Roles of Caspases in Necrotic Cell Death

Cell

Volumn 167, Issue 7, 2016, Pages 1693-1704

  Yuan, Junying ^a   Najafov, Ayaz ^a   Py, Bénédicte F ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 11; CASPASE 4; CASPASE 5; CASPASE 8; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; TUMOR NECROSIS FACTOR RECEPTOR 1;

AUTOINFLAMMATORY DISEASE; CELL DEATH; CELL SURVIVAL; HOMEOSTASIS; HOST RESISTANCE; HUMAN; NECROPTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PYROPTOSIS; REVIEW; ANIMAL; APOPTOSIS; ENZYMOLOGY; INFECTION; INFLAMMATION; METABOLISM; NECROSIS; PATHOLOGY;

ANIMALS; APOPTOSIS; CASPASES; HUMANS; INFECTION; INFLAMMATION; NECROSIS; PYROPTOSIS;

EID: 85006248546     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.11.047     Document Type: Review

References (100)

1. Aachoui, Y., Leaf, I.A., Hagar, J.A., Fontana, M.F., Campos, C.G., Zak, D.E., Tan, M.H., Cotter, P.A., Vance, R.E., Aderem, A., Miao, E.A., Caspase-11 protects against bacteria that escape the vacuole. Science 339 (2013), 975–978.
2. Aachoui, Y., Kajiwara, Y., Leaf, I.A., Mao, D., Ting, J.P., Coers, J., Aderem, A., Buxbaum, J.D., Miao, E.A., Canonical inflammasomes drive IFN-γ to prime caspase-11 in defense against a cytosol-invasive bacterium. Cell Host Microbe 18 (2015), 320–332.
3. Akhter, A., Caution, K., Abu Khweek, A., Tazi, M., Abdulrahman, B.A., Abdelaziz, D.H., Voss, O.H., Doseff, A.I., Hassan, H., Azad, A.K., et al. Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37 (2012), 35–47.
4. Arslan, S.C., Scheidereit, C., The prevalence of TNFα-induced necrosis over apoptosis is determined by TAK1-RIP1 interplay. PLoS ONE, 6, 2011, e26069.
5. Bauernfeind, F.G., Horvath, G., Stutz, A., Alnemri, E.S., MacDonald, K., Speert, D., Fernandes-Alnemri, T., Wu, J., Monks, B.G., Fitzgerald, K.A., et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183 (2009), 787–791.
6. Broz, P., Ruby, T., Belhocine, K., Bouley, D.M., Kayagaki, N., Dixit, V.M., Monack, D.M., Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490 (2012), 288–291.
7. Cerretti, D.P., Kozlosky, C.J., Mosley, B., Nelson, N., Van Ness, K., Greenstreet, T.A., March, C.J., Kronheim, S.R., Druck, T., Cannizzaro, L.A., et al. Molecular cloning of the interleukin-1 beta converting enzyme. Science 256 (1992), 97–100.
8. 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 137 (2009), 1112–1123.
9. Cirulli, E.T., Lasseigne, B.N., Petrovski, S., Sapp, P.C., Dion, P.A., Leblond, C.S., Couthouis, J., Lu, Y.F., Wang, Q., Krueger, B.J., et al., FALS Sequencing Consortium. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science 347 (2015), 1436–1441.
10. Damgaard, R.B., Walker, J.A., Marco-Casanova, P., Morgan, N.V., Titheradge, H.L., Elliott, P.R., McHale, D., Maher, E.R., McKenzie, A.N., Komander, D., The deubiquitinase OTULIN is an essential negative regulator of inflammation and autoimmunity. Cell 166 (2016), 1215–1230.e20.
11. de Zoete, M.R., Palm, N.W., Zhu, S., Flavell, R.A., Inflammasomes. Cold Spring Harb. Perspect. Biol., 6, 2014, a016287.
12. Degterev, A., Boyce, M., Yuan, J., A decade of caspases. Oncogene 22 (2003), 8543–8567.
13. Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G.D., Mitchison, T.J., Moskowitz, M.A., Yuan, J., Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1 (2005), 112–119.
14. Degterev, A., Hitomi, J., Germscheid, M., Ch'en, I.L., Korkina, O., Teng, X., Abbott, D., Cuny, G.D., Yuan, C., Wagner, G., et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4 (2008), 313–321.
15. Dillon, C.P., Oberst, A., Weinlich, R., Janke, L.J., Kang, T.B., Ben-Moshe, T., Mak, T.W., Wallach, D., Green, D.R., Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep. 1 (2012), 401–407.
16. Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H., Wang, D.C., Shao, F., Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535 (2016), 111–116.
17. Dondelinger, Y., Declercq, W., Montessuit, S., Roelandt, R., Goncalves, A., Bruggeman, I., Hulpiau, P., Weber, K., Sehon, C.A., Marquis, R.W., et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7 (2014), 971–981.
18. Dondelinger, Y., Jouan-Lanhouet, S., Divert, T., Theatre, E., Bertin, J., Gough, P.J., Giansanti, P., Heck, A.J., Dejardin, E., Vandenabeele, P., Bertrand, M.J., NF-κB-independent role of IKKα/IKKβ in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol. Cell 60 (2015), 63–76.
19. Draber, P., Kupka, S., Reichert, M., Draberova, H., Lafont, E., de Miguel, D., Spilgies, L., Surinova, S., Taraborrelli, L., Hartwig, T., et al. LUBAC-recruited CYLD and A20 regulate gene activation and cell death by exerting opposing effects on linear ubiquitin in signaling complexes. Cell Rep. 13 (2015), 2258–2272.
20. Fernandes-Alnemri, T., Armstrong, R.C., Krebs, J., Srinivasula, S.M., Wang, L., Bullrich, F., Fritz, L.C., Trapani, J.A., Tomaselli, K.J., Litwack, G., Alnemri, E.S., In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl. Acad. Sci. USA 93 (1996), 7464–7469.
21. Fink, S.L., Cookson, B.T., Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8 (2006), 1812–1825.
22. Gagliardini, V., Fernandez, P.A., Lee, R.K., Drexler, H.C., Rotello, R.J., Fishman, M.C., Yuan, J., Prevention of vertebrate neuronal death by the crmA gene. Science 263 (1994), 826–828.
23. Gerlach, B., Cordier, S.M., Schmukle, A.C., Emmerich, C.H., Rieser, E., Haas, T.L., Webb, A.I., Rickard, J.A., Anderton, H., Wong, W.W., et al. Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471 (2011), 591–596.
24. Green, D.R., Apoptotic pathways: the roads to ruin. Cell 94 (1998), 695–698.
25. Haas, T.L., Emmerich, C.H., Gerlach, B., Schmukle, A.C., Cordier, S.M., Rieser, E., Feltham, R., Vince, J., Warnken, U., Wenger, T., et al. 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 (2009), 831–844.
26. Hagar, J.A., Powell, D.A., Aachoui, Y., Ernst, R.K., Miao, E.A., Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341 (2013), 1250–1253.
27. He, S., Wang, L., Miao, L., Wang, T., Du, F., Zhao, L., Wang, X., Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137 (2009), 1100–1111.
28. He, W.T., Wan, H., Hu, L., Chen, P., Wang, X., Huang, Z., Yang, Z.H., Zhong, C.Q., Han, J., Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 25 (2015), 1285–1298.
29. Hildebrand, J.M., Tanzer, M.C., Lucet, I.S., Young, S.N., Spall, S.K., Sharma, P., Pierotti, C., Garnier, J.M., Dobson, R.C., Webb, A.I., et al. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc. Natl. Acad. Sci. USA 111 (2014), 15072–15077.
30. Hiscott, J., Marois, J., Garoufalis, J., D'Addario, M., Roulston, A., Kwan, I., Pepin, N., Lacoste, J., Nguyen, H., Bensi, G., et al. Characterization of a functional NF-kappa B site in the human interleukin 1 beta promoter: evidence for a positive autoregulatory loop. Mol. Cell. Biol. 13 (1993), 6231–6240.
31. Hitomi, J., Christofferson, D.E., Ng, A., Yao, J., Degterev, A., Xavier, R.J., Yuan, J., Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135 (2008), 1311–1323.
32. 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. 1 (2000), 489–495.
33. Hou, Y., Li, F., Karin, M., Ostrowski, M.C., Analysis of the IKKbeta/NF-kappaB signaling pathway during embryonic angiogenesis. Dev. Dyn. 237 (2008), 2926–2935.
34. Ikeda, F., Deribe, Y.L., Skånland, S.S., Stieglitz, B., Grabbe, C., Franz-Wachtel, M., van Wijk, S.J., Goswami, P., Nagy, V., Terzic, J., et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-κB activity and apoptosis. Nature 471 (2011), 637–641.
35. Ito, Y., Ofengeim, D., Najafov, A., Das, S., Saberi, S., Li, Y., Hitomi, J., Zhu, H., Chen, H., Mayo, L., et al. RIPK1 mediates axonal degeneration by promoting inflammation and necroptosis in ALS. Science 353 (2016), 603–608.
36. Joosten, L.A., Van De Veerdonk, F.L., Vonk, A.G., Boerman, O.C., Keuter, M., Fantuzzi, G., Verschueren, I., Van Der Poll, T., Dinarello, C.A., Kullberg, B.J., et al. Differential susceptibility to lethal endotoxaemia in mice deficient in IL-1α, IL-1β or IL-1 receptor type I. APMIS 118 (2010), 1000–1007.
37. 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 471 (2011), 368–372.
38. Kang, S.J., Wang, S., Hara, H., Peterson, E.P., Namura, S., Amin-Hanjani, S., Huang, Z., Srinivasan, A., Tomaselli, K.J., Thornberry, N.A., et al. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 149 (2000), 613–622.
39. Kang, S.J., Wang, S., Kuida, K., Yuan, J., Distinct downstream pathways of caspase-11 in regulating apoptosis and cytokine maturation during septic shock response. Cell Death Differ. 9 (2002), 1115–1125.
40. Kastner, D.L., Aksentijevich, I., Goldbach-Mansky, R., Autoinflammatory disease reloaded: a clinical perspective. Cell 140 (2010), 784–790.
41. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., Newton, K., Qu, Y., Liu, J., Heldens, S., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479 (2011), 117–121.
42. Kayagaki, N., Wong, M.T., Stowe, I.B., Ramani, S.R., Gonzalez, L.C., Akashi-Takamura, S., Miyake, K., Zhang, J., Lee, W.P., Muszyński, A., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341 (2013), 1246–1249.
43. Kayagaki, N., Stowe, I.B., Lee, B.L., O'Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q.T., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526 (2015), 666–671.
44. Komander, D., Reyes-Turcu, F., Licchesi, J.D., Odenwaelder, P., Wilkinson, K.D., Barford, D., Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10 (2009), 466–473.
45. Krueger, A., Schmitz, I., Baumann, S., Krammer, P.H., Kirchhoff, S., Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276 (2001), 20633–20640.
46. Lee, E.G., Boone, D.L., Chai, S., Libby, S.L., Chien, M., Lodolce, J.P., Ma, A., Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289 (2000), 2350–2354.
47. Legarda-Addison, D., Hase, H., O'Donnell, M.A., Ting, A.T., NEMO/IKKgamma regulates an early NF-kappaB-independent cell-death checkpoint during TNF signaling. Cell Death Differ. 16 (2009), 1279–1288.
48. 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 94 (1998), 491–501.
49. Li, J., Brieher, W.M., Scimone, M.L., Kang, S.J., Zhu, H., Yin, H., von Andrian, U.H., Mitchison, T., Yuan, J., Caspase-11 regulates cell migration by promoting Aip1-Cofilin-mediated actin depolymerization. Nat. Cell Biol. 9 (2007), 276–286.
50. Lin, Y., Devin, A., Rodriguez, Y., Liu, Z.G., Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13 (1999), 2514–2526.
51. Liu, X., Zhang, Z., Ruan, J., Pan, Y., Magupalli, V.G., Wu, H., Lieberman, J., Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535 (2016), 153–158.
52. Mandal, P., Berger, S.B., Pillay, S., Moriwaki, K., Huang, C., Guo, H., Lich, J.D., Finger, J., Kasparcova, V., Votta, B., et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56 (2014), 481–495.
53. Maruyama, H., Morino, H., Ito, H., Izumi, Y., Kato, H., Watanabe, Y., Kinoshita, Y., Kamada, M., Nodera, H., Suzuki, H., et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465 (2010), 223–226.
54. McDermott, M.F., Aksentijevich, I., Galon, J., McDermott, E.M., Ogunkolade, B.W., Centola, M., Mansfield, E., Gadina, M., Karenko, L., Pettersson, T., et al. Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell 97 (1999), 133–144.
55. Meunier, E., Dick, M.S., Dreier, R.F., Schürmann, N., Kenzelmann Broz, D., Warming, S., Roose-Girma, M., Bumann, D., Kayagaki, N., Takeda, K., et al. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509 (2014), 366–370.
56. 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 75 (1993), 653–660.
57. Moulin, M., Anderton, H., Voss, A.K., Thomas, T., Wong, W.W., Bankovacki, A., Feltham, R., Chau, D., Cook, W.D., Silke, J., Vaux, D.L., IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J. 31 (2012), 1679–1691.
58. 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 39 (2013), 443–453.
59. Muzio, M., Chinnaiyan, A.M., Kischkel, F.C., O'Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J.D., Zhang, M., Gentz, R., et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85 (1996), 817–827.
60. Netea, M.G., Nold-Petry, C.A., Nold, M.F., Joosten, L.A., Opitz, B., van der Meer, J.H., van de Veerdonk, F.L., Ferwerda, G., Heinhuis, B., Devesa, I., et al. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113 (2009), 2324–2335.
61. Newton, K., Dugger, D.L., Wickliffe, K.E., Kapoor, N., de Almagro, M.C., Vucic, D., Komuves, L., Ferrando, R.E., French, D.M., Webster, J., et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343 (2014), 1357–1360.
62. Newton, K., Dugger, D.L., Maltzman, A., Greve, J.M., Hedehus, M., Martin-McNulty, B., Carano, R.A., Cao, T.C., van Bruggen, N., Bernstein, L., et al. RIPK3 deficiency or catalytically inactive RIPK1 provides greater benefit than MLKL deficiency in mouse models of inflammation and tissue injury. Cell Death Differ. 23 (2016), 1565–1576.
63. Nogusa, S., Thapa, R.J., Dillon, C.P., Liedmann, S., Oguin, T.H. 3rd, Ingram, J.P., Rodriguez, D.A., Kosoff, R., Sharma, S., Sturm, O., et al. RIPK3 activates parallel pathways of MLKL-driven necroptosis and FADD-mediated apoptosis to protect against influenza A virus. Cell Host Microbe 20 (2016), 13–24.
64. 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. 13 (2011), 1437–1442.
65. 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 471 (2011), 363–367.
66. Ofengeim, D., Yuan, J., Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 14 (2013), 727–736.
67. Ofengeim, D., Ito, Y., Najafov, A., Zhang, Y., Shan, B., DeWitt, J.P., Ye, J., Zhang, X., Chang, A., Vakifahmetoglu-Norberg, H., et al. Activation of necroptosis in multiple sclerosis. Cell Rep. 10 (2015), 1836–1849.
68. Onizawa, M., Oshima, S., Schulze-Topphoff, U., Oses-Prieto, J.A., Lu, T., Tavares, R., Prodhomme, T., Duong, B., Whang, M.I., Advincula, R., et al. The ubiquitin-modifying enzyme A20 restricts ubiquitination of the kinase RIPK3 and protects cells from necroptosis. Nat. Immunol. 16 (2015), 618–627.
69. Pilla, D.M., Hagar, J.A., Haldar, A.K., Mason, A.K., Degrandi, D., Pfeffer, K., Ernst, R.K., Yamamoto, M., Miao, E.A., Coers, J., Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc. Natl. Acad. Sci. USA 111 (2014), 6046–6051.
70. Pobezinskaya, Y.L., Kim, Y.S., Choksi, S., Morgan, M.J., Li, T., Liu, C., Liu, Z., The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 9 (2008), 1047–1054.
71. Py, B.F., Jin, M., Desai, B.N., Penumaka, A., Zhu, H., Kober, M., Dietrich, A., Lipinski, M.M., Henry, T., Clapham, D.E., Yuan, J., Caspase-11 controls interleukin-1β release through degradation of TRPC1. Cell Rep. 6 (2014), 1122–1128.
72. Rathinam, V.A., Fitzgerald, K.A., Inflammasome complexes: emerging mechanisms and effector functions. Cell 165 (2016), 792–800.
73. Rathinam, V.A., Vanaja, S.K., Waggoner, L., Sokolovska, A., Becker, C., Stuart, L.M., Leong, J.M., Fitzgerald, K.A., TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150 (2012), 606–619.
74. Russo, H.M., Rathkey, J., Boyd-Tressler, A., Katsnelson, M.A., Abbott, D.W., Dubyak, G.R., Active caspase-1 induces plasma membrane pores that precede pyroptotic lysis and are blocked by lanthanides. J. Immunol. 197 (2016), 1353–1367.
75. Schlicher, L., Wissler, M., Preiss, F., Brauns-Schubert, P., Jakob, C., Dumit, V., Borner, C., Dengjel, J., Maurer, U., SPATA2 promotes CYLD activity and regulates TNF-induced NF-κB signaling and cell death. EMBO Rep. 17 (2016), 1485–1497.
76. Schmid-Burgk, J.L., Gaidt, M.M., Schmidt, T., Ebert, T.S., Bartok, E., Hornung, V., Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur. J. Immunol. 45 (2015), 2911–2917.
77. Shi, J., Zhao, Y., Wang, Y., Gao, W., Ding, J., Li, P., Hu, L., Shao, F., Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514 (2014), 187–192.
78. Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y., Cai, T., Wang, F., Shao, F., Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526 (2015), 660–665.
79. Skaug, B., Chen, J., Du, F., He, J., Ma, A., Chen, Z.J., Direct, noncatalytic mechanism of IKK inhibition by A20. Mol. Cell 44 (2011), 559–571.
80. Song, H.Y., Rothe, M., Goeddel, D.V., The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc. Natl. Acad. Sci. USA 93 (1996), 6721–6725.
81. Storek, K.M., Gertsvolf, N.A., Ohlson, M.B., Monack, D.M., cGAS and Ifi204 cooperate to produce type I IFNs in response to Francisella infection. J. Immunol. 194 (2015), 3236–3245.
82. 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 148 (2012), 213–227.
83. Thornberry, N.A., Bull, H.G., Calaycay, J.R., Chapman, K.T., Howard, A.D., Kostura, M.J., Miller, D.K., Molineaux, S.M., Weidner, J.R., Aunins, J., et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356 (1992), 768–774.
84. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y., Kirisako, T., Kamei, K., Nakagawa, T., Kato, M., Murata, S., Yamaoka, S., et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 11 (2009), 123–132.
85. Vereecke, L., Sze, M., Mc Guire, C., Rogiers, B., Chu, Y., Schmidt-Supprian, M., Pasparakis, M., Beyaert, R., van Loo, G., Enterocyte-specific A20 deficiency sensitizes to tumor necrosis factor-induced toxicity and experimental colitis. J. Exp. Med. 207 (2010), 1513–1523.
86. Viganò, E., Diamond, C.E., Spreafico, R., Balachander, A., Sobota, R.M., Mortellaro, A., Human caspase-4 and caspase-5 regulate the one-step non-canonical inflammasome activation in monocytes. Nat. Commun., 6, 2015, 8761.
87. Wagner, S.A., Satpathy, S., Beli, P., Choudhary, C., SPATA2 links CYLD to the TNF-α receptor signaling complex and modulates the receptor signaling outcomes. EMBO J. 35 (2016), 1868–1884.
88. Wang, S., Miura, M., Jung, Yk., Zhu, H., Gagliardini, V., Shi, L., Greenberg, A.H., Yuan, J., Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE. J. Biol. Chem. 271 (1996), 20580–20587.
89. Wang, S., Miura, M., Jung, Y.K., Zhu, H., Li, E., Yuan, J., Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92 (1998), 501–509.
90. Wang, L., Du, F., Wang, X., TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133 (2008), 693–703.
91. Wang, H., Sun, L., Su, L., Rizo, J., Liu, L., Wang, L.F., Wang, F.S., Wang, X., Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54 (2014), 133–146.
92. Wertz, I.E., O'Rourke, K.M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R., Boone, D.L., et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430 (2004), 694–699.
93. Yang, D., He, Y., Muñoz-Planillo, R., Liu, Q., Núñez, G., Caspase-11 requires the Pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity 43 (2015), 923–932.
94. Yuan, J., Shaham, S., Ledoux, S., Ellis, H.M., Horvitz, H.R., The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75 (1993), 641–652.
95. Zanoni, I., Tan, Y., Di Gioia, M., Broggi, A., Ruan, J., Shi, J., Donado, C.A., Shao, F., Wu, H., Springstead, J.R., Kagan, J.C., An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science 352 (2016), 1232–1236.
96. 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 325 (2009), 332–336.
97. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.
98. Zhou, W., Yuan, J., Necroptosis in health and diseases. Semin. Cell Dev. Biol. 35 (2014), 14–23.
99. Zhou, Q., Wang, H., Schwartz, D.M., Stoffels, M., Park, Y.H., Zhang, Y., Yang, D., Demirkaya, E., Takeuchi, M., Tsai, W.L., et al. Loss-of-function mutations in TNFAIP3 leading to A20 haploinsufficiency cause an early-onset autoinflammatory disease. Nat. Genet. 48 (2016), 67–73.
100. Zilberman-Rudenko, J., Shawver, L.M., Wessel, A.W., Luo, Y., Pelletier, M., Tsai, W.L., Lee, Y., Vonortas, S., Cheng, L., Ashwell, J.D., et al. Recruitment of A20 by the C-terminal domain of NEMO suppresses NF-κB activation and autoinflammatory disease. Proc. Natl. Acad. Sci. USA 113 (2016), 1612–1617.