Quercetin sensitizes human hepatoma cells to TRAIL-induced apoptosis via Sp1-mediated DR5 up-regulation and proteasome-mediated c-FLIPS down-regulation

Journal of Cellular Biochemistry

Volumn 105, Issue 6, 2008, Pages 1386-1398

  Jin, Yeop Kim ^a   Eun, Hee Kim ^a   Seok, Soon Park ^a   Jun, Hee Lim ^b   Taeg, Kyu Kwon ^b   Kyeong, Sook Choi ^a  

^a Ajou University School of Medicine   (South Korea)

^b Keimyung University School of Medicine   (South Korea)

Author keywords

c FLIPS; DR5; Hepatoma; Quercetin; Trail

Indexed keywords

DEATH RECEPTOR 5; FLICE INHIBITORY PROTEIN; MESSENGER RNA; MORIN; MYRICETIN; PROCASPASE 3; PROTEASOME; PROTEIN BCL XL; QUERCETIN; QUERCITRIN; RUTOSIDE; SMALL INTERFERING RNA; TAXIFOLIN; TRANSCRIPTION FACTOR SP1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CHEMOSENSITIZATION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG MECHANISM; DRUG POTENTIATION; DRUG RESISTANCE; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UPREGULATION;

ANTIOXIDANTS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; DOWN-REGULATION; HUMANS; LIVER NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; QUERCETIN; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SP1 TRANSCRIPTION FACTOR; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 57349169369     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21958     Document Type: Article

References (53)

1. Aghdassi A, Phillips P, Dudeja V, Dhaulakhandi D, Sharif R, Dawra R, Lerch MM, Saluja A. 2007. Heat shock protein 7 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res 67:616-625.
2. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155-162.
3. Avila MA, Berasain C, Sangro B, Prieto J. 2006. New therapies for hepatocellular carcinoma. Oncogene 25:3866-3884.
4. Bai J, Sui J, Demirjian A, Vollmer CM Jr, Marasco W, Callery MP. 2005. Predominant Bcl-XL knockdown disables antiapoptotic mechanisms: Tumor necrosis factor-related apoptosis-inducing ligand-based triple chemotherapy overcomes chemoresistance in pancreatic cancer cells in vitro. Cancer Res 65:2344-2352.
5. Brit DF, Hendrich S, Wang W. 2001. Dietary agents in cancer prevention: Flavonoids and isoflavonoids. Pharmacol Ther 90:157-177.
6. Bruix J, Boix L, Sala M, Llovet JM. 2004. Focus on hepatocellular carcinoma. Cancer Cell 5:215-219.
7. Budagova KR, Zhmaeva SV, Grigor'ev AN, Goncharova AY, Kabakov AE. 2003. Flavonoid dihydroquercetin, unlike quercetin, fails to inhibit expression of heat shock proteins under conditions of cellular stress. Biochemistry (Mosc) 68:1055-1061.
8. Chawla-Sarkar M, Bae SI, Reu FJ, Jacobs BS, Lindner DJ, Borden EC. 2004. 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: 915-923.
9. Chen W, Wang X, Zhuang J, Zhang L, Lin Y. 2007. Induction of death receptor 5 and suppression of survivin contribute to sensitization of TRAIL-induced cytotoxicity by quercetin in non-small cell lung cancer cells. Carcinogenesis 28:2114-2121.
10. Chowdhury SA, Kishino K, Satoh R, Hashimoto K, Kikuchi H, Nishikawa H, Shirataki Y, Sakagami H. 2005. Tumor-specificity and apoptosis-inducing activity of stilbenes and flavonoids. Anticancer Res 25:2055-2063.
11. Csokay B, Prajda N, Weber G, Olah E. 1997. Molecular mechanisms in the antiproliferative action of quercetin. Life Sci 60:2157-2163.
12. Dolcet X, Llobet D, Pallares J, Rue M, Comella JX, Matias-Guiu X. 2005. FLIP is frequently expressed in endometrial carcinoma and has a role in resistance to TRAIL-induced apoptosis. Lab Invest 85:885-894.
13. Duarte J, Pérez-Palencia R, Vargas F, Ocete MA, Pérez-Vizcaino F, Zarzuelo A, Tamargo J. 2001. Antihypertensive effects of the flavonoid quercetin in spontaneously hypertensive rats. Br J Pharmacol 133:117-124.
14. Habtemariam S. 1997. Flavonoids as inhibitors or enhancers of the cytotoxicity of tumor necrosis factor-alpha in L-929 tumor cells. J Nat Prod 60:775-778.
15. Havsteen R. 1983. Flavonoids, a class of natural products of high pharmacological potency. Biochem Pharmacol 32:1141-1148.
16. Hsu IC, Metcalf RA, Sun T, Welsh JA, Wang NJ, Harris CC. 1991. Mutational hotspot in the p53 gene in human hepatocellular carcinomas. Nature 350:427-428.
17. Hsu IC, Tokiwa T, Bennett W, Metcalf RA, Welsh JA, Sun T, Harris CC. 1993. p53 gene mutation and integrated hepatitis B viral DNA sequences in human liver cancer cell lines. Carcinogenesis 14:987-992.
18. Irmler M, Thome M, Hahne M, Schneider P, Hofmann K, Steiner V, Bodmer JL, Schröter M, Burns K, Mattmann C, Rimoldi D, French LE, Tschopp J. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388:190-195.
19. Kang MS, Lee HJ, Lee JH, Ku JL, Lee KP, Kelley MJ, Won YJ, Kim ST, Park JG. 1996. Mutation of p53 gene in hepatocellular carcinoma cell lines with HBX DNA. Int J Cancer 67:898-902.
20. Kelly MM, Hoel BD, Voelkel-Johnson C. 2002. Doxorubicin pretreatment sensitizes prostate cancer cell lines to TRAIL induced apoptosis which correlates with the loss of c-FLIP expression. Cancer Biol Ther 1:520-527.
21. Kim YH, Lee YJ. 2007. TRAIL apoptosis is enhanced by quercetin through Akt dephosphorylation. J Cell Biochem 100:998-1009.
22. Kim EH, Kim SU, Shin DY, Choi KS. 2004a. Roscovitine sensitizes glioma cells to TRAIL-mediated apoptosis by downregulation of survivin and XIAP. Oncogene 23:446-456.
23. Kim YH, Park JW, Lee JY, Kwon TK. 2004b. Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 25:1813-1820.
24. Kim H, Kim EH, Eom YW, Kim WH, Kwon TK, Lee SJ, Choi KS. 2006. Sulforaphane sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-resistant hepatoma cells to TRAIL-induced apoptosis through reactive oxygen species-mediated up-regulation of DR5. Cancer Res 66:1740-1750.
25. Lamson DW, Brignall MS. 2000. Antioxidants and cancer. Part 3. Quercetin. Altern Med Rev 5:196-208.
26. Le Marchand L, Murphy SP, Hankin JH, Wilkens LR, Kolonel LN. 2000. Intake of flavonoids and lung cancer. J Natl Cancer Inst 92:154-160.
27. Loke WM, Proudfoot JM, Stewart S, McKinley AJ, Needs PW, Kroon PA, Hodgson JM, Croft KD. 2008. Metabolic transformation has a profound effect on anti-inflammatory activity of flavonoids such as quercetin: Lack of association between antioxidant and lipoxygenase inhibitory activity. Biochem Pharmacol 75:1045-1053.
28. Micheau O, Thome M, Schneider P, Holler N, Tschopp J, Nicholson DW, Briand C, Grütter MG. 2002. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 277:45162-45167.
29. Mouria M, Gukovskaya AS, Jung Y, Buechler P, Hines OJ, Reber HA, Pandol SJ. 2002. Food-derived polyphenols inhibit pancreatic cancer growth through mitochondrial cytochrome c release and apoptosis. Int J Cancer 98:761-769.
30. Nair H, Rao K, Aalinkeel R, Mahajan S, Chawda R, Schwartz S. 2004. Inhibition of prostate cancer cell conlony formation by the flavonoid quercetin correlates with modulation of specific regulatory genes. Clin Diagnostic Lab Immunol 11:63-69.
31. Palacios C, Yerbes R, Lopez-Rivas A. 2006. Flavopiridol induces cellular FLICE-inhibitory protein degradation by the proteasome and promotes TRAIL-induced early signaling and apoptosis in breast tumor cells. Cancer Res 66:8858-8869.
32. Pan G, O'Rourke K, Chinnaiyan AM, Gentz R, Ebner R, Ni J, Dixit VM. 1997. The receptor for the cytotoxic ligand TRAIL. Science 276:111-113.
33. Pei Z, Chu L, Zou W, Zhang Z, Qiu S, Qi R, Gu J, Qian C, Liu X. 2004. An oncolytic adenoviral vector of Smac increases antitumor activity of TRAIL against HCC in human cells and in mice. Hepatology 39:1371-1381.
34. Perez-Vizcaino F, Duarte J, Andriantsitohaina R. 2006. Endothelial function and cardiovascular disease: Effects of quercetin and wine polyphenols. Free Radic Res 40:1054-1065.
35. Poukkula M, Kaunisto A, Hietakangas V, Denessiouk K, Katajamäki T, Johnson MS, Sistonen L, Eriksson JE. 2005. Rapid turnover of c-FLIP short is determined by its unique C-terminal tail. J Biol Chem 280:27345-27355.
36. Ravi R, Bedi GC, Engstrom LW, Zeng Q, Mookerjee B, Gélinas C, Fuchs EJ, Bedi A. 2001. Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB. Nat Cell Biol 3:409-416.
37. Shankar S, Srivastava RK. 2004. Enhancement of therapeutic potential of TRAIL by cancer chemotherapy and irradiation: Mechanisms and clinical implications. Drug Resist Updat 7:139-156.
38. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P, Ashkenazi A. 1997. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277:818-821.
39. Son YG, Kim EH, Kim JY, Kim SU, Kwon TK, Yoon AR, Yun CO, Choi KS. 2007. Silibinin sensitizes human glioma cells to TRAIL-mediated apoptosis via DR5 up-regulation and down-regulation of c-FLIP and survivin. Cancer Res 67:8274-8284.
40. Srivastava RK. 2001. TRAIL/Apo-2L: Mechanisms and clinical applications in cancer. Neoplasia 3:535-546.
41. Surh YJ. 2003. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 3:768-780.
42. Takehara T, Liu X, Fujimoto J, Friedman SL, Takahashi H. 2001. Expression and role of Bcl-xL in human hepatocellular carcinomas. Hepatology 34:55-61.
43. Thomas LR, Henson A, Reed JC, Salsbury FR, Thorburn A. 2004. Direct binding of Fas-associated death domain (FADD) to the tumor necrosis factor-related apoptosis-inducing ligand receptor DR5 is regulated by the death effector domain of FADD. J Biol Chem 279:32780-32785.
44. Velculescu VE, El-Deiry WS. 1996. Biological and clinical importance of the p53 tumor suppressor gene. Clin Chem 42:858-868.
45. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5:157-163.
46. Wei YQ, Zhao X, Kariya Y, Fukata H, Teshigawara K, Uchida A. 1994. Induction of apoptosis by quercetin: Involvement of heat shock protein. Cancer Res 54:4952-4957.
47. Wu GS, Burns TF, McDonald ER III, Meng RD, Kao G, Muschel R, Yen T, el-Deiry WS. 1999. Induction of the TRAIL receptor Killer/DR5 in p53-dependent apoptosis but not growth arrest. Oncogene 18:6411-6418.
48. Xiao J, Suzuki M, Jiang X, Chen X, Yamamoto K, Ren F, Xu M. 2008. Influence of B-ring hydroxylation on interactions of flavonols with bovine serum albumin. J Agric Food Chem 56:2350-2356.
49. Yamaguchi H, Wang HG. 2004. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 279:45495-45502.
50. Yamanaka T, Shiraki K, Sugimoto K, Ito T, Fujikawa K, Ito M, Takase K, Moriyama M, Nakano T, Suzuki A. 2000. Chemotherapeutic agents augment TRAIL-induced apoptosis in human hepatocellular carcinoma cell lines. Hepatology 32:482-490.
51. Yoshida T, Maeda A, Tani N, Sakai T. 2001. Promoter structure and transcription initiation sites of the human death receptor 5/TRAIL-R2 gene. FEBS Lett 507:381-385.
52. Yoshida T, Shiraishi T, Nakata S, Horinaka M, Wakada M, Mizutani Y, Miki T, Sakai T. 2005. Proteasome inhibitor MG132 induces death receptor 5 through CCAAT/enhancer-binding protein homologous protein. Cancer Res 65:5662-5667.
53. Zhang X, Jin TG, Yang H, DeWolf WC, Khosravi-Far R, Olumi AF. 2004. Persistent c-FLIPL expression is necessary and sufficient to maintain resistance to tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis in prostate cancer. Cancer Res 64:7086-7091.