Cell type-dependent ROS and mitophagy response leads to apoptosis or necroptosis in neuroblastoma

Oncogene

Volumn 35, Issue 29, 2016, Pages 3839-3853

  Radogna, F ^a   Cerella, C ^a   Gaigneaux, A ^a   Christov, C ^b   Dicato, M ^a   Diederich, M ^c  

^a LABORATOIRE DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE DU CANCER   (Luxembourg)

^b UNIVERSITÉ DE LORRAINE   (France)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; CARDIAC GLYCOSIDE; CASPASE 3; CASPASE 7; CATHEPSIN B; CATHEPSIN L; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; REACTIVE OXYGEN METABOLITE; RNA; UNBS 1450; UNCLASSIFIED DRUG; CARDENOLIDE;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL STIMULATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; LYSOSOME MEMBRANE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; NECROPTOSIS; NEUROBLASTOMA; NEUROBLASTOMA CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SCANNING ELECTRON MICROSCOPY; SENSITIZATION; CELL SURVIVAL; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; HUMAN; LYSOSOME; METABOLISM; NECROSIS; PROCEDURES; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; U-937 CELL LINE; ULTRASTRUCTURE; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CARDENOLIDES; CATHEPSIN B; CATHEPSIN L; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE ONTOLOGY; HUMANS; LYSOSOMES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MITOCHONDRIAL DEGRADATION; NECROSIS; NEUROBLASTOMA; REACTIVE OXYGEN SPECIES; U937 CELLS;

EID: 84949293247     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.455     Document Type: Article

References (51)

1. Cerella C, Dicato M, Diederich M. Assembling the puzzle of anti-cancer mechanisms triggered by cardiac glycosides. Mitochondrion 2013; 13: 225-234.
2. Slingerland M, Cerella C, Guchelaar HJ, Diederich M, Gelderblom H. Cardiac glycosides in cancer therapy: from preclinical investigations towards clinical trials. Invest New Drugs 2013; 31: 1087-1094.
3. Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med 2012; 4: 143-199.
4. Juncker T, Schumacher M, Dicato M, Diederich M. UNBS1450 from Calotropis procera as a regulator of signaling pathways involved in proliferation and cell death. Biochem Pharmacol 2009; 78: 1-10.
5. Cerella C, Muller F, Gaigneaux A, Radogna F, Viry E, Chateauvieux S et al. Early downregulation of Mcl-1 regulates apoptosis triggered by cardiac glycoside UNBS1450. Cell Death Dis 2015; 6: e1782.
6. Juncker T, Cerella C, Teiten MH, Morceau F, Schumacher M, Ghelfi J et al. UNBS1450, a steroid cardiac glycoside inducing apoptotic cell death in human leukemia cells. Biochem Pharmacol 2011; 81: 13-23.
7. Muller F, Cerella C, Radogna F, Dicato M, Diederich M. Effects of natural products on Mcl-1 expression and function. Curr Med Chem 2015; 22: 3447-3461.
8. Li Q, Pogwizd SM, Prabhu SD, Zhou L. Inhibiting Na+/K+ ATPase can impair mitochondrial energetics and induce abnormal Ca2+ cycling and automaticity in guinea pig cardiomyocytes. PloS One 2014; 9: e93928.
9. Newman RA, Yang P, Hittelman WN, Lu T, Ho DH, Ni D et al. Oleandrin-mediated oxidative stress in human melanoma cells. J Exp Ther Oncol 2006; 5: 167-181.
10. Xie CM, Chan WY, Yu S, Zhao J, Cheng CH. Bufalin induces autophagy-mediated cell death in human colon cancer cells through reactive oxygen species generation and JNK activation. Free Radic Biol Med 2011; 51: 1365-1375.
11. Hu F, Han J, Zhai B, Ming X, Zhuang L, Liu Y et al. Blocking autophagy enhances the apoptosis effect of bufalin on human hepatocellular carcinoma cells through endoplasmic reticulum stress and JNK activation. Apoptosis 2014; 19: 210-223.
12. Lang F, Qin Z, Li F, Zhang H, Fang Z, Hao E. Apoptotic cell death induced by resveratrol is partially mediated by the autophagy pathway in human ovarian cancer cells. PloS One 2015; 10: e0129196.
13. Zhang T, Li Y, Park KA, Byun HS, Won M, Jeon J et al. Cucurbitacin induces autophagy through mitochondrial ROS production which counteracts to limit caspase-dependent apoptosis. Autophagy 2012; 8: 559-576.
14. Wang Y, Zhan Y, Xu R, Shao R, Jiang J, Wang Z. Src mediates extracellular signalregulated kinase 1/2 activation and autophagic cell death induced by cardiac glycosides in human non-small cell lung cancer cell lines. Mol Carcinog 2015; 54: E26-E34.
15. Klose J, Stankov MV, Kleine M, Ramackers W, Panayotova-Dimitrova D, Jager MD et al. Inhibition of autophagic flux by salinomycin results in anti-cancer effect in hepatocellular carcinoma cells. PloS One 2014; 9: e95970.
16. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008; 15: 171-182.
17. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26: 1749-1760.
18. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008; 30: 214-226.
19. Cheng P, Ni Z, Dai X, Wang B, Ding W, Rae Smith A et al. The novel BH-3 mimetic apogossypolone induces Beclin-1-and ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell Death Dis 2013; 4: e489.
20. Radogna F, Dicato M, Diederich M. Cancer-type-specific crosstalk between autophagy, necroptosis and apoptosis as a pharmacological target. Biochem Pharmacol 2015; 94: 1-11.
21. Radogna F, Albertini MC, De Nicola M, Diederich M, Bejarano I, Ghibelli L. Melatonin promotes Bax sequestration to mitochondria reducing cell susceptibility to apoptosis via the lipoxygenase metabolite 5-hydroxyeicosatetraenoic acid. Mitochondrion 2015; 21: 113-121.
22. Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 2015; 22: 377-388.
23. Sui X, Chen R, Wang Z, Huang Z, Kong N, Zhang M et al. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis 2013; 4: e838.
24. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8: 741-752.
25. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132: 27-42.
26. Cerella C, Teiten MH, Radogna F, Dicato M, Diederich M. From nature to bedside: pro-survival and cell death mechanisms as therapeutic targets in cancer treatment. Biotechnol Adv 2014; 32: 1111-1122.
27. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet 2007; 369: 2106-2120.
28. Mora J, Cheung NK, Juan G, Illei P, Cheung I, Akram M et al. Neuroblastic and Schwannian stromal cells of neuroblastoma are derived from a tumoral progenitor cell. Cancer Res 2001; 61: 6892-6898.
29. Jasty R, van Golen C, Lin HJ, Solomon G, Heidelberger K, Polverini P et al. Bcl-2 and M-Myc coexpression increases IGF-IR and features of malignant growth in neuroblastoma cell lines. Neoplasia 2001; 3: 304-313.
30. Mijatovic T, Op De Beeck A, Van Quaquebeke E, Dewelle J, Darro F, de Launoit Y et al. The cardenolide UNBS1450 is able to deactivate nuclear factor kappaBmediated cytoprotective effects in human non-small cell lung cancer cells. Mol Cancer Ther 2006; 5: 391-399.
31. Cerella C, Radogna F, Dicato M, Diederich M. Natural compounds as regulators of the cancer cell metabolism. Int J Cell Biol 2013; 2013: 639401.
32. Pavlides S, Vera I, Gandara R, Sneddon S, Pestell RG, Mercier I et al. Warburg meets autophagy: cancer-associated fibroblasts accelerate tumor growth and metastasis via oxidative stress, mitophagy, and aerobic glycolysis. Antioxid Redox Signal 2012; 16: 1264-1284.
33. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 2011; 286: 7468-7478.
34. Salcher S, Hagenbuchner J, Geiger K, Seiter MA, Rainer J, Kofler R et al. C10ORF10/DEPP, a transcriptional target of FOXO3, regulates ROS-sensitivity in human neuroblastoma. Mol Cancer 2014; 13: 224.
35. Cerella C, Gaigneaux A, Dicato M, Diederich M. Antagonistic role of natural compounds in mTOR-mediated metabolic reprogramming. Cancer Lett 2015; 356: 251-262.
36. Boya P, Kroemer G. Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27: 6434-6451.
37. Li L, Chen Y, Gibson SB. Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cell Signal 2013; 25: 50-65.
38. Ostenfeld MS, Hoyer-Hansen M, Bastholm L, Fehrenbacher N, Olsen OD, Groth-Pedersen L et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 2008; 4: 487-499.
39. Vucicevic L, Misirkic-Marjanovic M, Paunovic V, Kravic-Stevovic T, Martinovic T, Ciric D et al. Autophagy inhibition uncovers the neurotoxic action of the antipsychotic drug olanzapine. Autophagy 2014; 10: 2362-2378.
40. Castino R, Fiorentino I, Cagnin M, Giovia A, Isidoro C. Chelation of lysosomal iron protects dopaminergic SH-SY5Y neuroblastoma cells from hydrogen peroxide toxicity by precluding autophagy and Akt dephosphorylation. Toxicol Sci 2011; 123: 523-541.
41. Goldsmith KC, Hogarty MD. Targeting programmed cell death pathways with experimental therapeutics: opportunities in high-risk neuroblastoma. Cancer Lett 2005; 228: 133-141.
42. Abhari BA, Cristofanon S, Kappler R, von Schweinitz D, Humphreys R, Fulda S. RIP1 is required for IAP inhibitor-mediated sensitization for TRAIL-induced apoptosis via a RIP1/FADD/caspase-8 cell death complex. Oncogene 2013; 32: 3263-3273.
43. Hashem SI, Perry CN, Bauer M, Han S, Clegg SD, Ouyang K et al. Brief report: oxidative stress mediates cardiomyocyte apoptosis in a human model of Danon disease and heart failure. Stem Cells 2015; 33: 2343-2350.
44. Parganlija D, Klinkenberg M, Dominguez-Bautista J, Hetzel M, Gispert S, Chimi MA et al. Loss of PINK1 impairs stress-induced autophagy and cell survival. PloS One 2014; 9: e95288.
45. Lefranc F, Mijatovic T, Kondo Y, Sauvage S, Roland I, Debeir O et al. Targeting the alpha 1 subunit of the sodium pump to combat glioblastoma cells. Neurosurgery 2008; 62: 211-221; discussion 221-212.
46. Van Quaquebeke E, Simon G, Andre A, Dewelle J, El Yazidi M, Bruyneel F et al. Identification of a novel cardenolide (2"-oxovoruscharin) from Calotropis procera and the hemisynthesis of novel derivatives displaying potent in vitro antitumor activities and high in vivo tolerance: structure-activity relationship analyses. J Med Chem 2005; 48: 849-856.
47. Cerella C, Scherer C, Cristofanon S, Henry E, Anwar A, Busch C et al. Cell cycle arrest in early mitosis and induction of caspase-dependent apoptosis in U937 cells by diallyltetrasulfide (Al2S4). Apoptosis 2009; 14: 641-654.
48. Radogna F, Sestili P, Martinelli C, Paolillo M, Paternoster L, Albertini MC et al. Lipoxygenase-mediated pro-radical effect of melatonin via stimulation of arachidonic acid metabolism. Toxicol Appl Pharmacol 2009; 238: 170-177.
49. Olenych SG, Claxton NS, Ottenberg GK, Davidson MW. The fluorescent protein color palette. Curr Protoc Cell Biol 2007; Chapter 21: Unit 21 25.
50. Schnekenburger M, Grandjenette C, Ghelfi J, Karius T, Foliguet B, Dicato M et al. Sustained exposure to the DNA demethylating agent, 2'-deoxy-5-azacytidine, leads to apoptotic cell death in chronic myeloid leukemia by promoting differentiation, senescence, and autophagy. Biochem Pharmacol 2011; 81: 364-378.
51. Radogna F, Paternoster L, De Nicola M, Cerella C, Ammendola S, Bedini A et al. Rapid and transient stimulation of intracellular reactive oxygen species by melatonin in normal and tumor leukocytes. Toxicol Appl Pharmacol 2009; 239: 37-45.