Neoalbaconol induces cell death through necroptosis by regulating RIPK-dependent autocrine TNFα and ROS production

Oncotarget

Volumn 6, Issue 4, 2015, Pages 1995-2008

  Yu, Xinfang ^a,b   Deng, Qipan ^a,b   Li, Wei ^a,b   Xiao, Lanbo ^a,b   Luo, Xiangjian ^a,b   Liu, Xiaolan ^a,b   Yang, Lifang ^a,b   Peng, Songling ^a,b   Ding, Zhihui ^c   Feng, Tao ^c   Zhou, Jian ^e   Fan, Jia ^e   Bode, Ann M ^d   Dong, Zigang ^d   Liu, Jikai ^c   Cao, Ya ^a,b  

^a Central South University   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c KUNMING INSTITUTE OF BOTANY   (China)

^d UNIVERSITY OF MINNESOTA   (United States)

^e ZHONGSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

Author keywords

Necoalbaconol; Necroptosis; NF B Signaling pathway; RIPK; ROS; TNF

Indexed keywords

CELLULAR INHIBITOR OF APOPTOSIS PROTEIN 1; CELLULAR INHIBITOR OF APOPTOSIS PROTEIN 2; FUNGAL EXTRACT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; NEOALBACONOL; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; RECEPTOR INTERACTING PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BIRC3 PROTEIN, HUMAN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, HUMAN; RIPK3 PROTEIN, HUMAN; SESQUITERPENE; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NECROPTOSIS; NONHUMAN; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION; BASIDIOMYCETES; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; NECROSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; BASIDIOMYCOTA; BLOTTING, WESTERN; CELL LINE, TUMOR; GENE EXPRESSION; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; NECROSIS; NF-KAPPA B; REACTIVE OXYGEN SPECIES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SESQUITERPENES; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84923062594     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3038     Document Type: Article

References (47)

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. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ. 2012; 19: 75-86.
3. Yu X, Deng Q, Bode AM, Dong Z, Cao Y. The role of necroptosis, an alternative form of cell death, in cancer therapy. Expert Rev Anticancer Ther. 2013; 13: 883-893.
4. Tenev T, Bianchi K, Darding M, Broemer M, Langlais C, Wallberg F, Zachariou A, Lopez J, MacFarlane M, Cain K, Meier P. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell. 2011; 43: 432-448.
5. Steinhart L, Belz K, Fulda S. Smac mimetic and demethylating agents synergistically trigger cell death in acute myeloid leukemia cells and overcome apoptosis resistance by inducing necroptosis. Cell Death Dis. 2013; 4: e802.
6. Laukens B, Jennewein C, Schenk B, Vanlangenakker N, Schier A, Cristofanon S, Zobel K, Deshayes K, Vucic D, Jeremias I, Bertrand MJ, Vandenabeele P, Fulda S. 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.
7. Han W, Li L, Qiu S, Lu Q, Pan Q, Gu Y, Luo J, Hu X. Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther. 2007; 6: 1641-1649.
8. Christofferson DE, Li Y, Hitomi J, Zhou W, Upperman C, Zhu H, Gerber SA, Gygi S, Yuan J. A novel role for RIP1 kinase in mediating TNFalpha production. Cell Death Dis. 2012; 3: e320.
9. Wu YT, Tan HL, Huang Q, Sun XJ, Zhu X, Shen HM. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFalpha mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ. 2011; 18: 26-37.
10. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010; 11: 700-714.
11. Christofferson DE, Yuan J. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol. 2010; 22: 263-268.
12. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell. 2008; 30: 689-700.
13. Feoktistova M, Geserick P, Kellert B, Dimitrova DP, Langlais C, Hupe M, Cain K, MacFarlane M, Hacker G, Leverkus M. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell. 2011; 43: 449-463.
14. 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.
15. 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.
16. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004; 25: 280-288.
17. Hayden MS, Ghosh S. NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012; 26: 203-234.
18. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J, Shiba T, Yang X, Yeh WC, Mak TW, Korneluk RG, Cheng G. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol. 2008; 9: 1371-1378.
19. Qing G, Qu Z, Xiao G. Stabilization of basally translated NF-kappaB-inducing kinase (NIK) protein functions as a molecular switch of processing of NF-kappaB2 p100. J Biol Chem. 2005; 280: 40578-40582.
20. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJ, Flygare JA, Fairbrother WJ, Deshayes K, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell. 2007; 131: 669-681.
21. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, Brink R, Leverkus M, Tergaonkar V, et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell. 2007; 131: 682-693.
22. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, Vignali DA, Bergsagel PL, Karin M. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol. 2008; 9: 1364-1370.
23. Bianchi K, Meier P. A tangled web of ubiquitin chains: breaking news in TNF-R1 signaling. Mol Cell. 2009; 36: 736-742.
24. Deng Q, Yu X, Xiao L, Hu Z, Luo X, Tao Y, Yang L, Liu X, Chen H, Ding Z, Feng T, Tang Y, Weng X, et al. Neoalbaconol induces energy depletion and multiple cell death in cancer cells by targeting PDK1-PI3-K/Akt signaling pathway. Cell Death Dis. 2013; 4: e804.
25. Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, Wang FS, Wang X. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell. 2014; 54: 133-146.
26. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K, Vucic D, Fulda S, Vandenabeele P, Bertrand MJ. 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.
27. Wong WW, Vince JE, Lalaoui N, Lawlor KE, Chau D, Bankovacki A, Anderton H, Metcalf D, O'Reilly L, Jost PJ, Murphy JM, Alexander WS, Strasser A, et al. cIAPs and XIAP regulate myelopoiesis through cytokine production in an RIPK1-and RIPK3-dependent manner. Blood. 2014; 123: 2562-2572.
28. Grech AP, Amesbury M, Chan T, Gardam S, Basten A, Brink R. TRAF2 differentially regulates the canonical and noncanonical pathways of NF-kappaB activation in mature B cells. Immunity. 2004; 21: 629-642.
29. Gentle IE, Wong WW, Evans JM, Bankovacki A, Cook WD, Khan NR, Nachbur U, Rickard J, Anderton H, Moulin M, Lluis JM, Moujalled DM, Silke J, 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.
30. Vince JE, Pantaki D, Feltham R, Mace PD, Cordier SM, Schmukle AC, Davidson AJ, Callus BA, Wong WW, Gentle IE, Carter H, Lee EF, Walczak H, et al. TRAF2 must bind to cellular inhibitors of apoptosis for tumor necrosis factor (tnf) to efficiently activate nf-{kappa}b and to prevent tnf-induced apoptosis. J Biol Chem. 2009; 284: 35906-35915.
31. He W, Wang Q, Srinivasan B, Xu J, Padilla MT, Li Z, Wang X, Liu Y, Gou X, Shen HM, Xing C, Lin Y. A JNK-mediated autophagy pathway that triggers c-IAP degradation and necroptosis for anticancer chemotherapy. Oncogene. 2013.
32. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ. 2007; 14: 400-410.
33. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, Bonizzi G, Chen Y, Hu Y, Fong A, Sun SC, Karin M. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science. 2001; 293: 1495-1499.
34. Mahoney DJ, Cheung HH, Mrad RL, Plenchette S, Simard C, Enwere E, Arora V, Mak TW, Lacasse EC, Waring J, Korneluk RG. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc Natl Acad SciUSA. 2008; 105: 11778-11783.
35. Kasibhatla S, Brunner T, Genestier L, Echeverri F, Mahboubi A, Green DR. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol Cell. 1998; 1: 543-551.
36. Probst BL, Liu L, Ramesh V, Li L, Sun H, Minna JD, Wang L. Smac mimetics increase cancer cell response to chemotherapeutics in a TNF-alpha-dependent manner. Cell Death Differ. 2010; 17: 1645-1654.
37. Fortes GB, Alves LS, de Oliveira R, Dutra FF, Rodrigues D, Fernandez PL, Souto-Padron T, De Rosa MJ, Kelliher M, Golenbock D, Chan FK, Bozza MT. Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production. Blood. 2012; 119: 2368-2375.
38. Ye YC, Wang HJ, Yu L, Tashiro S, 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.
39. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science. 2009; 325: 332-336.
40. Festjens N, Kalai M, Smet J, Meeus A, Van Coster R, Saelens X, Vandenabeele P. Butylated hydroxyanisole is more than a reactive oxygen species scavenger. Cell Death Differ. 2006; 13: 166-169.
41. Kamarajan P, Bunek J, Lin Y, Nunez G, Kapila YL. Receptor-interacting protein shuttles between cell death and survival signaling pathways. Mol Biol Cell. 2010; 21: 481-488.
42. Petersen SL, 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.
43. Greer RM, Peyton M, Larsen JE, Girard L, Xie Y, Gazdar AF, Harran P, Wang L, Brekken RA, Wang X, Minna JD. SMAC mimetic (JP1201) sensitizes non-small cell lung cancers to multiple chemotherapy agents in an IAP-dependent but TNF-alpha-independent manner. Cancer Res. 2011; 71: 7640-7648.
44. 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.
45. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005; 1: 112-119.
46. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, Tran JH, Nedospasov SA, Liu ZG. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem. 2004; 279: 10822-10828.
47. Tait SW, Oberst A, Quarato G, Milasta S, Haller M, Wang R, Karvela M, Ichim G, Yatim N, Albert ML, Kidd G, Wakefield R, Frase S, et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep. 2013; 5: 878-885.