIS; PROTEIN PROTEIN INTERACTION; REVIEW; T LYMPHOCYTE ACTIVATION; VACCINIA VIRUS;

ANIMALS; CELL DEATH; HOST-PATHOGEN INTERACTIONS; LYMPHOCYTES; MAMMALS; MODELS, IMMUNOLOGICAL; VIRUS DISEASES;

EID: 84899132580     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.01.027     Document Type: Review

References (87)

1. Antonopoulos C., El Sanadi C., Kaiser W.J., Mocarski E.S., Dubyak G.R. Proapoptotic chemotherapeutic drugs induce noncanonical processing and release of IL-1β via caspase-8 in dendritic cells. J.Immunol. 2013, 191:4789-4803.
2. Bahl K., Kim S.K., Calcagno C., Ghersi D., Puzone R., Celada F., Selin L.K., Welsh R.M. IFN-induced attrition of CD8 Tcells in the presence or absence of cognate antigen during the early stages of viral infections. J.Immunol. 2006, 176:4284-4295.
3. Balkow S., Kersten A., Tran T.T., Stehle T., Grosse P., Museteanu C., Utermöhlen O., Pircher H., von Weizsäcker F., Wallich R., et al. Concerted action of the FasL/Fas and perforin/granzyme A and B pathways is mandatory for the development of early viral hepatitis but not for recovery from viral infection. J.Virol. 2001, 75:8781-8791.
4. Bouillet P., Metcalf D., Huang D.C., Tarlinton D.M., Kay T.W., Köntgen F., Adams J.M., Strasser A. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999, 286:1735-1738.
5. Brune W. Inhibition of programmed cell death by cytomegaloviruses. Virus Res. 2011, 157:144-150.
6. Cain K., Bratton S.B., Langlais C., Walker G., Brown D.G., Sun X.M., Cohen G.M. Apaf-1 oligomerizes into biologically active approximately 700-kDa and inactive approximately 1.4-MDa apoptosome complexes. J.Biol. Chem. 2000, 275:6067-6070.
7. Challa S., Woelfel M., Guildford M., Moquin D., Chan F.K. Viral cell death inhibitor MC159 enhances innate immunity against vaccinia virus infection. J.Virol. 2010, 84:10467-10476.
8. Chan F.K., Chun H.J., Zheng L., Siegel R.M., Bui K.L., Lenardo M.J. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science 2000, 288:2351-2354.
9. Chan F.K., Shisler J., Bixby J.G., Felices M., Zheng L., Appel M., Orenstein J., Moss B., Lenardo M.J. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J.Biol. Chem. 2003, 278:51613-51621.
10. Chen W., Zhou Z., Li L., Zhong C.Q., Zheng X., Wu X., Zhang Y., Ma H., Huang D., Li W., et al. Diverse sequence determinants control human and mouse receptor interacting protein 3 (RIP3) and mixed lineage kinase domain-like (MLKL) interaction in necroptotic signaling. J.Biol. Chem. 2013, 288:16247-16261.
11. Cho Y.S., Challa S., Moquin D., Genga R., Ray T.D., Guildford M., Chan F.K. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009, 137:1112-1123.
12. Degterev A., Maki J.L., Yuan J. Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ. 2013, 20:366.
13. Deretic V., Saitoh T., Akira S. Autophagy in infection, inflammation and immunity. Nat. Rev. Immunol. 2013, 13:722-737.
14. Dix R.D., Ekworomadu C.O., Hernandez E., Cousins S.W. Perforin knockout mice, but not mice with MAIDS, show protection against experimental cytomegalovirus retinitis after adoptive transfer of immune cells with a functional perforin cytotoxic pathway. Arch. Virol. 2004, 149:2235-2244.
15. Dixit E., Kagan J.C. Intracellular pathogen detection by RIG-I-like receptors. Adv. Immunol. 2013, 117:99-125.
16. Dobbelstein M., Shenk T. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J.Virol. 1996, 70:6479-6485.
17. Ewen C.L., Kane K.P., Bleackley R.C. A quarter century of granzymes. Cell Death Differ. 2012, 19:28-35.
18. Feoktistova M., Geserick P., Kellert B., Dimitrova D.P., Langlais C., Hupe M., Cain K., MacFarlane M., Häcker G., Leverkus M. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 2011, 43:449-463.
19. Fliss P.M., Jowers T.P., Brinkmann M.M., Holstermann B., Mack C., Dickinson P., Hohenberg H., Ghazal P., Brune W. Viral mediated redirection of NEMO/IKKγ to autophagosomes curtails the inflammatory cascade. PLoS Pathog. 2012, 8:e1002517.
20. Galluzzi L., Brenner C., Morselli E., Touat Z., Kroemer G. Viral control of mitochondrial apoptosis. PLoS Pathog. 2008, 4:e1000018.
21. Goldmacher V.S. Cell death suppression by cytomegaloviruses. Apoptosis 2005, 10:251-265.
22. He S., Liang Y., Shao F., Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc. Natl. Acad. Sci. USA 2011, 108:20054-20059.
23. Heibein J.A., Barry M., Motyka B., Bleackley R.C. Granzyme B-induced loss of mitochondrial inner membrane potential (Delta Psi m) and cytochrome c release are caspase independent. J.Immunol. 1999, 163:4683-4693.
24. Holler N., Zaru R., Micheau O., Thome M., Attinger A., Valitutti S., Bodmer J.L., Schneider P., Seed B., Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 2000, 1:489-495.
25. Kägi D., Vignaux F., Ledermann B., Bürki K., Depraetere V., Nagata S., Hengartner H., Golstein P. Fas and perforin pathways as major mechanisms of Tcell-mediated cytotoxicity. Science 1994, 265:528-530.
26. Kägi D., Seiler P., Pavlovic J., Ledermann B., Bürki K., Zinkernagel R.M., Hengartner H. The roles of perforin- and Fas-dependent cytotoxicity in protection against cytopathic and noncytopathic viruses. Eur. J. Immunol. 1995, 25:3256-3262.
27. Kaiser W.J., Upton J.W., Mocarski E.S. Receptor-interacting protein homotypic interaction motif-dependent control of NF-kappa B activation via the DNA-dependent activator of IFN regulatory factors. J.Immunol. 2008, 181:6427-6434.
28. Kaiser W.J., Upton J.W., Long A.B., Livingston-Rosanoff D., Daley-Bauer L.P., Hakem R., Caspary T., Mocarski E.S. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011, 471:368-372.
29. Kaiser W.J., Sridharan H., Huang C., Mandal P., Upton J.W., Gough P.J., Sehon C.A., Marquis R.W., Bertin J., Mocarski E.S. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J.Biol. Chem. 2013, 288:31268-31279.
30. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
31. Kettle S., Alcamí A., Khanna A., Ehret R., Jassoy C., Smith G.L. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1beta-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1beta-induced fever. J.Gen. Virol. 1997, 78:677-685.
32. Laster S.M., Wood J.G., Gooding L.R. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J.Immunol. 1988, 141:2629-2634.
33. Legrand F.A., Verardi P.H., Jones L.A., Chan K.S., Peng Y., Yilma T.D. Induction of potent humoral and cell-mediated immune responses by attenuated vaccinia virus vectors with deleted serpin genes. J.Virol. 2004, 78:2770-2779.
34. Li M., Beg A.A. Induction of necrotic-like cell death by tumor necrosis factor alpha and caspase inhibitors: novel mechanism for killing virus-infected cells. J.Virol. 2000, 74:7470-7477.
35. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998, 94:491-501.
36. Loh J., Thomas D.A., Revell P.A., Ley T.J., Virgin H.W. Granzymes and caspase 3 play important roles in control of gammaherpesvirus latency. J.Virol. 2004, 78:12519-12528.
37. Lowin B., Hahne M., Mattmann C., Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994, 370:650-652.
38. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998, 94:481-490.
39. MacDonald G., Shi L., Vande Velde C., Lieberman J., Greenberg A.H. Mitochondria-dependent and -independent regulation of Granzyme B-induced apoptosis. J.Exp. Med. 1999, 189:131-144.
40. Mack C., Sickmann A., Lembo D., Brune W. Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc. Natl. Acad. Sci. USA 2008, 105:3094-3099.
41. Martinvalet D., Dykxhoorn D.M., Ferrini R., Lieberman J. Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 2008, 133:681-692.
42. McCormick A.L., Skaletskaya A., Barry P.A., Mocarski E.S., Goldmacher V.S. 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 2003, 316:221-233.
43. McQuade T., Cho Y., Chan F.K. Positive and negative phosphorylation regulates RIP1- and RIP3-induced programmed necrosis. Biochem. J. 2013, 456:409-415.
44. Ménard C., Wagner M., Ruzsics Z., Holak K., Brune W., Campbell A.E., Koszinowski U.H. Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J.Virol. 2003, 77:5557-5570.
45. Meylan E., Burns K., Hofmann K., Blancheteau V., Martinon F., Kelliher M., Tschopp J. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol. 2004, 5:503-507.
46. Micheau O., Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114:181-190.
47. Miura M., Zhu H., Rotello R., Hartwieg E.A., Yuan J. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 1993, 75:653-660.
48. Mocarski E.S., Upton J.W., Kaiser W.J. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 2012, 12:79-88.
49. Moquin D.M., McQuade T., Chan F.K. CYLD deubiquitinates RIP1 in the TNFα-induced necrosome to facilitate kinase activation and programmed necrosis. PLoS ONE 2013, 8:e76841.
50. Moriwaki K., Chan F.K. RIP3: a molecular switch for necrosis and inflammation. Genes Dev. 2013, 27:1640-1649.
51. Müllbacher A., Ebnet K., Blanden R.V., Hla R.T., Stehle T., Museteanu C., Simon M.M. Granzyme A is critical for recovery of mice from infection with the natural cytopathic viral pathogen, ectromelia. Proc. Natl. Acad. Sci. USA 1996, 93:5783-5787.
52. Müllbacher A., Waring P., Tha Hla R., Tran T., Chin S., Stehle T., Museteanu C., Simon M.M. Granzymes are the essential downstream effector molecules for the control of primary virus infections by cytolytic leukocytes. Proc. Natl. Acad. Sci. USA 1999, 96:13950-13955.
53. Murphy J.M., Czabotar P.E., Hildebrand J.M., Lucet I.S., Zhang J.G., Alvarez-Diaz S., Lewis R., Lalaoui N., Metcalf D., Webb A.I., et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 2013, 39:443-453.
54. O'Donnell M.A., Perez-Jimenez E., Oberst A., Ng A., Massoumi R., Xavier R., Green D.R., Ting A.T. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat. Cell Biol. 2011, 13:1437-1442.
55. Oberst A., Dillon C.P., Weinlich R., McCormick L.L., Fitzgerald P., Pop C., Hakem R., Salvesen G.S., Green D.R. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471:363-367.
56. Odake S., Kam C.M., Narasimhan L., Poe M., Blake J.T., Krahenbuhl O., Tschopp J., Powers J.C. Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins. Biochemistry 1991, 30:2217-2227.
57. Olson M.R., Varga S.M. Fas ligand is required for the development of respiratory syncytial virus vaccine-enhanced disease. J.Immunol. 2009, 182:3024-3031.
58. Pao L.I., Sumaria N., Kelly J.M., van Dommelen S., Cretney E., Wallace M.E., Anthony D.A., Uldrich A.P., Godfrey D.I., Papadimitriou J.M., et al. Functional analysis of granzyme M and its role in immunity to infection. J.Immunol. 2005, 175:3235-3243.
59. Quan L.T., Caputo A., Bleackley R.C., Pickup D.J., Salvesen G.S. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J.Biol. Chem. 1995, 270:10377-10379.
60. Rajani D.K., Walch M., Martinvalet D., Thomas M.P., Lieberman J. Alterations in RNA processing during immune-mediated programmed cell death. Proc. Natl. Acad. Sci. USA 2012, 109:8688-8693.
61. Rathinam V.A., Vanaja S.K., Fitzgerald K.A. Regulation of inflammasome signaling. Nat. Immunol. 2012, 13:333-342.
62. Ray C.A., Black R.A., Kronheim S.R., Greenstreet T.A., Sleath P.R., Salvesen G.S., Pickup D.J. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 1992, 69:597-604.
63. Seedhom M.O., Mathurin K.S., Kim S.K., Welsh R.M. Increased protection from vaccinia virus infection in mice genetically prone to lymphoproliferative disorders. J.Virol. 2012, 86:6010-6022.
64. Singh A., Suresh M. A role for TNF in limiting the duration of CTL effector phase and magnitude of CD8 Tcell memory. J.Leukoc. Biol. 2007, 82:1201-1211.
65. Sinha S., Colbert C.L., Becker N., Wei Y., Levine B. Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 2008, 4:989-997.
66. Skaletskaya A., Bartle L.M., Chittenden T., McCormick A.L., Mocarski E.S., Goldmacher V.S. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. USA 2001, 98:7829-7834.
67. Su H.C., Lenardo M.J. Genetic defects of apoptosis and primary immunodeficiency. Immunol. Allergy Clin. North Am. 2008, 28:329-351. ix.
68. Sun X., Yin J., Starovasnik M.A., Fairbrother W.J., Dixit V.M. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J.Biol. Chem. 2002, 277:9505-9511.
69. Sun L., Wang H., Wang Z., He S., Chen S., Liao D., Wang L., Yan J., Liu W., Lei X., Wang X. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148:213-227.
70. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 2010, 11:621-632.
71. Tenev T., Bianchi K., Darding M., Broemer M., Langlais C., Wallberg F., Zachariou A., Lopez J., MacFarlane M., Cain K., Meier P. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 2011, 43:432-448.
72. Terrell C.E., Jordan M.B. Perforin deficiency impairs a critical immunoregulatory loop involving murine CD8(+) Tcells and dendritic cells. Blood 2013, 121:5184-5191.
73. Tripathi P., Koss B., Opferman J.T., Hildeman D.A. Mcl-1 antagonizes Bax/Bak to promote effector CD4(+) and CD8(+) T-cell responses. Cell Death Differ. 2013, 20:998-1007.
74. Upton J.W., Kaiser W.J., Mocarski E.S. Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J.Biol. Chem. 2008, 283:16966-16970.
75. Upton J.W., Kaiser W.J., Mocarski E.S. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 2010, 7:302-313.
76. Upton J.W., Kaiser W.J., Mocarski E.S. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 2012, 11:290-297.
77. van Dommelen S.L., Sumaria N., Schreiber R.D., Scalzo A.A., Smyth M.J., Degli-Esposti M.A. Perforin and granzymes have distinct roles in defensive immunity and immunopathology. Immunity 2006, 25:835-848.
78. Vince J.E., Wong W.W., Gentle I., Lawlor K.E., Allam R., O'Reilly L., Mason K., Gross O., Ma S., Guarda G., et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 2012, 36:215-227.
79. Wang Z., Jiang H., Chen S., Du F., Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012, 148:228-243.
80. Weant A.E., Michalek R.D., Khan I.U., Holbrook B.C., Willingham M.C., Grayson J.M. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ Tcell contraction. Immunity 2008, 28:218-230.
81. Welsh R.M., Bahl K., Marshall H.D., Urban S.L. Type 1 interferons and antiviral CD8 T-cell responses. PLoS Pathog. 2012, 8:e1002352.
82. Wu H., Tschopp J., Lin S.C. Smac mimetics and TNFalpha: a dangerous liaison?. Cell 2007, 131:655-658.
83. Zhang H.G., Fleck M., Kern E.R., Liu D., Wang Y., Hsu H.C., Yang P., Wang Z., Curiel D.T., Zhou T., Mountz J.D. Antigen presenting cells expressing Fas ligand down-modulate chronic inflammatory disease in Fas ligand-deficient mice. J.Clin. Invest. 2000, 105:813-821.
84. Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., Dong M.Q., Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325:332-336.
85. Zhang H., Zhou X., McQuade T., Li J., Chan F.K., Zhang J. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 2011, 471:373-376.
86. Zhao J., Jitkaew S., Cai Z., Choksi S., Li Q., Luo J., Liu Z.G. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. USA 2012, 109:5322-5327.
87. Zhou Q., Snipas S., Orth K., Muzio M., Dixit V.M., Salvesen G.S. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J.Biol. Chem. 1997, 272:7797-7800.