Quercetin sensitizes pancreatic cancer cells to TRAIL-induced apoptosis through JNK-mediated cFLIP turnover

International Journal of Biochemistry and Cell Biology

Volumn 78, Issue , 2016, Pages 327-334

  Kim, Ji Hye ^a   Kim, Min Joo ^a   Choi, Kyung Chul ^a   Son, Jaekyoung ^a  

^a University of Ulsan College of Medicine   (South Korea)

Author keywords

cFLIP; JNK; Pancreatic cancer; Quercetin; TRAIL

Indexed keywords

BH3 PROTEIN; CASPASE 9; FLICE INHIBITORY PROTEIN; QUERCETIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; CASPASE; CFLAR PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; CELL FRACTIONATION; CELL PERMEABILIZATION; CELL STRUCTURE; CELL VIABILITY; DRUG CYTOTOXICITY; DRUG EFFECT; ENZYME ACTIVATION; FLOW CYTOMETRY; MITOCHONDRIAL MEMBRANE; OUTER MEMBRANE; PANCREAS ADENOCARCINOMA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; WESTERN BLOTTING; DOWN REGULATION; DRUG EFFECTS; DRUG RESISTANCE; HUMAN; METABOLISM; MITOCHONDRION; MOLECULARLY TARGETED THERAPY; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASES; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; PROTEOLYSIS; QUERCETIN; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84979897074     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.07.033     Document Type: Article

References (47)

1. Adams, J.M., Cory, S., Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr. Opin. Immunol. 19:5 (2007), 488–496.
2. Ashkenazi, A., Dixit, V.M., Death receptors: signaling and modulation. Science 281:5381 (1998), 1305–1308.
3. Ashkenazi, A., Herbst, R.S., To kill a tumor cell: the potential of proapoptotic receptor agonists. J. Clin. Invest. 118:6 (2008), 1979–1990.
4. Borja-Cacho, D., Yokoyama, Y., Chugh, R.K., Mujumdar, N.R., Dudeja, V., Clawson, K.A., Dawra, R.K., Saluja, A.K., Vickers, S.M., TRAIL and triptolide: an effective combination that induces apoptosis in pancreatic cancer cells. J. Gastrointest. Surg. 14:2 (2010), 252–260.
5. Bratton, S.B., Cohen, G.M., Death receptors leave a caspase footprint that Smacs of XIAP. Cell Death Differ. 10:1 (2003), 4–6.
6. Chang, L., Kamata, H., Solinas, G., Luo, J.L., Maeda, S., Venuprasad, K., Liu, Y.C., Karin, M., The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover. Cell 124:3 (2006), 601–613.
7. Chang, C.C., Kuan, C.P., Lin, J.Y., Lai, J.S., Ho, T.F., Tanshinone IIA facilitates TRAIL sensitization by up-regulating DR5 through the ROS-JNK-CHOP signaling axis in human ovarian carcinoma cell lines. Chem. Res. Toxicol. 28:8 (2015), 1574–1583.
8. Chawla-Sarkar, M., Bae, S.I., Reu, F.J., Jacobs, B.S., Lindner, D.J., Borden, E.C., Downregulation of Bcl-2, FLIP or IAPs (XIAP and survivin) by siRNAs sensitizes resistant melanoma cells to Apo2L/TRAIL-induced apoptosis. Cell Death Differ. 11:8 (2004), 915–923.
9. Chowdhury, S.A., Kishino, K., Satoh, R., Hashimoto, K., Kikuchi, H., Nishikawa, H., Shirataki, Y., Sakagami, H., Tumor-specificity and apoptosis-inducing activity of stilbenes and flavonoids. Anticancer Res. 25:3B (2005), 2055–2063.
10. Coultas, L., Strasser, A., The role of the Bcl-2 protein family in cancer. Semin. Cancer Biol. 13:2 (2003), 115–123.
11. De Smaele, E., Zazzeroni, F., Papa, S., Nguyen, D.U., Jin, R., Jones, J., Cong, R., Franzoso, G., Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414:6861 (2001), 308–313.
12. Djerbi, M., Screpanti, V., Catrina, A.I., Bogen, B., Biberfeld, P., Grandien, A., The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med. 190:7 (1999), 1025–1032.
13. Galligan, L., Longley, D.B., McEwan, M., Wilson, T.R., McLaughlin, K., Johnston, P.G., Chemotherapy and TRAIL-mediated colon cancer cell death: the roles of p53, TRAIL receptors, and c-FLIP. Mol. Cancer Ther. 4:12 (2005), 2026–2036.
14. Granado-Serrano, A.B., Martin, M.A., Bravo, L., Goya, L., Ramos, S., Quercetin induces apoptosis via caspase activation, regulation of Bcl-2, and inhibition of PI-3-kinase/Akt and ERK pathways in a human hepatoma cell line (HepG2). J. Nutr. 136:11 (2006), 2715–2721.
15. Hamacher, R., Schmid, R.M., Saur, D., Schneider, G., Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol. Cancer, 7, 2008, 64.
16. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J.L., Schroter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L.E., Tschopp, J., Inhibition of death receptor signals by cellular FLIP. Nature 388:6638 (1997), 190–195.
17. Ivanov, V.N., Bhoumik, A., Ronai, Z., Death receptors and melanoma resistance to apoptosis. Oncogene 22:20 (2003), 3152–3161.
18. Jemal, A., Siegel, R., Xu, J., Ward, E., Cancer statistics, 2010. CA : a cancer journal for clinicians 60:5 (2010), 277–300.
19. Jung, Y.H., Heo, J., Lee, Y.J., Kwon, T.K., Kim, Y.H., Quercetin enhances TRAIL-induced apoptosis in prostate cancer cells via increased protein stability of death receptor 5. Life Sci. 86:9–10 (2010), 351–357.
20. Kim, Y.H., Lee, Y.J., TRAIL apoptosis is enhanced by quercetin through Akt dephosphorylation. J. Cell. Biochem. 100:4 (2007), 998–1009.
21. Kim, J.Y., Kim, E.H., Park, S.S., Lim, J.H., Kwon, T.K., Choi, K.S., Quercetin sensitizes human hepatoma cells to TRAIL-induced apoptosis via Sp1-mediated DR5 up-regulation and proteasome-mediated c-FLIPS down-regulation. J. Cell. Biochem. 105:6 (2008), 1386–1398.
22. Kim, Y.H., Lee, D.H., Jeong, J.H., Guo, Z.S., Lee, Y.J., Quercetin augments TRAIL-induced apoptotic death: involvement of the ERK signal transduction pathway. Biochem. Pharmacol. 75:10 (2008), 1946–1958.
23. Kim, H.J., Kim, S.K., Kim, B.S., Lee, S.H., Park, Y.S., Park, B.K., Kim, S.J., Kim, J., Choi, C., Kim, J.S., Cho, S.D., Jung, J.W., Roh, K.H., Kang, K.S., Jung, J.Y., Apoptotic effect of quercetin on HT-29 colon cancer cells via the AMPK signaling pathway. J. Agric. Food Chem. 58:15 (2010), 8643–8650.
24. Lamson, D.W., Brignall, M.S., Antioxidants and cancer, part 3: quercetin. Altern. Med. Rev. 5:3 (2000), 196–208.
25. LeBlanc, H.N., Ashkenazi, A., Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ. 10:1 (2003), 66–75.
26. Longley, D.B., Wilson, T.R., McEwan, M., Allen, W.L., McDermott, U., Galligan, L., Johnston, P.G., c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene 25:6 (2006), 838–848.
27. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., Wang, X., Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:4 (1998), 481–490.
28. Luqmani, Y.A., Mechanisms of drug resistance in cancer chemotherapy. Med. Princ. Pract. 14:Suppl. 1 (2005), 35–48.
29. Malladi, S., Challa-Malladi, M., Fearnhead, H.O., Bratton, S.B., The Apaf-1*procaspase-9 apoptosome complex functions as a proteolytic-based molecular timer. EMBO J. 28:13 (2009), 1916–1925.
30. Micheau, O., Lens, S., Gaide, O., Alevizopoulos, K., Tschopp, J., NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 21:16 (2001), 5299–5305.
31. Muppidi, J.R., Tschopp, J., Siegel, R.M., Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 21:4 (2004), 461–465.
32. Nesterov, A., Lu, X., Johnson, M., Miller, G.J., Ivashchenko, Y., Kraft, A.S., Elevated AKT activity protects the prostate cancer cell line LNCaP from TRAIL-induced apoptosis. J. Biol. Chem. 276:14 (2001), 10767–10774.
33. Nobili, S., Lippi, D., Witort, E., Donnini, M., Bausi, L., Mini, E., Capaccioli, S., Natural compounds for cancer treatment and prevention. Pharmacol. Res. 59:6 (2009), 365–378.
34. Pitti, R.M., Marsters, S.A., Ruppert, S., Donahue, C.J., Moore, A., Ashkenazi, A., Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271:22 (1996), 12687–12690.
35. Primikyri, A., Chatziathanasiadou, M.V., Karali, E., Kostaras, E., Mantzaris, M.D., Hatzimichael, E., Shin, J.S., Chi, S.W., Briasoulis, E., Kolettas, E., Gerothanassis, I.P., Tzakos, A.G., Direct binding of Bcl-2 family proteins by quercetin triggers its pro-apoptotic activity. ACS Chem. Biol. 9:12 (2014), 2737–2741.
36. Sayers, T.J., Targeting the extrinsic apoptosis signaling pathway for cancer therapy. Cancer Immunol. Immunother: CII 60:8 (2011), 1173–1180.
37. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K.J., Debatin, K.M., Krammer, P.H., Peter, M.E., Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:6 (1998), 1675–1687.
38. Senthilkumar, K., Arunkumar, R., Elumalai, P., Sharmila, G., Gunadharini, D.N., Banudevi, S., Krishnamoorthy, G., Benson, C.S., Arunakaran, J., Quercetin inhibits invasion, migration and signalling molecules involved in cell survival and proliferation of prostate cancer cell line (PC-3). Cell Biochem. Funct. 29:2 (2011), 87–95.
39. Son, J.K., Varadarajan, S., Bratton, S.B., TRAIL-activated stress kinases suppress apoptosis through transcriptional upregulation of MCL-1. Cell Death Differ. 17:8 (2010), 1288–1301.
40. Trivedi, R., Mishra, D.P., Trailing TRAIL resistance: novel targets for TRAIL sensitization in cancer cells. Front. Oncol., 5, 2015, 69.
41. Ullenhag, G.J., Mukherjee, A., Watson, N.F., Al-Attar, A.H., Scholefield, J.H., Durrant, L.G., Overexpression of FLIPL is an independent marker of poor prognosis in colorectal cancer patients. Clin. Cancer Res: Off. J. Am. Assoc. Cancer Res. 13:17 (2007), 5070–5075.
42. Valente, G., Manfroi, F., Peracchio, C., Nicotra, G., Castino, R., Nicosia, G., Kerim, S., Isidoro, C., cFLIP expression correlates with tumour progression and patient outcome in non-Hodgkin lymphomas of low grade of malignancy. Br. J. Haematol. 132:5 (2006), 560–570.
43. Vijayababu, M.R., Kanagaraj, P., Arunkumar, A., Ilangovan, R., Dharmarajan, A., Arunakaran, J., Quercetin induces p53-independent apoptosis in human prostate cancer cells by modulating Bcl-2-related proteins: a possible mediation by IGFBP-3. Oncol. Res. 16:2 (2006), 67–74.
44. Walczak, H., Krammer, P.H., The CD95 (APO-1/Fas) and the TRAIL (APO-2L) apoptosis systems. Exp. Cell Res. 256:1 (2000), 58–66.
45. Walczak, H., Miller, R.E., Ariail, K., Gliniak, B., Griffith, T.S., Kubin, M., Chin, W., Jones, J., Woodward, A., Le, T., Smith, C., Smolak, P., Goodwin, R.G., Rauch, C.T., Schuh, J.C., Lynch, D.H., Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5:2 (1999), 157–163.
46. Wang, P., Zhang, J., Bellail, A., Jiang, W., Hugh, J., Kneteman, N.M., Hao, C., Inhibition of RIP and c-FLIP enhances TRAIL-induced apoptosis in pancreatic cancer cells. Cell. Signal. 19:11 (2007), 2237–2246.
47. Yi, L., Zongyuan, Y., Cheng, G., Lingyun, Z., Guilian, Y., Wei, G., 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-binding protein homologous protein (CHOP)-death receptor 5 pathway. Cancer Sci. 105:5 (2014), 520–527.