Suppression of cFLIP by lupeol, a dietary triterpene, is sufficient to overcome resistance to TRAIL-mediated apoptosis in chemoresistant human pancreatic cancer cells

Cancer Research

Volumn 69, Issue 3, 2009, Pages 1156-1165

  Murtaza, Imtiyaz ^a   Saleem, Mohammad ^a   Adhami, Vaqar Mustafa ^a   Hafeez, Bilal Bin ^a   Mukhtar, Hasan ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; FLICE INHIBITORY PROTEIN; LUPEOL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CARCINOGENICITY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUDE MOUSE; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SENSITIZATION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 8; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DRUG SYNERGISM; HUMANS; MICE; MICE, NUDE; PANCREATIC NEOPLASMS; RECOMBINANT PROTEINS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSCRIPTIONAL ACTIVATION; TRITERPENES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 59149087882     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2917     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Garcea G, Dennison AR, Pattenden CJ, Neal CP, Sutton CD, Berry DP. Survival following curative resection for pancreatic ductal adenocarcinoma. A systematic review of the literature. JOP 2008;9:99-132.
3. Mimeault M, Brand RE, Sasson AA, Batra SK. Recent advances on the molecular mechanisms involved in pancreatic cancer progression and therapies. Pancreas 2005;31:301-16.
4. Westphal S, Kalthoff H. Apoptosis: targets in pancreatic cancer. Mol Cancer 2003;2:6.
5. Xiong HQ. Molecular targeting therapy for pancreatic cancer. Cancer Chemother Pharmacol 2004;54:69-77.
6. Hall MA, Cleveland JL. Clearing the TRAIL for cancer therapy. Cancer Cell 2007;12:4-6.
7. Kruyt FA. TRAIL and cancer therapy. Cancer Lett 2008;263:14-25.
8. Yang JK. FLIP as an anti-cancer therapeutic target. Yonsei Med J 2008;49:19-27.
9. Chaudhari BR, Murphy RF, Agrawal DK. Following the TRAIL to apoptosis. Immunol Res 2006;35:249-62.
10. Koschny R, Walczak H, Ganten TM. The promise of TRAIL-potential and risks of a novel anticancer therapy. J Mol Med 2007;85:923-35.
11. Mori T, Doi R, Toyoda E, et al. Regulation of the resistance to TRAIL-induced apoptosis as a new strategy for pancreatic cancer. Surgery 2005;138:71-7.
12. Ibrahim SM, Ringel J, Schmidt C, et al. Pancreatic adenocarcinoma cell lines show variable susceptibility to TRAIL-mediated cell death. Pancreas 2001;23:72-9.
13. Zhang L, Fang B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 2005;12:228-37.
14. Zhang L, Zhu H, Teraishi F, et al. Accelerated degradation of caspase-8 protein correlates with TRAIL resistance in a DLD1 human colon cancer cell line. Neoplasia 2005;7:594-602.
15. Yamaguchi Y, Shiraki K, Fuke H, et al. Adenovirus-mediated transfection of caspase-8 sensitizes hepatocellular carcinoma to TRAIL- and chemotherapeutic agent-induced cell death. Biochim Biophys Acta 2006;1763:844-53.
16. Mühlethaler-Mottet A, Balmas K, Auderset K, Joseph JM, Gross N. Restoration of TRAIL-induced apoptosis in a caspase-8-deficient neuroblastoma cell line by stable re-expression of caspase-8. Ann N Y Acad Sci 2003;1010:195-9.
17. Longley DB, Wilson TR, McEwan M, et al. c-FLIP inhibits chemotherapy-induced colorectal cancer cell death. Oncogene 2006;25:838-48.
18. Rippo MR, Moretti S, Vescovi S, et al. FLIP overexpression inhibits death receptor-induced apoptosis in malignant mesothelial cells. Oncogene 2004;23:7753-60.
19. Jönsson G, Paulie S, Grandien A. High level of cFLIP correlates with resistance to death receptor-induced apoptosis in bladder carcinoma cells. Anticancer Res 2003;23:1213-8.
20. Wang P, Zhang J, Bellail A, et al. Inhibition of RIP and c-FLIP enhances TRAIL-induced apoptosis in pancreatic cancer cells. Cell Signal 2007;9:2237-46.
21. Siegmund D, Hadwiger P, Pfizenmaier K, Vornlocher HP, Wajant H. Selective inhibition of FLICE-like inhibitory protein expression with small interfering RNA oligonucleotides is sufficient to sensitize tumor cells for TRAIL-induced apoptosis. Mol Med 2002;8:725-32.
22. Kim Y, Suh N, Sporn M, Reed JC. An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J Biol Chem 2002;277:22320-9.
23. El-Rayes BF, Zalupski MM, Shields AF, et al. A phase II study of celecoxib, gemcitabine, and cisplatin in advanced pancreatic cancer. Invest New Drugs 2005;23:583-90.
24. Chaturvedi PK, Bhui K, Shukla Y. Lupeol: connotations for chemoprevention. Cancer Lett 2008;263:1-13.
25. Saleem M, Alam A, Arifin S, Shah MS, Ahmed B, Sultana S. Lupeol, a triterpene, inhibits early responses of tumor promotion induced by benzoyl peroxide in murine skin. Pharmacol Res 2001;43:127-34.
26. Hasmeda M, Kweifio-Okai G, Macrides T, et al. Antiprotease effect of anti-inflammatory lupeol esters. Mol Cell Biochem 2003;252:97-101.
27. Rajic A, Kweifio-Okai G, Macrides T, Sandeman RM, Chandler DS, Polya GM. Inhibition of serine proteases by anti-inflammatory triterpenoids. Planta Med 2000;66:206-10.
28. Wada S, Iida A, Tanaka R. Triterpene constituents from the stem barks of Pinus luchuensis and their DNA topoisomerase II inhibitory effect. Planta Med 2001;67:659-64.
29. Saleem M, Kaur S, Kweon MH, Adhami VM, Afaq F, Mukhtar H. Lupeol, a fruit and vegetable based triterpene, induces apoptotic death of human pancreatic adenocarcinoma cells via inhibition of Ras signaling pathway. Carcinogenesis 2005;26:1956-64.
30. Saleem M, Maddodi N, Abu Zaid M, et al. Lupeol inhibits growth of highly aggressive human metastatic melanoma cells in vitro and in vivo by inducing apoptosis. Clin Cancer Res 2008;14:2119-27.
31. Saleem M, Kweon MH, Yun JM, et al. A novel dietary triterpene Lupeol induces fas-mediated apoptotic death of androgen-sensitive prostate cancer cells and inhibits tumor growth in a xenograft model. Cancer Res 2005;65:11203-13.
32. Saleem M, Adhami VM, Zhong W, et al. A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol Biomarkers Prev 2006;15:217-27.
33. 3H]arabinothymidine, and cell-analysis in 22 asynchronously growing tumor cell lines. Nucl Med Biol 2002;29:281-7.
34. Kwok CF, Juan CC, Shih KC, Hwu CM, Jap TS, Ho LT. Insulin-like growth factor-1 increases endothelin receptor A levels and action in cultured rat aortic smooth muscle cells. J Cell Biochem 2005;94:1126-34.
35. Bao Q, Shi Y. Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ 2007;14:56-65.
36. Kim PK, Mahidhara R, Seol DW. The role of caspase-8 in resistance to cancer chemotherapy. Drug Resist Updat 2001;4:293-6.
37. Kruidering M, Evan GI. Caspase-8 in apoptosis: the beginning of "the end"? IUBMB Life 2000;50:85-90.
38. Lázcoz P, Muñoz J, Nistal M, Pestaña A, Encío I, Castresana JS. Frequent promoter hypermethylation of RASSF1A and CASP8 in neuroblastoma. BMC Cancer 2006;6:254.
39. Margetts CD, Astuti D, Gentle DC, et al. Epigenetic analysis of HIC1, CASP8, FLIP, TSP1, DCR1, DCR2, DR4, DR5, KvDMR1, H19 and preferential 11p15.5 maternal-allele loss in von Hippel-Lindau and sporadic phaeochromocytomas. Endocr Relat Cancer 2005;12:161-72.
40. Kataoka T. The caspase-8 modulator c-FLIP. Crit Rev Immunol 2005;25:31-58.
41. Sartorius U, Schmitz I, Krammer PH. Molecular mechanisms of death-receptor-mediated apoptosis. Chembiochem 2001;2:20-9.
42. Roth W, Reed JC. FLIP protein and TRAIL-induced apoptosis. Vitam Horm 2004;67:189-206.
43. Wajant H. Targeting the FLICE Inhibitory Protein (FLIP) in cancer therapy. Mol Interv 2003;3:124-7.
44. Sarkar FH, Adsule S, Li Y, Padhye S. Back to the future: COX-2 inhibitors for chemoprevention and cancer therapy. Mini Rev Med Chem 2007;7:599-608.
45. Burke YD, Ayoubi AS, Werner SR, et al. Effects of the isoprenoids perillyl alcohol and farnesol on apoptosis biomarkers in pancreatic cancer chemoprevention. Anticancer Res 2002;22:3127-34.
46. Duiker EW, Mom CH, de Jong S, et al. The clinical trail of TRAIL. Eur J Cancer 2006;42:2233-40.
47. Eggert A, Grotzer MA, Zuzak TJ, et al. Resistance to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in neuroblastoma cells correlates with a loss of caspase-8 expression. Cancer Res 2001;61:1314-9.
48. Krueger A, Baumann S, Krammer PH, Kirchhoff S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 2001;21:8247-54.
49. Ivanov VN, Hei TK. Sodium arsenite accelerates TRAIL-mediated apoptosis in melanoma cells through up-regulation of TRAIL-R1/R2 surface levels and downregulation of cFLIP expression. Exp Cell Res 2006;312:4120-38.