NF-κB-Independent Role of IKKα/IKKβ in Preventing RIPK1 Kinase-Dependent Apoptotic and Necroptotic Cell Death during TNF Signaling

Molecular Cell

Volumn 60, Issue 1, 2015, Pages 63-76

  Dondelinger, Yves ^a,b   Jouan Lanhouet, Sandrine ^a,b   Divert, Tatyana ^a,b   Theatre, Emilie ^c   Bertin, John ^d   Gough, Peter J ^d   Giansanti, Piero ^e,f   Heck, Albert J R ^e,f   Dejardin, Emmanuel ^c   Vandenabeele, Peter ^a,b   Bertrand, Mathieu J M ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d GLAXOSMITHKLINE   (United States)

^e UTRECHT UNIVERSITY   (Netherlands)

^f NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CASPASE 3; CASPASE 8; I KAPPA B ALPHA; I KAPPA B BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LACTATE DEHYDROGENASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; CASP8 PROTEIN, MOUSE; FADD PROTEIN, MOUSE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; I KAPPA B KINASE; RIPK1 PROTEIN, MOUSE; TNFRSF1A PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL DEATH; CELL FUNCTION; CELL PROTECTION; CELL SURVIVAL; CLINICAL EVALUATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EVIDENCE BASED PRACTICE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; NECROPTOSIS; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; CELL LINE; CYTOLOGY; FIBROBLAST; METABOLISM; MOUSE; PHOSPHORYLATION;

ANIMALS; CASPASE 8; CELL DEATH; CELL LINE; EMBRYO, MAMMALIAN; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FIBROBLASTS; I-KAPPA B KINASE; MICE; NF-KAPPA B; PHOSPHORYLATION; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947923888     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.07.032     Document Type: Article

References (57)

1. Baldwin A.S. Regulation of cell death and autophagy by IKK and NF-κB: critical mechanisms in immune function and cancer. Immunol. Rev. 2012, 246:327-345.
2. Baud V., Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 2009, 8:33-40.
3. Beg A.A., Sha W.C., Bronson R.T., Ghosh S., Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 1995, 376:167-170.
4. Berger S.B., Kasparcova V., Hoffman S., Swift B., Dare L., Schaeffer M., Capriotti C., Cook M., Finger J., Hughes-Earle A., et al. Cutting Edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J. Immunol. 2014, 192:5476-5480.
5. Bertrand M.J., Milutinovic S., Dickson K.M., Ho W.C., Boudreault A., Durkin J., Gillard J.W., Jaquith J.B., Morris S.J., Barker P.A. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 2008, 30:689-700.
6. 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.
7. Conte M.I., Pescatore A., Paciolla M., Esposito E., Miano M.G., Lioi M.B., McAleer M.A., Giardino G., Pignata C., Irvine A.D., et al. Insight into IKBKG/NEMO locus: report of new mutations and complex genomic rearrangements leading to incontinentia pigmenti disease. Hum. Mutat. 2014, 35:165-177.
8. Decker K., Keppler D. Galactosamine hepatitis: key role of the nucleotide deficiency period in the pathogenesis of cell injury and cell death. Rev. Physiol. Biochem. Pharmacol. 1974, 71:77-106.
9. 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.
10. Dejardin E., Droin N.M., Delhase M., Haas E., Cao Y., Makris C., Li Z.W., Karin M., Ware C.F., Green D.R. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 2002, 17:525-535.
11. Dondelinger Y., Aguileta M.A., Goossens V., Dubuisson C., Grootjans S., Dejardin E., Vandenabeele P., Bertrand M.J. RIPK3 contributes to TNFR1-mediated RIPK1 kinase-dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition. Cell Death Differ. 2013, 20:1381-1392.
12. Ea C.K., Deng L., Xia Z.P., Pineda G., Chen Z.J. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 2006, 22:245-257.
13. Gentle I.E., Wong W.W., Evans J.M., Bankovacki A., Cook W.D., Khan N.R., Nachbur U., Rickard J., Anderton H., Moulin M., et al. In TNF-stimulated cells, RIPK1 promotes cell survival by stabilizing TRAF2 and cIAP1, which limits induction of non-canonical NF-kappaB and activation of caspase-8. J. Biol. Chem. 2011, 286:13282-13291.
14. 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 2011, 471:591-596.
15. 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 2009, 36:831-844.
16. Hayden M.S., Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012, 26:203-234.
17. Hayden M.S., Ghosh S. Regulation of NF-κB by TNF family cytokines. Semin. Immunol. 2014, 26:253-266.
18. 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 2009, 137:1100-1111.
19. Hinz M., Scheidereit C. The IκB kinase complex in NF-κB regulation and beyond. EMBO Rep. 2014, 15:46-61.
20. Hu Y., Baud V., Delhase M., Zhang P., Deerinck T., Ellisman M., Johnson R., Karin M. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 1999, 284:316-320.
21. Irmler M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., Bodmer J.L., Schröter M., Burns K., Mattmann C., et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997, 388:190-195.
22. Kanayama A., Seth R.B., Sun L., Ea C.K., Hong M., Shaito A., Chiu Y.H., Deng L., Chen Z.J. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 2004, 15:535-548.
23. Karin M., Lin A. NF-kappaB at the crossroads of life and death. Nat. Immunol. 2002, 3:221-227.
24. Kreuz S., Siegmund D., Scheurich P., Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 2001, 21:3964-3973.
25. Kumari S., Redouane Y., Lopez-Mosqueda J., Shiraishi R., Romanowska M., Lutzmayer S., Kuiper J., Martinez C., Dikic I., Pasparakis M., Ikeda F. Sharpin prevents skin inflammation by inhibiting TNFR1-induced keratinocyte apoptosis. eLife, 2014, 3:e03422.
26. 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. 2009, 16:1279-1288.
27. Li Q., Van Antwerp D., Mercurio F., Lee K.F., Verma I.M. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 1999, 284:321-325.
28. Li Q., Estepa G., Memet S., Israel A., Verma I.M. Complete lack of NF-kappaB activity in IKK1 and IKK2 double-deficient mice: additional defect in neurulation. Genes Dev. 2000, 14:1729-1733.
29. Li H., Kobayashi M., Blonska M., You Y., Lin X. Ubiquitination of RIP is required for tumor necrosis factor alpha-induced NF-kappaB activation. J. Biol. Chem. 2006, 281:13636-13643.
30. Liu Z.G., Hsu H., Goeddel D.V., Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 1996, 87:565-576.
31. Liu F., Xia Y., Parker A.S., Verma I.M. IKK biology. Immunol. Rev. 2012, 246:239-253.
32. Luedde T., Beraza N., Kotsikoris V., van Loo G., Nenci A., De Vos R., Roskams T., Trautwein C., Pasparakis M. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007, 11:119-132.
33. Mahoney D.J., Cheung H.H., Mrad R.L., Plenchette S., Simard C., Enwere E., Arora V., Mak T.W., Lacasse E.C., Waring J., Korneluk R.G. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc. Natl. Acad. Sci. USA 2008, 105:11778-11783.
34. McQuade T., Cho Y., Chan F.K. Positive and negative phosphorylation regulates RIP1- and RIP3-induced programmed necrosis. Biochem. J. 2013, 456:409-415.
35. Micheau O., Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114:181-190.
36. Micheau O., Lens S., Gaide O., Alevizopoulos K., Tschopp J. NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 2001, 21:5299-5305.
37. 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. 2012, 31:1679-1691.
38. O'Donnell M.A., Ting A.T. RIP1 comes back to life as a cell death regulator in TNFR1 signaling. FEBS J. 2011, 278:877-887.
39. O'Donnell M.A., Legarda-Addison D., Skountzos P., Yeh W.C., Ting A.T. Ubiquitination of RIP1 regulates an NF-kappaB-independent cell-death switch in TNF signaling. Curr. Biol. 2007, 17:418-424.
40. O'Donnell M.A., Hase H., Legarda D., Ting A.T. NEMO inhibits programmed necrosis in an NFκB-independent manner by restraining RIP1. PLoS ONE 2012, 7:e41238.
41. Panayotova-Dimitrova D., Feoktistova M., Ploesser M., Kellert B., Hupe M., Horn S., Makarov R., Jensen F., Porubsky S., Schmieder A., et al. cFLIP regulates skin homeostasis and protects against TNF-induced keratinocyte apoptosis. Cell Rep. 2013, 5:397-408.
42. Pasparakis M., Vandenabeele P. Necroptosis and its role in inflammation. Nature 2015, 517:311-320.
43. Petersen S.L., Wang L., Yalcin-Chin A., Li L., Peyton M., Minna J., Harran P., Wang X. Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 2007, 12:445-456.
44. Podolin P.L., Callahan J.F., Bolognese B.J., Li Y.H., Carlson K., Davis T.G., Mellor G.W., Evans C., Roshak A.K. Attenuation of murine collagen-induced arthritis by a novel, potent, selective small molecule inhibitor of IkappaB Kinase 2, TPCA-1 (2-[(aminocarbonyl)amino]-5-(4-fluorophenyl)-3-thiophenecarboxamide), occurs via reduction of proinflammatory cytokines and antigen-induced T cell Proliferation. J. Pharmacol. Exp. Ther. 2005, 312:373-381.
45. Rickard J.A., Anderton H., Etemadi N., Nachbur U., Darding M., Peltzer N., Lalaoui N., Lawlor K.E., Vanyai H., Hall C., et al. TNFR1-dependent cell death drives inflammation in Sharpin-deficient mice. eLife 2014, 3:e03464.
46. Rudolph D., Yeh W.C., Wakeham A., Rudolph B., Nallainathan D., Potter J., Elia A.J., Mak T.W. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 2000, 14:854-862.
47. 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.
48. Takeda K., Takeuchi O., Tsujimura T., Itami S., Adachi O., Kawai T., Sanjo H., Yoshikawa K., Terada N., Akira S. Limb and skin abnormalities in mice lacking IKKalpha. Science 1999, 284:313-316.
49. Van Antwerp D.J., Martin S.J., Kafri T., Green D.R., Verma I.M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 1996, 274:787-789.
50. Vanlangenakker N., Vanden Berghe T., Bogaert P., Laukens B., Zobel K., Deshayes K., Vucic D., Fulda S., Vandenabeele P., Bertrand M.J. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011, 18:656-665.
51. Walczak H. TNF and ubiquitin at the crossroads of gene activation, cell death, inflammation, and cancer. Immunol. Rev. 2011, 244:9-28.
52. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998, 281:1680-1683.
53. Wang L., Du F., Wang X. TNF-alpha induces two distinct caspase-8 activation pathways. Cell 2008, 133:693-703.
54. Wilson N.S., Dixit V., Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat. Immunol. 2009, 10:348-355.
55. Wu C.J., Conze D.B., Li T., Srinivasula S.M., Ashwell J.D. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-kappaB activation [corrected]. Nat. Cell Biol. 2006, 8:398-406.
56. 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.
57. 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.