The roles of ROS and caspases in TRAIL-induced apoptosis and necroptosis in human pancreatic cancer cells

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Zhang, Min ^a,b   Harashima, Nanae ^b   Moritani, Tamami ^b   Huang, Weidong ^a   Harada, Mamoru ^b  

^a NINGXIA MEDICAL UNIVERSITY   (China)

^b SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CASPASE; CASPASE 2; CASPASE 9; LIPOCORTIN 5; PROPIDIUM IODIDE; PROTEIN KINASE; PROTEIN RIP1; PROTEIN RIP3; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TEMPOL; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; AMINE OXIDE; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; NECROSTATIN-1; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; SPIN LABEL;

APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; NECROPTOSIS; PANCREAS CANCER; REGULATORY MECHANISM; CELL DEATH; DRUG EFFECTS; GENETICS; METABOLISM; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ACETYLCYSTEINE; ANNEXIN A5; APOPTOSIS; CASPASES; CELL DEATH; CELL LINE, TUMOR; CYCLIC N-OXIDES; HUMANS; IMIDAZOLES; INDOLES; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SPIN LABELS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84930617410     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127386     Document Type: Article

References (53)

1. Ashkenazi A, Dixit VM (1999) Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11: 255-60. PMID: 10209153
2. Almasan A, Ashkenazi A (2003) Cytokine & Growth Factor Reviews 14: 337-48.
3. Almasan A, Ashkenazi A (2003) Apo2L/TRAIL: apoptosis signaling, biology, and potential for cancer therapy. Cytokine Growth Factor Rev 14:337-348. PMID: 12787570
4. Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM (1997) An antagonist decpy receptor and a death domain-containing receptor for TRAIL. Science 277:815-818. PMID: 9242610
5. Herbst RS, Eckhardt G, Kurzrock R, Ebbinghaus S, O'Dwyer PJ, Gordon MS (2010) Phase I dose-escalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer. J Clin Oncol 28: 2839-2846. doi: 10.1200/JCO.2009.25.1991 PMID: 20458040
6. Soria JC, Márk Z, Zatloukal P, Szima B, Albert I, Juháse E, (2011) Randomized phase II study of dulanermin in comination with paclitaxel, carboplatin, and bevacizuan in advanced non-small-cell lung cancer. J Clin Oncol 29: 4442-4451. doi: 10.1200/JCO.2011.37.2623 PMID: 22010015
7. Konopleva M, Zhao S, Xie Z, Segall H, Younes A, Claxton DF, et al. (1999) Apoptosis. molecules and mechanisms. Adv Exp Med Biol 457: 217-236. PMID: 10500797
8. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501. PMID: 9727492
9. Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: L1005-L1028. PMID: 11076791
10. Singh KK. (2006) Mitochondria damage checkpoint, aging and cancer. Ann N Y Acad Sci 1067: 182-190. PMID: 16803984
11. Kim BM, Rode AB, Han EJ, Hong IS, Hong SH (2012) 5-Phenylselenyl- and 5-methylselenyl-methyl-2′- deoxyuridine induce oxidative stress, DNA damage, and caspase-dependent apoptosis in cancer cells. Apoptosis 17: 200-216. doi: 10.1007/s10495-011-0665-2 PMID: 22002103
12. Suzuki-Karasaki Y, Suzuki-Karasaki M, Uchida M, Ochiai T (2014) Depolarization controls TRAIL-sensitization and tumor-selective killing of cancer cells: crosstalk with ROS. Frontiers in Oncol 4: 1-14.
13. Yi L, Zongyuan Y, Cheng G, Lingyun Z, Guilian Y, Wei G (2014) Quercetin enhances apoptotic effect of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) in ovarian cancer cells through reactive oxygen species (ROS) mediated CCAAT enhancer receptor 5 pathway. Cancer Sci 105: 520-527. doi: 10.1111/cas.12395 PMID: 24612139
14. Park KJ, Lee CH, Kim A, Jeong KJ, Kim CH, Kim YS (2012) Death Receptors 4 and 5 Activate Nox 1 NADPH Oxidase through Riboflavin Kinase to Induse Reactive Oxygen Species-mediated Apoptotic Cell Death. J Biol Cehm 287: 3313-3325. doi: 10.1074/jbc.M111.309021 PMID: 22158615
15. Christofferson DE, Yuan J (2010) Necroptosis as an alternative form of programmed cell death. Current Opi Cell Biol 22: 263-269.
16. Linkermann A, Green DR (2014) Necroptosis. N Engl J Med 370: 455-465. doi: 10.1056/NEJMra1310050 PMID: 24476434
17. Kaczmarek A, Vandenabeele P, Krysko DV (2013) Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38: 209-223. doi: 10.1016/j.immuni.2013. 02.003 PMID: 23438821
18. Moriwaki K, Chan F K-M (2013) RIP3: a molecular switch for necrosis and inflammation. Genes Develop 27: 1640-1649. doi: 10.1101/gad.223321.113 PMID: 23913919
19. Dillon CP, Weinlich R, Rodriguez DA, Cripps JG, Quarato G, Gurung P, et al. (2014) RIPK1 Blocks Early Postnatal Lethality Mediated by Caspase-8 and RIP3. Cell 157: 1189-1202. doi: 10.1016/j.cell.2014.04.018 PMID: 24813850
20. Green DR, Oberst A, Dillon CP, Weinlich R, Salvesen GS (2011) RIP-dependent necrosis and regulation by caspase: A mystery in five acts. Mol Cell 44: 9-16. doi: 10.1016/j.molcel.2011.09.003 PMID: 21981915
21. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, et al. (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336. doi: 10.1126/science.1172308 PMID: 19498109
22. Jouan-Lanhouet S, Arshad MI, Piquiet-Pellorce C, Martin-Chouly C, Moigne-Muller GL, Van Herre-weghe F, et al. (2012) TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ 19: 2003-2014. doi: 10.1038/cdd.2012.90 PMID: 22814620
23. Meurette O, Rebillard A, Huc L, Moigne GL, Merino D, Micheau O, et al, (2007) TRAIL induces receptor-interacting protein 1-dependent and caspase-dependent necrosis-like cell dearth under acidic extracellular conditions. Cancer Res 67: 218-226. PMID: 17210702
24. Karl I, Jossberger-Werner M, Schmidt N, Horn S, Goebeler M, Leverkus M, et al. (2014) TRAF2 inhibits TRAIL- and CD95L-induced apoptosis and necroptosis. Cell Death Dis 5: e1444. doi: 10.1038/cddis.2014.404 PMID: 25299769
25. Zhivotovsly B, Orrenius S (2005) Caspase-2 function in response to DNA damage. Biochem Biophys Res Commun 331: 859-867. PMID: 15865942
26. Chen Y, Azad MB, Gibson SB (2009) Superoxide is the major reactive oxygen specieis regulating autophagy. Cell Death Differ 16: 1040-1052. doi: 10.1038/cdd.2009.49 PMID: 19407826
27. Shimojo Y, Akimoto M, Hisanaga T, Tanala T, Tajima Y, Honma Y, et al. (2013) Attenuation of reactive oxygen species by antioxidants suppress hypoxia-induced epithelila-mesenchymal transition and metastasis of pancreatic cancer cells. Clin Exp Metastasis 30:143-154. doi: 10.1007/s10585-012-9519-8 PMID: 22833345
28. Nagaraj NS, Washington MK, Merchant NB (2011) Combined blockade of Src kinase and epidermal growth factor receptor with gemcitabine overcomes STAT3-mediated resistance of inhibition of pancreatic tumor growth. Clin Cancer Res 17:483-493. doi: 10.1158/1078-0432.CCR-10-1670 PMID: 21266529
29. Monma H, Harashima N, Inao T, Okano S, Tajima Y, Harada M (2013) The HSP70 and autophagy inhibitor pifithrin-μ enhances the antitumor effects of TRAIL on human pancreatic cancer. Mol Cancer Ther 12: 341-351. doi: 10.1158/1535-7163.MCT-12-0954 PMID: 23371857
30. Tiwari M, Sharma LK, Vanegas D, Callaway DA, Bai Y, Lechleiter JD (2014) A nonapoptotic role for CASP2/caspase 2. Autophagy 10: 1054-1070. doi: 10.4161/auto.28528 PMID: 24879153
31. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X, et al. (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4: 313-321. doi: 10.1038/nchembio.83 PMID: 18408713
32. Puccini J, Dorstyn L, Kumar S (2013) Caspase-2 as a tumor suppressor. Cell Death Differ 20: 1133-1139. doi: 10.1038/cdd.2013.87 PMID: 23811850
33. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics 2009. CA J Clin 59: 225-49. doi: 10.3322/caac.20006 PMID: 19474385
34. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48: 749-762. doi: 10.1016/j.freeradbiomed.2009.12.022 PMID: 20045723
35. Mellier G. Pervaiz S (2012) The three Rs along the TRAIL: resistance, re-sensitization and reactive oxygen species (ROS). Free Radic Res 46: 996-1003. doi: 10.3109/10715762.2012.690514 PMID: 22559302
36. Delhalle S, Deregowski V, Benoit V, Merville MP, Bours V (2002) NF-kappaB-dependent MnSOD expression protects adenocarcinoma cells from TNF-alpha-induced apoptosis. Oncogene 21: 3917-3924. PMID: 12032830
37. Perez-Cruz I, Carcamo JM, Golde DW (2003) Vitamin C inhibits FAS-induced apoptosis in monocytes and U937 cells. Blood 102: 336-343. PMID: 12623840
38. Wang Y, Nartiss Y, Steipe B, McQuibban GA, Kim PK (2012) ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 8:1462-1476. doi: 10.4161/auto.21211 PMID: 22889933
39. Gewirtz DA (2014) The four faces of autophagy: implication for cancer therapy. Cancer Res 74: 647-651. doi: 10.1158/0008-5472.CAN-13-2966 PMID: 24459182
40. Han J, Hou W, Goldstein LA, Lu C, Stolz DB, Yin XM, et al. (2008) Involvement of protective autophagy in TRAIL resistance of apoptosis-defective tumor cells. J Bio Chem 283: 19665-19677.
41. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728. PMID: 11060023
42. Vanlangenakker N, Berghe TV, Bogaert P, Laukens B, Zobel K, Deshayes K, et al. (2011) clAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ 18: 656-665. doi: 10.1038/cdd.2010.138 PMID: 21052097
43. Goossens V, De Vos K, Vercammen D, Steemans M, Vancompemolle K, Fiers W, et al. (1999) Redox regulation of TNF signaling. Biofactors 10: 145-156. PMID: 10609876
44. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, et al. (2004) Tumor necrosis factor-induced non-apoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279: 10822-10828. PMID: 14701813
45. He S, Wang L, Miao L, Wang T, Du F, Zhao L, et al. (2009) Receptor interacting protein kinase-3 determine cellular necrotic response to TNF-alpha. Cell 137: 1100-1111. doi: 10.1016/j.cell.2009.05.021 PMID: 19524512
46. Temkin V, Huang Q, Liu H, Osada H, Pope RM (2006) Inhibition of ADP/ATP exchange in receptor-interacting protein-mediated necrosis. Mol Cell Biol 26: 22125-2225.
47. Wagner KW, Engels IH, Deveraux QL (2004) Caspase-2 Can Function Upstream of Bid Cleavage in the TRAIL Apoptosis Pathway. J Biol Chem 279: 35047-35052. PMID: 15173176
48. Shin S, Lee Y, Kim W, Ko H, Choi H, Kim K (2005) Caspase-2 primes cancer cells for TRAIL-mediated apoptosis by processing procaspase-8. EMBO J 24: 3532-3542. PMID: 16193064
49. Robertson JD, Enoksson M, Suomela M, Zhivotovsky B, Orrenius S (2002) Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apoptosis. J Biol Chem 277: 29803-29809. PMID: 12065594
50. Harashima N, Minami T, Uemura H, Harada H (2014) Transfection of poly(I:C) can induce reactive oxygen species-triggered apoptosis and interferon-β-mediated growth arrest in human renal cell carcinoma cells via innate adjuvant receptors and the 2-5A system. Mol Cancer 13: 217. doi: 10.1186/1476-4598-13-217 PMID: 25227113
51. Prasad V, Chandele A, Jagtap JC, Kumar PS, Shastry P (2006) ROS-triggered caspase 2 activation and feed back amplification loop in β-carotene-induced apoptosis. Free Rad Biol Med 41: 431-442. PMID: 16843824
52. Zhang L, Fang B (2005) Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 12:228-237. PMID: 15550937
53. Ebrahimi B, Tucker SL, Li D, Abbruzzese JL, Kurzrock R (2004) Cytokines in pancreatic cancrcinoma: correlation with phanotypic characteristics and prognosis. Cancer 101: 2727-2736. PMID: 15526319