Parthenolide enhances sensitivity of colorectal cancer cells to TRAIL by inducing death receptor 5 and promotes TRAIL-induced apoptosis

International Journal of Oncology

Volumn 46, Issue 3, 2015, Pages 1121-1130

  Kim, Se Lim ^a   Liu, Yu Chuan ^a   Park, Young Ran ^a   Seo, Seung Young ^a   Kim, Seong Hun ^a   Kim, In Hee ^a   Lee, Seung Ok ^a   Lee, Soo Teik ^a   Kim, Dae Ghon ^a   Kim, Sang Wook ^a  

^a Chonbuk National University Medical School and Hospital   (South Korea)

Author keywords

Apoptosis; Death receptor; Parthenolide; TRAIL; TRAIL resistance

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; DEATH RECEPTOR 5; LIPOCORTIN 5; PARTHENOLIDE; PROTEIN BCL 2; PROTEIN P53; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ANTINEOPLASTIC AGENT; SESQUITERPENE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CELL ASSAY; CELL DEATH; CELL STRUCTURE; CELL VIABILITY; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DRUG SENSITIVITY; G1 PHASE CELL CYCLE CHECKPOINT; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MTT ASSAY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STAINING; UPREGULATION; CELL CULTURE; COLORECTAL NEOPLASMS; DRUG EFFECTS; DRUG POTENTIATION; METABOLISM; PATHOLOGY;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL DEATH; CELLS, CULTURED; COLORECTAL NEOPLASMS; DRUG SYNERGISM; HCT116 CELLS; HT29 CELLS; HUMANS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SESQUITERPENES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION;

EID: 84921898029     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2795     Document Type: Article

References (59)

1. Johnstone RW, Frew AJ and Smyth MJ: The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 8: 782-798, 2008.
2. Koschny R, Walczak H and Ganten TM: The promise of TRAIL - potential and risks of a novel anticancer therapy. J Mol Med (Berl) 85: 923-935, 2007.
3. Walczak H, Miller RE, Ariail K, et al: Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163, 1999.
4. Gonzalvez F and Ashkenazi A: New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 29: 4752-4765, 2010.
5. Shi Y: Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9: 459-470, 2002.
6. Ashkenazi A, Holland P and Eckhardt SG: Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol 26: 3621-3630, 2008.
7. Pan Y, Xu R, Peach M, et al: Evaluation of pharmacodynamic biomarkers in a Phase 1a trial of dulanermin (rhApo2L/TRAIL) in patients with advanced tumours. Br J Cancer 105: 1830-1838, 2011.
8. Wiezorek J, Holland P and Graves J: Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res 16: 1701-1708, 2010.
9. Dimberg LY, Anderson CK, Camidge R, Behbakht K, Thorburn A and Ford HL: On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene 32: 1341-1350, 2013.
10. Zhang L and Fang B: Mechanisms of resistance to TRAILinduced apoptosis in cancer. Cancer Gene Ther 12: 228-237, 2005.
11. Jin Z, McDonald ER III, Dicker DT and El-Deiry WS: Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 279: 35829-35839, 2004.
12. Kim HS, Lee JW, Soung YH, et al: Inactivating mutations of caspase-8 gene in colorectal carcinomas. Gastroenterology 125: 708-715, 2003.
13. Hernandez A, Wang QD, Schwartz SA and Evers BM: Sensitization of human colon cancer cells to TRAIL-mediated apoptosis. J Gastrointest Surg 5: 56-65, 2001.
14. Burns TF and El-Deiry WS: Identification of inhibitors of TRAIL-induced death (ITIDs) in the TRAIL-sensitive colon carcinoma cell line SW480 using a genetic approach. J Biol Chem 276: 37879-37886, 2001.
15. Cummins JM, Kohli M, Rago C, Kinzler KW, Vogelstein B and Bunz F: X-linked inhibitor of apoptosis protein (XIAP) is a nonredundant modulator of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis in human cancer cells. Cancer Res 64: 3006-3008, 2004.
16. Murphy JJ, Heptinstall S and Mitchell JR: Randomised doubleblind placebo-controlled trial of feverfew in migraine prevention. Lancet 2: 189-192, 1988.
17. Hehner SP, Heinrich M, Bork PM, et al: Sesquiterpene lactones specifically inhibit activation of NF-kappa B by preventing the degradation of I kappa B-alpha and I kappa B-beta. J Biol Chem 273: 1288-1297, 1998.
18. Lyss G, Knorre A, Schmidt TJ, Pahl HL and Merfort I: The anti-inflammatory sesquiterpene lactone helenalin inhibits the transcription factor NF-kappaB by directly targeting p65. J Biol Chem 273: 33508-33516, 1998.
19. Zhang S, Ong CN and Shen HM: Involvement of proapoptotic Bcl-2 family members in parthenolide-induced mitochondrial dysfunction and apoptosis. Cancer Lett 211: 175-188, 2004.
20. Kim SL, Trang KT, Kim SH, et al: Parthenolide suppresses tumor growth in a xenograft model of colorectal cancer cells by inducing mitochondrial dysfunction and apoptosis. Int J Oncol 41: 1547-1553, 2012.
21. Wen J, You KR, Lee SY, Song CH and Kim DG: Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J Biol Chem 277: 38954-38964, 2002.
22. Zhang S, Ong CN and Shen HM: Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett 208: 143-153, 2004.
23. Pajak B, Gajkowska B and Orzechowski A: Molecular basis of parthenolide-dependent proapoptotic activity in cancer cells. Folia Histochem Cytobiol 46: 129-135, 2008.
24. Dai Y, Guzman ML, Chen S, et al : The NF (Nuclear factor)-kappaB inhibitor parthenolide interacts with histone deacetylase inhibitors to induce MKK7/JNK1-dependent apoptosis in human acute myeloid leukaemia cells. Br J Haematol 151: 70-83, 2010.
25. Sun Y, St Clair DK, Xu Y, Crooks PA and St Clair WH: A NADPH oxidase-dependent redox signaling pathway mediates the selective radiosensitization effect of parthenolide in prostate cancer cells. Cancer Res 70: 2880-2890, 2010.
26. Sobota R, Szwed M, Kasza A, Bugno M and Kordula T: Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochem Biophys Res Commun 267: 329-333, 2000.
27. Kim SL, Lee ST, Trang KT, et al: Parthenolide exerts inhibitory effects on angiogenesis through the downregulation of VEGF/ VEGFRs in colorectal cancer. Int J Mol Med 33: 1261-1267, 2014.
28. Carlisi D, D'Anneo A, Angileri L, et al: Parthenolide sensitizes hepatocellular carcinoma cells to TRAIL by inducing the expression of death receptors through inhibition of STAT3 activation. J Cell Physiol 226: 1632-1641, 2011.
29. Fang LJ, Shao XT, Wang S, Lu GH, Xu T and Zhou JY: Sesquiterpene lactone parthenolide markedly enhances sensitivity of human A549 cells to low-dose oxaliplatin via inhibition of NF-kappaB activation and induction of apoptosis. Planta Med 76: 258-264, 2010.
30. Gao ZW, Zhang DL and Guo CB: Paclitaxel efficacy is increased by parthenolide via nuclear factor-kappaB pathways in in vitro and in vivo human non-small cell lung cancer models. Curr Cancer Drug Targets 10: 705-715, 2010.
31. Yun BR, Lee MJ, Kim JH, Kim IH, Yu GR and Kim DG: Enhancement of parthenolide-induced apoptosis by a PKC-alpha inhibition through heme oxygenase-1 blockage in cholangiocarcinoma cells. Exp Mol Med 42: 787-797, 2010.
32. Lee CS, Kim YJ, Lee SA, Myung SC and Kim W: Combined effect of Hsp90 inhibitor geldanamycin and parthenolide via reactive oxygen species-mediated apoptotic process on epithelial ovarian cancer cells. Basic Clin Pharmacol Toxicol 111: 173-181, 2012.
33. Yip-Schneider MT, Nakshatri H, Sweeney CJ, Marshall MS, Wiebke EA and Schmidt CM: Parthenolide and sulindac cooperate to mediate growth suppression and inhibit the nuclear factor-kappa B pathway in pancreatic carcinoma cells. Mol Cancer Ther 4: 587-594, 2005.
34. Kim SL, Kim SH, Trang KT, et al: Synergistic antitumor effect of 5-fluorouracil in combination with parthenolide in human colorectal cancer. Cancer Lett 335: 479-486, 2013.
35. Fulda S and Debatin KM: Death receptor signaling in cancer therapy. Curr Med Chem Anticancer Agents 3: 253-262, 2003.
36. Fearon ER and Vogelstein B: A genetic model for colorectal tumorigenesis. Cell 61: 759-767, 1990.
37. Bates RC, Edwards NS, Burns GF and Fisher DE: A CD44 survival pathway triggers chemoresistance via lyn kinase and phosphoinositide 3-kinase/Akt in colon carcinoma cells. Cancer Res 61: 5275-5283, 2001.
38. Woynarowski JM and Konopa J: Inhibition of DNA biosynthesis in HeLa cells by cytotoxic and antitumor sesquiterpene lactones. Mol Pharmacol 19: 97-102, 1981.
39. Nakshatri H, Rice SE and Bhat-Nakshatri P: Antitumor agent parthenolide reverses resistance of breast cancer cells to tumor necrosis factor-related apoptosis-inducing ligand through sustained activation of c-Jun N-terminal kinase. Oncogene 23: 7330-7344, 2004.
40. Vasilevskaya IA and O'Dwyer PJ: 17-Allylamino-17-demethoxygeldanamycin overcomes TRAIL resistance in colon cancer cell lines. Biochem Pharmacol 70: 580-589, 2005.
41. Galligan L, Longley DB, McEwan M, Wilson TR, McLaughlin K and Johnston PG: Chemotherapy and TRAIL-mediated colon cancer cell death: the roles of p53, TRAIL receptors, and c-FLIP. Mol Cancer Ther 4: 2026-2036, 2005.
42. Saturno G, Valenti M, De Haven Brandon A, et al: Combining trail with PI3 kinase or HSP90 inhibitors enhances apoptosis in colorectal cancer cells via suppression of survival signaling. Oncotarget 4: 1185-1198, 2013.
43. Ashkenazi A and Herbst RS: To kill a tumor cell: the potential of proapoptotic receptor agonists. J Clin Invest 118: 1979-1990, 2008.
44. Eberle J, Fecker LF, Forschner T, Ulrich C, Rowert-Huber J and Stockfleth E: Apoptosis pathways as promising targets for skin cancer therapy. Br J Dermatol 156 (Suppl 3): 18-24, 2007.
45. Pennarun B, Meijer A, de Vries EG, Kleibeuker JH, Kruyt F and de Jong S: Playing the DISC: turning on TRAIL death receptormediated apoptosis in cancer. Biochim Biophys Acta 1805: 123-140, 2010.
46. Jung YH, Heo J, Lee YJ, Kwon TK and Kim YH: Quercetin enhances TRAIL-induced apoptosis in prostate cancer cells via increased protein stability of death receptor 5. Life Sci 86: 351-357, 2010.
47. Prasad S, Ravindran J, Sung B, Pandey MK and Aggarwal BB: Garcinol potentiates TRAIL-induced apoptosis through modulation of death receptors and antiapoptotic proteins. Mol Cancer Ther 9: 856-868, 2010.
48. Kim YH, Lee DH, Jeong JH, Guo ZS and Lee YJ: Quercetin augments TRAIL-induced apoptotic death: involvement of the ERK signal transduction pathway. Biochem Pharmacol 75: 1946-1958, 2008.
49. Psahoulia FH, Drosopoulos KG, Doubravska L, Andera L and Pintzas A: Quercetin enhances TRAIL-mediated apoptosis in colon cancer cells by inducing the accumulation of death receptors in lipid rafts. Mol Cancer Ther 6: 2591-2599, 2007.
50. Sung B, Park B, Yadav VR and Aggarwal BB: Celastrol, a triterpene, enhances TRAIL-induced apoptosis through the down-regulation of cell survival proteins and up-regulation of death receptors. J Biol Chem 285: 11498-11507, 2010.
51. Park MH, Jo M, Won D, Song HS, Song MJ and Hong JT: Snake venom toxin from Vipera lebetina turanica sensitizes cancer cells to TRAIL through ROS- and JNK-mediated upregulation of death receptors and downregulation of survival proteins. Apoptosis 17: 1316-1326, 2012.
52. Fernandes-Alnemri T, Litwack G and Alnemri ES: CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 beta-converting enzyme. J Biol Chem 269: 30761-30764, 1994.
53. Teitz T, Wei T, Valentine MB, et al: Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 6: 529-535, 2000.
54. Mignotte B and Vayssiere JL: Mitochondria and apoptosis. Eur J Biochem 252: 1-15, 1998.
55. Reed JC: Double identity for proteins of the Bcl-2 family. Nature 387: 773-776, 1997.
56. De Angelis PM, Stokke T, Thorstensen L, Lothe RA and Clausen OP: Apoptosis and expression of Bax, Bcl-x, and Bcl-2 apoptotic regulatory proteins in colorectal carcinomas, and association with p53 genotype/phenotype. Mol Pathol 51: 254-261, 1998.
57. Maurer CA, Friess H, Buhler SS, et al: Apoptosis inhibiting factor Bcl-xL might be the crucial member of the Bcl-2 gene family in colorectal cancer. Dig Dis Sci 43: 2641-2648, 1998.
58. Rampino N, Yamamoto H, Ionov Y, et al: Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 275: 967-969, 1997.
59. Sionov RV and Haupt Y: The cellular response to p53: the decision between life and death. Oncogene 18: 6145-6157, 1999.