Reactive oxygen species regulate Smac mimetic/TNFα-induced necroptotic signaling and cell death

Oncogene

Volumn 34, Issue 47, 2015, Pages 5796-5806

  Schenk, B ^a   Fulda, S ^a,b  

^a GOETHE UNIVERSITY   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; BUTYLATED HYDROXYANISOLE; DEUBIQUITINASE; DYNAMIN; DYNAMIN RELATED PROTEIN 1; MIXED LINEAGE KINASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 5; PROTEIN KINASE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; RECEPTOR INTERACTING PROTEIN KINASE 1; RECEPTOR INTERACTING PROTEIN KINASE 3; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AGFG1 PROTEIN, HUMAN; BV6 PEPTIDE; FADD PROTEIN, HUMAN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MLKL PROTEIN, HUMAN; NUCLEOPORIN; OLIGOPEPTIDE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE SILENCING; JURKAT CELL LINE; NECROPTOSIS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; DEFICIENCY; DRUG EFFECTS; HUMAN; METABOLISM; PHOSPHORYLATION;

CELL DEATH; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HUMANS; JURKAT CELLS; NUCLEAR PORE COMPLEX PROTEINS; OLIGOPEPTIDES; PHOSPHORYLATION; PROTEIN KINASES; REACTIVE OXYGEN SPECIES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947869935     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.35     Document Type: Article

References (53)

1. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat Rev Mol Cell Biol 2014; 15: 135-147.
2. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 2014; 16: 55-65.
3. Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell 2014; 54: 133-146.
4. Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A, Bruggeman I et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep 2014; 7: 971-981.
5. 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.
6. Fulda S, Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat Rev Drug Discov 2012; 11: 109-124.
7. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008; 30: 689-700.
8. Wright A, Reiley WW, Chang M, Jin W, Lee AJ, Zhang M et al. Regulation of early wave of germ cell apoptosis and spermatogenesis by deubiquitinating enzyme CYLD. Dev Cell 2007; 13: 705-716.
9. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 2008; 135: 1311-1323.
10. Han D, Ybanez MD, Ahmadi S, Yeh K, Kaplowitz N. Redox regulation of tumor necrosis factor signaling. Antioxid Redox Signal 2009; 11: 2245-2263.
11. Morgan MJ, Liu ZG. Reactive oxygen species in TNFalpha-induced signaling and cell death. Molecules Cells 2010; 30: 1-12.
12. Vanden Berghe T, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N et al. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ 2010; 17: 922-930.
13. Shulga N, Pastorino JG. GRIM-19-mediated translocation of STAT3 to mitochondria is necessary for TNF-induced necroptosis. J Cell Sci 2012; 125: 2995-3003.
14. Shindo R, Kakehashi H, Okumura K, Kumagai Y, Nakano H. Critical contribution of oxidative stress to TNFalpha-induced necroptosis downstream of RIPK1 activation. Biochem Biophys Res Commun 2015; 436: 212-216.
15. Kim YS, Morgan MJ, Choksi S, Liu ZG. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol Cell 2007; 26: 675-687.
16. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K et al. 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.
17. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009; 325: 332-336.
18. Tait SW, Oberst A, Quarato G, Milasta S, Haller M, Wang R et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep 2013; 5: 878-885.
19. Laukens B, Jennewein C, Schenk B, Vanlangenakker N, Schier A, Cristofanon S et al. Smac mimetic bypasses apoptosis resistance in FADD- or caspase-8-deficient cells by priming for tumor necrosis factor alpha-induced necroptosis. Neoplasia 2011; 13: 971-979.
20. Sun L, Wang H, Wang Z, He S, Chen S, Liao D et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012; 148: 213-227.
21. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 2008; 14: 193-204.
22. Dixon SJ, Stockwell BR. The role of iron and reactive oxygen species in cell death. Nat Chem Biol 2014; 10: 9-17.
23. Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010; 48: 749-762.
24. Vernon PJ, Tang D. Eat-me: autophagy, phagocytosis, and reactive oxygen species signaling. Antioxid Redox Signal 2013; 18: 677-691.
25. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS et al. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 2004; 279: 10822-10828.
26. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009; 137: 1112-1123.
27. Shulga N, Pastorino JG. Mitoneet mediates TNFalpha-induced necroptosis promoted by exposure to fructose and ethanol. J Cell Sci 2014; 127: 896-907.
28. Irrinki KM, Mallilankaraman K, Thapa RJ, Chandramoorthy HC, Smith FJ, Jog NR et al. Requirement of FADD, NEMO, and BAX/BAK for aberrant mitochondrial function in tumor necrosis factor alpha-induced necrosis. Mol Cell Biol 2011; 31: 3745-3758.
29. Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013; 153: 521-534.
30. Ye YC, Wang HJ, Yu L, Tashiro SI, Onodera S, Ikejima T. RIP1-mediated mitochondrial dysfunction and ROS production contributed to tumor necrosis factor alpha-induced L929 cell necroptosis and autophagy. Int Immunopharmacol 2012; 14: 674-682.
31. Davis CW, Hawkins BJ, Ramasamy S, Irrinki KM, Cameron BA, Islam K et al. Nitration of the mitochondrial complex I subunit NDUFB8 elicits RIP1- and RIP3-mediated necrosis. Free Radic Biol Med 2010; 48: 306-317.
32. Huang CY, Kuo WT, Huang YC, Lee TC, Yu LC. Resistance to hypoxia-induced necroptosis is conferred by glycolytic pyruvate scavenging of mitochondrial superoxide in colorectal cancer cells. Cell Death Dis 2013; 4: e622.
33. Coupienne I, Fettweis G, Rubio N, Agostinis P, Piette J. 5-ALA-PDT induces RIP3-dependent necrosis in glioblastoma. Photochem Photobiol Sci 2011; 10: 1868-1878.
34. Song KJ, Jang YS, Lee YA, Kim KA, Lee SK, Shin MH. Reactive oxygen species-dependent necroptosis in Jurkat T cells induced by pathogenic free-living Naegleria fowleri. Parasite Immunol 2011; 33: 390-400.
35. Chen TY, Chi KH, Wang JS, Chien CL, Lin WW. Reactive oxygen species are involved in FasL-induced caspase-independent cell death and inflammatory responses. Free Radic Biol Med 2009; 46: 643-655.
36. He S, Wang L, Miao L, Wang T, Du F, Zhao L et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009; 137: 1100-1111.
37. Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov 2013; 12: 931-947.
38. Held JM, Gibson BW. Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol Cell Proteom 2012; 11: 013037.
39. Vanlangenakker N, Bertrand MJ, Bogaert P, Vandenabeele P, Vanden Berghe T. TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members. Cell Death Dis 2011; 2: e230.
40. Kulathu Y, Garcia FJ, Mevissen TE, Busch M, Arnaudo N, Carroll KS et al. Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nat Commun 2013; 4: 1569.
41. Arslan SC, Scheidereit C. The prevalence of TNFalpha-induced necrosis over apoptosis is determined by TAK1-RIP1 interplay. PLoS One 2011; 6: e26069.
42. Kikuchi M, Kuroki S, Kayama M, Sakaguchi S, Lee KK, Yonehara S. Protease activity of procaspase-8 is essential for cell survival by inhibiting both apoptotic and nonapoptotic cell death dependent on receptor-interacting protein kinase 1 (RIP1) and RIP3. J Biol Chem 2012; 287: 41165-41173.
43. 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.
44. Luedde M, Lutz M, Carter N, Sosna J, Jacoby C, Vucur M et al. RIP3, a kinase promoting necroptotic cell death, mediates adverse remodelling after myocardial infarction. Cardiovasc Res 2014; 103: 206-216.
45. Moquin DM, McQuade T, Chan FK. CYLD deubiquitinates RIP1 in the TNFalpha-induced necrosome to facilitate kinase activation and programmed necrosis. PLoS One 2013; 8: e76841.
46. Zhao J, Jitkaew S, Cai Z, Choksi S, Li Q, Luo J et al. 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.
47. Gomes A, Fernandes E, Lima JL. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 2005; 65: 45-80.
48. Remijsen Q, Goossens V, Grootjans S, Van den Haute C, Vanlangenakker N, Dondelinger Y et al. Depletion of RIPK3 or MLKL blocks TNF-driven necroptosis and switches towards a delayed RIPK1 kinase-dependent apoptosis. Cell Death Dis 2014; 5: e1004.
49. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alvarez-Diaz S et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 2013; 39: 443-453.
50. Juo P, Woo MS, Kuo CJ, Signorelli P, Biemann HP, Hannun YA et al. FADD is required for multiple signaling events downstream of the receptor Fas. Cell Growth Differ 1999; 10: 797-804.
51. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007; 131: 669-681.
52. Gonzalez P, Mader I, Tchoghandjian A, Enzenmuller S, Cristofanon S, Basit F et al. Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ 2012; 19: 1337-1346.
53. Fulda S, Strauss G, Meyer E, Debatin KM. Functional CD95 ligand and CD95 death-inducing signaling complex in activation-induced cell death and doxorubicin-induced apoptosis in leukemic T cells. Blood 2000; 95: 301-308.