Programmed necrosis in inflammation: Toward identification of the effector molecules

Science

Volumn 352, Issue 6281, 2016, Pages

  Wallach, David ^a   Kang, Tae Bong ^b   Dillon, Christopher P ^c   Green, Douglas R ^c  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Konkuk University   (South Korea)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CASPASE 4; CASPASE 5; EFFECTOR CASPASE; INITIATOR CASPASE; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MIXED LINEAGE KINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 1; RECEPTOR INTERACTING PROTEIN KINASE 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; GSDMD PROTEIN, HUMAN; MLKL PROTEIN, HUMAN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; TUMOR PROTEIN;

APOPTOSIS; ASSESSMENT METHOD; CAUSE OF DEATH; CELLS AND CELL COMPONENTS; IMMUNOASSAY; MOLECULAR ANALYSIS; PROBE; PROTEIN;

AMINO TERMINAL SEQUENCE; APOPTOSIS; CELL FUNCTION; EFFECTOR CELL; EX VIVO STUDY; GENE IDENTIFICATION; HUMAN; INFLAMMATION; MEMBRANE RUPTURE; NECROPTOSIS; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PYROPTOSIS; REVIEW; ANIMAL; METABOLISM; NECROSIS; PATHOLOGY;

ANIMALS; APOPTOSIS; CASPASE 1; CYTOKINES; HUMANS; INFLAMMATION; NECROSIS; NEOPLASM PROTEINS; PROTEIN KINASES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES;

EID: 84963543290     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aaf2154     Document Type: Review

References (69)

1. R. A. Lockshin, Z. Zakeri, Programmed cell death and apoptosis: Origins of the theory. Nat. Rev. Mol. Cell Biol. 2, 545-550 (2001). doi: 10.1038/35080097; pmid: 11433369
2. D. Wallach, T. B. Kang, A. Kovalenko, Concepts of tissue injury and cell death in inflammation: A historical perspective. Nat. Rev. Immunol. 14, 51-59 (2014). doi: 10.1038/nri3561; pmid: 24336099
3. A. Hochreiter-Hufford, K. S. Ravichandran, Clearing the dead: Apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb. Perspect. Biol. 5, a008748 (2013). doi: 10.1101/cshperspect.a008748; pmid: 23284042
4. K. Segawa, S. Nagata, An apoptotic 'eat me' signal: Phosphatidylserine exposure. Trends Cell Biol. 25, 639-650 (2015). doi: 10.1016/j.tcb.2015.08.003; pmid: 26437594
5. G. Kroemer, L. Galluzzi, O. Kepp, L. Zitvogel, Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 31, 51-72 (2013). doi: 10.1146/annurev-immunol-032712-100008; pmid: 23157435
6. A. Giodini, M. L. Albert, A whodunit: An appointment with death. Curr. Opin. Immunol. 22, 94-108 (2010). doi: 10.1016/j.coi.2010.01.023; pmid: 20171862
7. E. D. Crawford et al., Conservation of caspase substrates across metazoans suggests hierarchical importance of signaling pathways over specific targets and cleavage site motifs in apoptosis. Cell Death Differ. 19, 2040-2048 (2012). doi: 10.1038/cdd.2012.99; pmid: 22918439
8. V. A. Fadok et al., Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890-898 (1998). doi: 10.1172/JCI1112; pmid: 9466984
9. S. W. Tait, D. R. Green, Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11, 621-632 (2010). doi: 10.1038/nrm2952; pmid: 20683470
10. T. Moldoveanu, A. V. Follis, R. W. Kriwacki, D. R. Green, Many players in BCL-2 family affairs. Trends Biochem. Sci. 39, 101-111 (2014). doi: 10.1016/j.tibs.2013.12.006; pmid: 24503222
11. I. Budihardjo, H. Oliver, M. Lutter, X. Luo, X. Wang, Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15, 269-290 (1999). doi: 10.1146/annurev.cellbio.15.1.269; pmid: 10611963
12. H. H. Park et al., The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu. Rev. Immunol. 25, 561-586 (2007). doi: 10.1146/annurev.immunol.25.022106.141656; pmid: 17201679
13. G. A. Granger, W. P. Kolb, Lymphocyte in vitro cytotoxicity: Mechanisms of immune and non-immune small lymphocyte mediated target L cell destruction. J. Immunol. 101, 111-120 (1968). pmid: 5690881
14. N. H. Ruddle, B. H. Waksman, Cytotoxicity mediated by soluble antigen and lymphocytes in delayed hypersensitivity. J. Exp. Med. 128, 1267-1279 (1968). doi: 10.1084/jem.128.6.1267; pmid: 5693925
15. S. M. Laster, J. G. Wood, L. R. Gooding, Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 141, 2629-2634 (1988). pmid: 3171180
16. N. Holler et al., Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495 (2000). doi: 10.1038/82732; pmid: 11101870
17. A. Degterev et al., Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4, 313-321 (2008). doi: 10.1038/nchembio.83; pmid: 18408713
18. R. J. Thapa et al., Interferon-induced RIPl/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc. Natl. Acad. Sci. U.S.A. 110, E3109-E3118 (2013). doi: 10.1073/pnas.1301218110; pmid: 23898178
19. C. P. Dillon et al., RIPKl blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 157, 1189-1202 (2014). doi: 10.1016/j.cell.2014.04.018; pmid: 24813850
20. W. J. Kaiser et al., Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288, 31268-31279 (2013). doi: 10.1074/jbc.M113.462341; pmid: 24019532
21. J. W. Upton, W. J. Kaiser, E. S. Mocarski, DAI/ZBP1/DLM- 1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11, 290-297 (2012). doi: 10.1016/j.chom.2012.01.016; pmid: 22423968
22. Z. Huang et al., RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host Microbe 17, 229-242 (2015). doi: 10.1016/j.chom.2015.01.002; pmid: 25674982
23. X. Wang et al., Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc. Natl. Acad. Sci. U.S.A. 111, 15438-15443 (2014). doi: 10.1073/pnas.1412767111; pmid: 25316792
24. D. W. Zhang et al., RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325, 332-336 (2009). doi: 10.1126/science.1172308; pmid: 19498109
25. Y. S. Cho et al., Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123 (2009). doi: 10.1016/j.cell.2009.05.037; pmid: 19524513
26. S. He et al., Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137, 1100-1111 (2009). doi: 10.1016/j.cell.2009.05.021; pmid: 19524512
27. D. Vercammen et al., Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187, 1477-1485 (1998). doi: 10.1084/jem.187.9.1477; pmid: 9565639
28. A. Oberst et al., Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471, 363-367 (2011). doi: 10.1038/nature09852; pmid: 21368763
29. T. Tenev et al., The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43, 432-448 (2011). doi: 10.1016/j.molcel.2011.06.006; pmid: 21737329
30. L. Sun et al., Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213-227 (2012). doi: 10.1016/j.cell.2011.11.031; pmid: 22265413
31. J. Zhao et al., Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. U.S.A. 109, 5322-5327 (2012). doi: 10.1073/pnas.1200012109; pmid: 22421439
32. Z. Cai et al., Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16, 55-65 (2014). doi: 10.1038/ncb2883; pmid: 24316671
33. J. M. Murphy et al., The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443-453 (2013). doi: 10.1016/j.immuni.2013.06.018; pmid: 24012422
34. J. M. Hildebrand et al., Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc. Natl. Acad. Sei. U.S.A. 111, 15072-15077 (2014). doi: 10.1073/pnas.1408987111; pmid: 25288762
35. X. Chen et al., Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 24, 105-121 (2014). doi: 10.1038/cr.2013.171; pmid: 24366341
36. H. Wang et al., Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54, 133-146 (2014). doi: 10.1016/j.molcel.2014.03.003; pmid: 24703947
37. Y. Dondelinger et al., RIPK3 contributes to TNFRl-mediated RIPKl kinase-dependent apoptosis in conditions of clAP1/2 depletion or TAK1 kinase inhibition. Cell Death Differ. 20, 1381-1392 (2013). doi: 10.1038/cdd.2013.94; pmid: 23892367
38. K. Newton et al., Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343, 1357-1360 (2014). doi: 10.1126/science.1249361; pmid: 24557836
39. P. Mandai et al., RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56, 481-495 (2014). doi: 10.1016/j.molcel.2014.10.021; pmid: 25459880
40. Z. Wang, H. Jiang, S. Chen, F. Du, X. Wang, The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148, 228-243 (2012). doi: 10.1016/j.cell.2011.11.030; pmid: 22265414
41. T. Zhang et al., CaMKII is a RIP3 substrate mediating ischemia-and oxidative stress-induced myocardial necroptosis. Nat. Med. 22, 175-182 (2016). doi: 10.1038/nm.4017; pmid: 26726877
42. M. Pasparakis, P. Vandenabeele, Necroptosis and its role in inflammation. Nature 517, 311-320 (2015). doi: 10.1038/nature14191; pmid: 25592536
43. K. D. Marshall, C. P. Baines, Necroptosis: Is there a role for mitochondria? Front. Physiol. 5, 323 (2014). doi: 10.3389/fphys.2014.00323; pmid: 25206339
44. W. K. Joklik, T. C. Merigan, Concerning the mechanism of action of interferon. Proc. Natl. Acad. Sci. U.S.A. 56, 558-565 (1966). doi: 10.1073/pnas.56.2.558; pmid: 5229977
45. D. Aderka, D. Novick, T. Hahn, D. G. Fischer, D. Wallach, Increase of vulnerability to lymphotoxin in cells infected by vesicular stomatitis virus and its further augmentation by interferon. Cell. Immunol. 92, 218-225 (1985). doi: 10.1016/0008-8749(85)90003-6; pmid: 2986852
46. E. S. Mocarski, H. Guo, W. J. Kaiser, Necroptosis: The Trojan horse in cell autonomous antiviral host defense. Virology 479-480, 160-166 (2015). doi: 10.1016/j.virol.2015.03.016; pmid: 25819165
47. E. A. Miao et al., Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11, 1136-1142 (2010). doi: 10.1038/ni.1960; pmid: 21057511
48. J. Shi et al., Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187-192 (2014). pmid: 25119034
49. I. Jorgensen, E. A. Miao, Pyroptotic cell death defends against intracellular pathogens. Immunol. Rev. 265, 130-142 (2015). doi: 10.1111/imr.12287; pmid: 25879289
50. N. J. Agard, D. Maltby, J. A. Wells, Inflammatory stimuli regulate caspase substrate profiles. Mol. Cell. Proteomics 9, 880-893 (2010). doi: 10.1074/mcp.M900528-MCP200, pmid: 20173201
51. K. Labbé, M. Saleh, in Progress in Inflammation Research: The Inflammasomes, I. Couillin, V. Pétrilli, F. Martinon, Eds. (Springer Basel AG, Basel, 2011), pp. 17-36.
52. N. Kayagaki et al., Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666-671 (2015). doi: 10.1038/nature15541; pmid: 26375259
53. J. Shi et al., Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660-665 (2015). doi: 10.1038/nature15514; pmid: 26375003
54. W. T. He et al., Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 25, 1285-1298 (2015). doi: 10.1038/cr.2015.139; pmid: 26611636
55. D. E. Christofferson, Y. Li, J. Yuan, Control of life-or-death decisions by RIP1 kinase. Annu. Rev. Physiol. 76, 129-150 (2014). doi: 10.1146/annurev-physiol-021113-170259; pmid: 24079414
56. D. Wallach, T.-B. Kang, A. Kovalenko, The extrinsic cell death pathway and the élan mortel. Cell Death Differ. 15, 1533-1541 (2008). doi: 10.1038/cdd.2008.41; pmid: 18794887
57. R. Weinlich, D. R. Green, The two faces of receptor interacting protein kinase-1. Mol. Cell 56, 469-480 (2014). doi: 10.1016/j.molcel.2014.11.001; pmid: 25459879
58. + T cells. Science 350, 328-334 (2015). doi: 10.1126/science.aad0395; pmid: 26405229
59. J. E. Vince et al., Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36, 215-227 (2012). doi: 10.1016/j.immuni.2012.01.012; pmid: 22365665
60. T. B. Kang, S. H. Yang, B. Toth, A. Kovalenko, D. Wallach, Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38, 27-40 (2013). doi: 10.1016/j.immuni.2012.09.015; pmid: 23260196
61. X. Wang et al., RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat. Immunol. 15, 1126-1133 (2014). doi: 10.1038/ni.3015; pmid: 25326752
62. K. Moriwaki et al., The necroptosis adaptor RIPK3 promotes injury-induced cytokine expression and tissue repair. Immunity 41, 567-578 (2014). doi: 10.1016/j.immuni.2014.09.016; pmid: 25367573
63. E. Kuranaga, M. Miura, Nonapoptotic functions of caspases: Caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol. 17, 135-144 (2007). doi: 10.1016/j.tcb.2007.01.001; pmid: 17275304
64. L. Gurcel, L Abrami, S. Girardin, J. Tschopp, F. G. van der Goot, Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126, 1135-1145 (2006). doi: 10.1016/j.cell.2006.07.033; pmid: 16990137
65. B. F. Py et al., Caspase-11 controls interleukin-1β release through degradation of TRPC1. Cell Rep. 6, 1122-1128 (2014). doi: 10.1016/j.celrep.2014.02.015; pmid: 24630989
66. D. Wallach, T. B. Kang, S. H. Yang, A. Kovalenko, The in vivo significance of necroptosis: Lessons from exploration of caspase-8 function. Cytokine Growth Factor Rev. 25, 157-165 (2014). doi: 10.1016/j.cytogfr.2013.12.001; pmid: 24411566
67. Y. Dondelinger et al., MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7, 971-981 (2014). doi: 10.1016/j.celrep.2014.04.026; pmid: 24813885
68. W. Chen 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. 288, 16247-16261 (2013). doi: 10.1074/jbc.M112.435545; pmid: 23612963
69. S. Yoon, K. Bogdanov, A. Kovalenko, D. Wallach, Necroptosis is preceded by nuclear translocation of the signaling proteins that induce it. Cell Death Differ. 23, 253-260 (2016). doi: 10.1038/cdd.2015.92; pmid: 26184911