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Annual Review of Biochemistry

Volume 85, 2016

Necroptosis and Inflammation

Abstract

Necroptosis is a regulated form of necrosis, with the dying cell rupturing and releasing intracellular components that can trigger an innate immune response. Toll-like receptor 3 and 4 agonists, tumor necrosis factor, certain viral infections, or the T cell receptor can trigger necroptosis if the activity of the protease caspase-8 is compromised. Necroptosis signaling is modulated by the kinase RIPK1 and requires the kinase RIPK3 and the pseudokinase MLKL. Either RIPK3 deficiency or RIPK1 inhibition confers resistance in various animal disease models, suggesting that inflammation caused by necroptosis contributes to tissue damage and that inhibitors of these kinases could have therapeutic potential. Recent studies have revealed unexpected complexity in the regulation of cell death programs by RIPK1 and RIPK3 with the possibility that necroptosis is but one mechanism by which these kinases promote inflammation.

Keyword(s): MLKL, RIPK1, RIPK3
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2016-06-02
2024-04-20
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Literature Cited

  1. Kerr JF, Wyllie AH, Currie AR. 1.  1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239–57 [Google Scholar]
  2. Crawford ED, Wells JA. 2.  2011. Caspase substrates and cellular remodeling. Annu. Rev. Biochem. 80:1055–87 [Google Scholar]
  3. Ravichandran KS. 3.  2011. Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35:445–55 [Google Scholar]
  4. Rickard JA, Anderton H, Etemadi N, Nachbur U, Darding M. 4.  et al. 2014. TNFR1-dependent cell death drives inflammation in Sharpin-deficient mice. eLife 3:e03464 [Google Scholar]
  5. Kumari S, Redouane Y, Lopez-Mosqueda J, Shiraishi R, Romanowska M. 5.  et al. 2014. Sharpin prevents skin inflammation by inhibiting TNFR1-induced keratinocyte apoptosis. eLife 3:e03422 [Google Scholar]
  6. Panayotova-Dimitrova D, Feoktistova M, Ploesser M, Kellert B, Hupe M. 6.  et al. 2013. cFLIP regulates skin homeostasis and protects against TNF-induced keratinocyte apoptosis. Cell Rep. 5:397–408 [Google Scholar]
  7. Lamkanfi M, Dixit VM. 7.  2014. Mechanisms and functions of inflammasomes. Cell 157:1013–22 [Google Scholar]
  8. Vercammen D, Beyaert R, Denecker G, Goossens V, van Loo G. 8.  et al. 1998. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187:1477–85 [Google Scholar]
  9. Vercammen D, Brouckaert G, Denecker G, Van de Craen M, Declercq W. 9.  et al. 1998. Dual signaling of the Fas receptor: initiation of both apoptotic and necrotic cell death pathways. J. Exp. Med. 188:919–30 [Google Scholar]
  10. Holler N, Zaru R, Micheau O, Thome M, Attinger A. 10.  et al. 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1:489–95 [Google Scholar]
  11. Matsumura H, Shimizu Y, Ohsawa Y, Kawahara A, Uchiyama Y, Nagata S. 11.  2000. Necrotic death pathway in Fas receptor signaling. J. Cell. Biol. 151:1247–56 [Google Scholar]
  12. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L. 12.  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]
  13. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P. 13.  et al. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1:112–19 [Google Scholar]
  14. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O. 14.  et al. 2008. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4:313–21 [Google Scholar]
  15. Smith CC, Davidson SM, Lim SY, Simpkin JC, Hothersall JS, Yellon DM. 15.  2007. Necrostatin: a potentially novel cardioprotective agent?. Cardiovasc. Drugs Ther. 21:227–33 [Google Scholar]
  16. Takahashi N, Duprez L, Grootjans S, Cauwels A, Nerinckx W. 16.  et al. 2012. Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models. Cell Death Dis 3:e437 [Google Scholar]
  17. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ. 17.  et al. 2009. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325:332–36 [Google Scholar]
  18. Cho YS, Challa S, Moquin D, Genga R, Ray TD. 18.  et al. 2009. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112–23 [Google Scholar]
  19. He S, Wang L, Miao L, Wang T, Du F. 19.  et al. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137:1100–11 [Google Scholar]
  20. Newton K, Sun X, Dixit VM. 20.  2004. Kinase RIP3 is dispensable for normal NF-κBs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol. Cell. Biol. 24:1464–69 [Google Scholar]
  21. Duprez L, Takahashi N, Van Hauwermeiren F, Vandendriessche B, Goossens V. 21.  et al. 2011. RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 35:908–18 [Google Scholar]
  22. Newton K, Dugger DL, Wickliffe KE, Kapoor N, de Almagro MC. 22.  et al. 2014. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343:1357–60 [Google Scholar]
  23. Lin J, Li H, Yang M, Ren J, Huang Z. 23.  et al. 2013. A role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep. 3:200–10 [Google Scholar]
  24. Murakami Y, Matsumoto H, Roh M, Suzuki J, Hisatomi T. 24.  et al. 2012. Receptor interacting protein kinase mediates necrotic cone but not rod cell death in a mouse model of inherited degeneration. PNAS 109:14598–603 [Google Scholar]
  25. Murakami Y, Matsumoto H, Roh M, Giani A, Kataoka K. 25.  et al. 2014. Programmed necrosis, not apoptosis, is a key mediator of cell loss and DAMP-mediated inflammation in dsRNA-induced retinal degeneration. Cell Death Differ. 21:270–77 [Google Scholar]
  26. Luedde M, Lutz M, Carter N, Sosna J, Jacoby C. 26.  et al. 2014. RIP3, a kinase promoting necroptotic cell death, mediates adverse remodelling after myocardial infarction. Cardiovasc. Res. 103:206–16 [Google Scholar]
  27. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB. 27.  et al. 2013. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. PNAS 110:12024–29 [Google Scholar]
  28. Gautheron J, Vucur M, Reisinger F, Cardenas DV, Roderburg C. 28.  et al. 2014. A positive feedback loop between RIP3 and JNK controls non-alcoholic steatohepatitis. EMBO Mol. Med. 6:1062–74 [Google Scholar]
  29. Vitner EB, Salomon R, Farfel-Becker T, Meshcheriakova A, Ali M. 29.  et al. 2014. RIPK3 as a potential therapeutic target for Gaucher's disease. Nat. Med. 20:204–8 [Google Scholar]
  30. Roychowdhury S, McMullen MR, Pisano SG, Liu X, Nagy LE. 30.  2013. Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 57:1773–83 [Google Scholar]
  31. Micheau O, Tschopp J. 31.  2003. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114:181–90 [Google Scholar]
  32. Ermolaeva MA, Michallet MC, Papadopoulou N, Utermohlen O, Kranidioti K. 32.  et al. 2008. Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat. Immunol. 9:1037–46 [Google Scholar]
  33. Pobezinskaya YL, Kim YS, Choksi S, Morgan MJ, Li T. 33.  et al. 2008. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 9:1047–54 [Google Scholar]
  34. Hsu H, Shu HB, Pan MG, Goeddel DV. 34.  1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84:299–308 [Google Scholar]
  35. Shu HB, Takeuchi M, Goeddel DV. 35.  1996. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. PNAS 93:13973–78 [Google Scholar]
  36. Vince JE, Pantaki D, Feltham R, Mace PD, Cordier SM. 36.  et al. 2009. TRAF2 must bind to cellular inhibitors of apoptosis for tumor necrosis factor (TNF) to efficiently activate NF-κB and to prevent TNF-induced apoptosis. J. Biol. Chem. 284:35906–15 [Google Scholar]
  37. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K. 37.  et al. 2008. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor α (TNFα)-induced NF-κB activation. J. Biol. Chem. 283:24295–99 [Google Scholar]
  38. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C. 38.  et al. 2008. Both cIAP1 and cIAP2 regulate TNFα-mediated NF-κB activation. PNAS 105:11778–83 [Google Scholar]
  39. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM. 39.  et al. 2009. Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol. Cell 36:831–44 [Google Scholar]
  40. Cheung PC, Nebreda AR, Cohen P. 40.  2004. TAB3, a new binding partner of the protein kinase TAK1. Biochem. J. 378:27–34 [Google Scholar]
  41. Kanayama A, Seth RB, Sun L, Ea CK, Hong M. 41.  et al. 2004. TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol. Cell 15:535–48 [Google Scholar]
  42. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M. 42.  et al. 2011. SHARPIN is a component of the NF-κB-activating linear ubiquitin chain assembly complex. Nature 471:633–36 [Google Scholar]
  43. Ikeda F, Deribe YL, Skanland SS, Stieglitz B, Grabbe C. 43.  et al. 2011. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471:637–41 [Google Scholar]
  44. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E. 44.  et al. 2011. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471:591–96 [Google Scholar]
  45. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H. 45.  et al. 2006. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25:4877–87 [Google Scholar]
  46. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A. 46.  et al. 2010. c-IAP1 and UbcH5 promote K11-linked polyubiquitination of RIP1 in TNF signalling. EMBO J. 29:4198–209 [Google Scholar]
  47. Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N. 47.  et al. 2009. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell 136:1098–109 [Google Scholar]
  48. Lo YC, Lin SC, Rospigliosi CC, Conze DB, Wu CJ. 48.  et al. 2009. Structural basis for recognition of diubiquitins by NEMO. Mol. Cell 33:602–15 [Google Scholar]
  49. Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG. 49.  et al. 2013. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. PNAS 110:15247–52 [Google Scholar]
  50. Zhang J, Clark K, Lawrence T, Peggie MW, Cohen P. 50.  2014. An unexpected twist to the activation of IKKβ: TAK1 primes IKKβ for activation by autophosphorylation. Biochem. J. 461:531–37 [Google Scholar]
  51. Newton K, Dixit VM. 51.  2012. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4:a006049 [Google Scholar]
  52. Dickens LS, Boyd RS, Jukes-Jones R, Hughes MA, Robinson GL. 52.  et al. 2012. A death effector domain chain DISC model reveals a crucial role for caspase-8 chain assembly in mediating apoptotic cell death. Mol. Cell 47:291–305 [Google Scholar]
  53. Schleich K, Warnken U, Fricker N, Ozturk S, Richter P. 53.  et al. 2012. Stoichiometry of the CD95 death-inducing signaling complex: experimental and modeling evidence for a death effector domain chain model. Mol. Cell 47:306–19 [Google Scholar]
  54. Majkut J, Sgobba M, Holohan C, Crawford N, Logan AE. 54.  et al. 2014. Differential affinity of FLIP and procaspase 8 for FADD's DED binding surfaces regulates DISC assembly. Nat. Commun. 5:3350 [Google Scholar]
  55. Sun L, Wang H, Wang Z, He S, Chen S. 55.  et al. 2012. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148:213–27 [Google Scholar]
  56. Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q. 56.  et al. 2012. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. PNAS 109:5322–27 [Google Scholar]
  57. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG. 57.  et al. 2013. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39:443–53 [Google Scholar]
  58. Wu J, Huang Z, Ren J, Zhang Z, He P. 58.  et al. 2013. Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res. 23:994–1006 [Google Scholar]
  59. Sun X, Yin J, Starovasnik MA, Fairbrother WJ, Dixit VM. 59.  2002. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J. Biol. Chem. 277:9505–11 [Google Scholar]
  60. Wu XN, Yang ZH, Wang XK, Zhang Y, Wan H. 60.  et al. 2014. Distinct roles of RIP1-RIP3 hetero- and RIP3-RIP3 homo-interaction in mediating necroptosis. Cell Death Differ. 21:1709–20 [Google Scholar]
  61. Chen W, Zhou Z, Li L, Zhong CQ, Zheng X. 61.  et al. 2013. 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. 288:16247–61 [Google Scholar]
  62. Wang H, Sun L, Su L, Rizo J, Liu L. 62.  et al. 2014. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54:133–46 [Google Scholar]
  63. Su L, Quade B, Wang H, Sun L, Wang X, Rizo J. 63.  2014. A plug release mechanism for membrane permeation by MLKL. Structure 22:1489–500 [Google Scholar]
  64. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S. 64.  et al. 2014. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16:55–65 [Google Scholar]
  65. Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A. 65.  et al. 2014. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7:971–81 [Google Scholar]
  66. Hildebrand JM, Tanzer MC, Lucet IS, Young SN, Spall SK. 66.  et al. 2014. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. PNAS 111:15072–77 [Google Scholar]
  67. Chen X, Li W, Ren J, Huang D, He WT. 67.  et al. 2014. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 24:105–21 [Google Scholar]
  68. He S, Liang Y, Shao F, Wang X. 68.  2011. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. PNAS 108:20054–59 [Google Scholar]
  69. Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW. 69.  et al. 2013. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288:31268–79 [Google Scholar]
  70. Meylan E, Burns K, Hofmann K, Blancheteau V, Martinon F. 70.  et al. 2004. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat. Immunol. 5:503–7 [Google Scholar]
  71. Kaiser WJ, Offermann MK. 71.  2005. Apoptosis induced by the Toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174:4942–52 [Google Scholar]
  72. Polykratis A, Hermance N, Zelic M, Roderick J, Kim C. 72.  et al. 2014. Cutting edge: RIPK1 kinase inactive mice are viable and protected from TNF-induced necroptosis in vivo. J. Immunol. 193:1539–43 [Google Scholar]
  73. Berger SB, Kasparcova V, Hoffman S, Swift B, Dare L. 73.  et al. 2014. Cutting edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J. Immunol. 192:5476–80 [Google Scholar]
  74. Upton JW, Kaiser WJ, Mocarski ES. 74.  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]
  75. Upton JW, Kaiser WJ, Mocarski ES. 75.  2010. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7:302–13 [Google Scholar]
  76. Guo H, Omoto S, Harris PA, Finger JN, Bertin J. 76.  et al. 2015. Herpes simplex virus suppresses necroptosis in human cells. Cell Host Microbe 17:243–51 [Google Scholar]
  77. Newton K, Harris AW, Bath ML, Smith KG, Strasser A. 77.  1998. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO. J. 17:706–18 [Google Scholar]
  78. Salmena L, Lemmers B, Hakem A, Matysiak-Zablocki E, Murakami K. 78.  et al. 2003. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17:883–95 [Google Scholar]
  79. Zhang H, Zhou X, McQuade T, Li J, Chan FK, Zhang J. 79.  2011. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471:373–76 [Google Scholar]
  80. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P. 80.  et al. 2011. Catalytic activity of the caspase-8–FLIPL complex inhibits RIPK3-dependent necrosis. Nature 471:363–67 [Google Scholar]
  81. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP. 81.  et al. 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471:368–72 [Google Scholar]
  82. Ch'en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM. 82.  2011. Mechanisms of necroptosis in T cells. J. Exp. Med. 208:633–41 [Google Scholar]
  83. Lu JV, Weist BM, van Raam BJ, Marro BS, Nguyen LV. 83.  et al. 2011. Complementary roles of Fas-associated death domain (FADD) and receptor interacting protein kinase-3 (RIPK3) in T-cell homeostasis and antiviral immunity. PNAS 108:15312–17 [Google Scholar]
  84. Leverrier S, Salvesen GS, Walsh CM. 84.  2011. Enzymatically active single chain caspase-8 maintains T-cell survival during clonal expansion. Cell Death Differ. 18:90–98 [Google Scholar]
  85. Welz PS, Wullaert A, Vlantis K, Kondylis V, Fernandez-Majada V. 85.  et al. 2011. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 477:330–34 [Google Scholar]
  86. Bonnet MC, Preukschat D, Welz PS, van Loo G, Ermolaeva MA. 86.  et al. 2011. The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 35:572–82 [Google Scholar]
  87. Dillon CP, Oberst A, Weinlich R, Janke LJ, Kang TB. 87.  et al. 2012. Survival function of the FADD-CASPASE-8-cFLIPL complex. Cell Rep. 1:401–7 [Google Scholar]
  88. Weinlich R, Oberst A, Dillon CP, Janke LJ, Milasta S. 88.  et al. 2013. Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep. 5:340–48 [Google Scholar]
  89. Dillon CP, Weinlich R, Rodriguez DA, Cripps JG, Quarato G. 89.  et al. 2014. RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 157:1189–202 [Google Scholar]
  90. Kang TB, Oh GS, Scandella E, Bolinger B, Ludewig B. 90.  et al. 2008. Mutation of a self-processing site in caspase-8 compromises its apoptotic but not its nonapoptotic functions in bacterial artificial chromosome-transgenic mice. J. Immunol. 181:2522–32 [Google Scholar]
  91. Smith KG, Strasser A, Vaux DL. 91.  1996. CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO-1)-transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. EMBO J. 15:5167–76 [Google Scholar]
  92. Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS. 92.  et al. 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 9:267–76 [Google Scholar]
  93. Yeh WC, de la Pompa JL, McCurrach ME, Shu HB, Elia AJ. 93.  et al. 1998. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954–58 [Google Scholar]
  94. Yeh WC, Itie A, Elia AJ, Ng M, Shu HB. 94.  et al. 2000. Requirement for casper (c-FLIP) in regulation of death receptor–induced apoptosis and embryonic development. Immunity 12:633–42 [Google Scholar]
  95. Pop C, Oberst A, Drag M, Van Raam BJ, Riedl SJ. 95.  et al. 2011. FLIPL induces caspase 8 activity in the absence of interdomain caspase 8 cleavage and alters substrate specificity. Biochem. J. 433:447–57 [Google Scholar]
  96. O'Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R. 96.  et al. 2011. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat. Cell Biol. 13:1437–42 [Google Scholar]
  97. Wright A, Reiley WW, Chang M, Jin W, Lee AJ. 97.  et al. 2007. Regulation of early wave of germ cell apoptosis and spermatogenesis by deubiquitinating enzyme CYLD. Dev. Cell 13:705–16 [Google Scholar]
  98. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A. 98.  et al. 2008. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135:1311–23 [Google Scholar]
  99. Wang L, Du F, Wang X. 99.  2008. TNF-α induces two distinct caspase-8 activation pathways. Cell 133:693–703 [Google Scholar]
  100. Moquin DM, McQuade T, Chan FK. 100.  2013. CYLD deubiquitinates RIP1 in the TNFα-induced necrosome to facilitate kinase activation and programmed necrosis. PLOS ONE 8:e76841 [Google Scholar]
  101. Kaiser WJ, Daley-Bauer LP, Thapa RJ, Mandal P, Berger SB. 101.  et al. 2014. RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition. PNAS 111:7753–58 [Google Scholar]
  102. McQuade T, Cho Y, Chan FK. 102.  2013. Positive and negative phosphorylation regulates RIP1- and RIP3-induced programmed necrosis. Biochem. J. 456:409–15 [Google Scholar]
  103. Weng D, Marty-Roix R, Ganesan S, Proulx MK, Vladimer GI. 103.  et al. 2014. Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death. PNAS 111:7391–96 [Google Scholar]
  104. Philip NH, Dillon CP, Snyder AG, Fitzgerald P, Wynosky-Dolfi MA. 104.  et al. 2014. Caspase-8 mediates caspase-1 processing and innate immune defense in response to bacterial blockade of NF-κB and MAPK signaling. PNAS 111:7385–90 [Google Scholar]
  105. Dondelinger Y, Aguileta MA, Goossens V, Dubuisson C, Grootjans S. 105.  et al. 2013. RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition. Cell Death Differ. 20:1381–92 [Google Scholar]
  106. Lamothe B, Lai Y, Xie M, Schneider MD, Darnay BG. 106.  2013. TAK1 is essential for osteoclast differentiation and is an important modulator of cell death by apoptosis and necroptosis. Mol. Cell. Biol. 33:582–95 [Google Scholar]
  107. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K. 107.  et al. 2011. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 18:656–65 [Google Scholar]
  108. Moulin M, Anderton H, Voss AK, Thomas T, Wong WW. 108.  et al. 2012. IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J. 31:1679–91 [Google Scholar]
  109. O'Donnell MA, Hase H, Legarda D, Ting AT. 109.  2012. NEMO inhibits programmed necrosis in an NFκB-independent manner by restraining RIP1. PLOS ONE 7:e41238 [Google Scholar]
  110. Irmler M, Thome M, Hahne M, Schneider P, Hofmann K. 110.  et al. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388:190–95 [Google Scholar]
  111. Opipari AW. Hu HM, Yabkowitz R, Dixit VM. 111.  Jr, 1992. The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J. Biol. Chem. 267:12424–27 [Google Scholar]
  112. Legarda-Addison D, Hase H, O'Donnell MA, Ting AT. 112.  2009. NEMO/IKKγ regulates an early NF-κB-independent cell-death checkpoint during TNF signaling. Cell Death Differ. 16:1279–88 [Google Scholar]
  113. de Almagro MC, Goncharov T, Newton K, Vucic D. 113.  2015. Cellular IAP proteins and LUBAC differentially regulate necrosome-associated RIP1 ubiquitination. Cell Death Dis. 6e1800
  114. Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P. 114.  1998. The death domain kinase RIP mediates the TNF-induced NF-κB signal. Immunity 8:297–303 [Google Scholar]
  115. Rickard JA, O'Donnell JA, Evans JM, Lalaoui N, Poh AR. 115.  et al. 2014. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell 157:1175–88 [Google Scholar]
  116. Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C. 116.  et al. 2014. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 513:90–94 [Google Scholar]
  117. Takahashi N, Vereecke L, Bertrand MJ, Duprez L, Berger SB. 117.  et al. 2014. RIPK1 ensures intestinal homeostasis by protecting the epithelium against apoptosis. Nature 513:95–99 [Google Scholar]
  118. Orozco S, Yatim N, Werner MR, Tran H, Gunja SY. 118.  et al. 2014. RIPK1 both positively and negatively regulates RIPK3 oligomerization and necroptosis. Cell Death Differ. 21:1511–21 [Google Scholar]
  119. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C. 119.  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]
  120. Tenev T, Bianchi K, Darding M, Broemer M, Langlais C. 120.  et al. 2011. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43:432–48 [Google Scholar]
  121. Chen W, Wu J, Li L, Zhang Z, Ren J. 121.  et al. 2015. Ppm1b negatively regulates necroptosis through dephosphorylating Rip3. Nat. Cell Biol. 17:434–44 [Google Scholar]
  122. Cusson N, Oikemus S, Kilpatrick ED, Cunningham L, Kelliher M. 122.  2002. The death domain kinase RIP protects thymocytes from tumor necrosis factor receptor type 2–induced cell death. J. Exp. Med. 196:15–26 [Google Scholar]
  123. Thapa RJ, Nogusa S, Chen P, Maki JL, Lerro A. 123.  et al. 2013. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. PNAS 110:E3109–18 [Google Scholar]
  124. McComb S, Cessford E, Alturki NA, Joseph J, Shutinoski B. 124.  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]
  125. Kearney CJ, Cullen SP, Clancy D, Martin SJ. 125.  2014. RIPK1 can function as an inhibitor rather than an initiator of RIPK3-dependent necroptosis. FEBS J. 281:4921–34 [Google Scholar]
  126. Gentle IE, Wong WW, Evans JM, Bankovacki A, Cook WD. 126.  et al. 2011. In TNF-stimulated cells, RIPK1 promotes cell survival by stabilizing TRAF2 and cIAP1, which limits induction of non-canonical NF-κB and activation of caspase-8. J. Biol. Chem. 286:13282–91 [Google Scholar]
  127. Kim JY, Morgan M, Kim DG, Lee JY, Bai L. 127.  et al. 2011. TNFα induced noncanonical NF-κB activation is attenuated by RIP1 through stabilization of TRAF2. J. Cell Sci. 124:647–56 [Google Scholar]
  128. Mandal P, Berger SB, Pillay S, Moriwaki K, Huang C. 128.  et al. 2014. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56:481–95 [Google Scholar]
  129. Lawlor KE, Khan N, Mildenhall A, Gerlic M, Croker BA. 129.  et al. 2015. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat. Commun. 6:6282 [Google Scholar]
  130. Moriwaki K, Bertin J, Gough PJ, Chan FK. 130.  2015. A RIPK3-caspase 8 complex mediates atypical pro-IL-1β processing. J. Immunol. 194:1938–44 [Google Scholar]
  131. Tsutsui H, Kayagaki N, Kuida K, Nakano H, Hayashi N. 131.  et al. 1999. Caspase-1-independent, Fas/Fas ligand-mediated IL-18 secretion from macrophages causes acute liver injury in mice. Immunity 11:359–67 [Google Scholar]
  132. Bossaller L, Chiang PI, Schmidt-Lauber C, Ganesan S, Kaiser WJ. 132.  et al. 2012. Cutting edge: FAS (CD95) mediates noncanonical IL-1β and IL-18 maturation via caspase-8 in an RIP3-independent manner. J. Immunol. 189:5508–12 [Google Scholar]
  133. Vince JE, Wong WW, Gentle I, Lawlor KE, Allam R. 133.  et al. 2012. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36:215–27 [Google Scholar]
  134. Kang TB, Yang SH, Toth B, Kovalenko A, Wallach D. 134.  2013. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38:27–40 [Google Scholar]
  135. Yabal M, Muller N, Adler H, Knies N, Gross CJ. 135.  et al. 2014. XIAP restricts TNF- and RIP3-dependent cell death and inflammasome activation. Cell Rep. 7:1796–808 [Google Scholar]
  136. Wang X, Jiang W, Yan Y, Gong T, Han J. 136.  et al. 2014. RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat. Immunol. 15:1126–33 [Google Scholar]
  137. Duong BH, Onizawa M, Oses-Prieto JA, Advincula R, Burlingame A. 137.  et al. 2015. A20 restricts ubiquitination of pro-interleukin-1β protein complexes and suppresses NLRP3 inflammasome activity. Immunity 42:55–67 [Google Scholar]
  138. Kang S, Fernandes-Alnemri T, Rogers C, Mayes L, Wang Y. 138.  et al. 2015. Caspase-8 scaffolding function and MLKL regulate NLRP3 inflammasome activation downstream of TLR3. Nat. Commun. 6:7515 [Google Scholar]
  139. Wong WW, Vince JE, Lalaoui N, Lawlor KE, Chau D. 139.  et al. 2014. cIAPs and XIAP regulate myelopoiesis through cytokine production in an RIPK1- and RIPK3-dependent manner. Blood 123:2562–72 [Google Scholar]
  140. Rodriguez DA, Weinlich R, Brown S, Guy C, Fitzgerald P. 140.  et al. 2015. Characterization of RIPK3-mediated phosphorylation of the activation loop of MLKL during necroptosis. Cell Death Differ. 23:76–88 [Google Scholar]
  141. Onizawa M, Oshima S, Schulze-Topphoff U, Oses-Prieto JA, Lu T. 141.  et al. 2015. The ubiquitin-modifying enzyme A20 restricts ubiquitination of the kinase RIPK3 and protects cells from necroptosis. Nat. Immunol. 16:618–27 [Google Scholar]
  142. Lu TT, Onizawa M, Hammer GE, Turer EE, Yin Q. 142.  et al. 2013. Dimerization and ubiquitin mediated recruitment of A20, a complex deubiquitinating enzyme. Immunity 38:896–905 [Google Scholar]
  143. De A, Dainichi T, Rathinam CV, Ghosh S. 143.  2014. The deubiquitinase activity of A20 is dispensable for NF-κB signaling. EMBO Rep. 15:775–83 [Google Scholar]
  144. Catrysse L, Vereecke L, Beyaert R, van Loo G. 144.  2014. A20 in inflammation and autoimmunity. Trends Immunol. 35:22–31 [Google Scholar]
  145. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G. 145.  2004. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. PNAS 101:11707–12 [Google Scholar]
  146. Xie T, Peng W, Yan C, Wu J, Gong X, Shi Y. 146.  2013. Structural insights into RIP3-mediated necroptotic signaling. Cell Rep. 5:70–78 [Google Scholar]
  147. Kitur K, Parker D, Nieto P, Ahn DS, Cohen TS. 147.  et al. 2015. Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage. PLOS Pathog. 11:e1004820 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060815-014830
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Necroptosis and Inflammation
Annual Review of Biochemistry 85, 743 (2016); https://doi.org/10.1146/annurev-biochem-060815-014830
/content/journals/10.1146/annurev-biochem-060815-014830
/content/journals/10.1146/annurev-biochem-060815-014830
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