Dihydroartemisinin enhances Apo2l/TRAIL-mediated apoptosis in pancreatic cancer cells via ROS-mediated up-regulation of death receptor 5

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Kong, Rui ^a   Jia, Guang ^a   Cheng, Zhuo xin ^a   Wang, Yong wei ^a   Mu, Ming ^b   Wang, Shuang jia ^a   Pan, Shang ha ^a   Gao, Yue ^a   Jiang, Hong chi ^a   Dong, De li ^c   Sun, Bei ^a  

^a THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; DEATH RECEPTOR 5; DIHYDROARTEMISININ; REACTIVE OXYGEN METABOLITE; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SMALL INTERFERING RNA; ANTINEOPLASTIC AGENT; ARTEMISININ DERIVATIVE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; COMBINATION CHEMOTHERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MONOTHERAPY; MOUSE; NONHUMAN; PANCREAS CANCER; RECEPTOR UPREGULATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARTEMISININS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION;

EID: 84861586454     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037222     Document Type: Article

References (54)

1. Raraty MG, Magee CJ, Ghaneh P, Neoptolemos JP, (2002) New techniques and agents in the adjuvant therapy of pancreatic cancer. Acta Oncol 41: 582-595.
2. Beger HG, Rau B, Gansauge F, Poch B, Link KH, (2003) Treatment of pancreatic cancer: Challenge of the facts. World J Surg 27: 1075-1084.
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
4. Meshnick SR, (2002) Artemisinin: mechanisms of action, resistance and toxicity. Int J Parasitol 32: 1655-1660.
5. O'Neill PM, Posner GH, (2004) A medicinal chemistry perspective on artemisinin and related endoperoxides. J Med Chem 47: 2945-2964.
6. Woerdenbag HJ, Pras N, van Uden W, Wallaart TE, Beekman AC, et al. (1994) Progress in the research of artemisinin-related antimalarials: an update. Pharm World Sci 16: 169-180.
7. Singh NP, Lai H, (2001) Selective toxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci 70: 49-56.
8. Disbrow GL, Baege AC, Kierpiec KA, Yuan H, Centeno JA, et al. (2005) Dihydroartemisinin Is Cytotoxic to Papillomavirus-Expressing Epithelial Cells In vitro and In vivo. Cancer Res 65: 10854-10861.
9. Chen H, Sun B, Pan S, Jiang H, Sun X, (2009) Dihydroartemisinin inhibits growth of pancreatic cancer cells in vitro and in vivo. Anticancer Drugs 20: 131-140.
10. Mu D, Zhang W, Chu D, Liu T, Xie Y, et al. (2008) The role of calcium, P38 MAPK in dihydroartemisinin-induced apoptosis of lung cancer PC-14 cells. Cancer Chemother Pharmacol 61: 639-645.
11. Nam W, Tak J, Ryu JK, Jung M, Yook JI, et al. (2007) Effects of artemisinin and its derivatives on growth inhibition and apoptosis of oral cancer cells. Head Neck 29: 335-340.
12. He Q, Shi J, Shen XL, An J, Sun H, et al. (2010) Dihydroartemisinin upregulates death receptor 5 expression and cooperates with TRAIL to induce apoptosis in human prostate cancer cells. Cancer Biol Ther 9: 819-824.
13. Singh NP, Lai HC, (2004) Artemisinin induces apoptosis in human cancer cells. Anticancer Res 24: 2277-2280.
14. Van Agtmael MA, Eggelte TA, Van Boxtel CJ, (1999) Artemisinin drugs in the treatment of malaria: from medicinal herb to registered medication. Trends Pharmacol Sci 20: 199-205.
15. Shterman N, Kupfer B, Moroz C, (1991) Comparison of transferrin receptors, iron content and isoferritin profile in normal and malignant human breast cell lines. Pathobiology 59: 19-25.
16. Kim SJ, Kim MS, Lee JW, Lee CH, Yoo H, et al. (2006) Dihydroartemisinin enhances radiosensitivity of human glioma cells in vitro. J Cancer Res Clin Oncol 132: 129-135.
17. Sprick MR, Weigand MA, Rieser E, Rauch CT, Juo P, et al. (2000) FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 12: 599-609.
18. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, et al. (2000) Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 12: 611-620.
19. Wu GS, (2009) TRAIL as a target in anti-cancer therapy. Cancer Lett 285: 1-5.
20. Yodkeeree S, Sung B, Limtrakul P, Aggarwal BB, (2009) Zerumbone enhances TRAIL-Induced apoptosis through the induction of death receptors in human colon cancer cells: Evidence for an essential role of reactive oxygen species. Cancer Res 69: 6581-6589.
21. Sung B, Park B, Yadav VR, Aggarwal BB, (2010) 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.
22. Yasui H, Adachi M, Hamada H, Imai K, (2005) Adenovirus-mediated gene transfer of caspase-8 sensitizes human adenocarcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand. Int J Oncol 26: 537-544.
23. Trauzold A, Schmiedel S, Sipos B, Wermann H, Westphal S, et al. (2003) PKCmu prevents CD95-mediated apoptosis and enhances proliferation in pancreatic tumour cells. Oncogene 22: 8939-8947.
24. Vogler M, Dürr K, Jovanovic M, Debatin KM, Fulda S, (2007) Regulation of TRAIL-induced apoptosis by XIAP in pancreatic carcinoma cells. Oncogene 26: 248-257.
25. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, et al. (2008) Targeting XIAP bypasses Bcl-2-mediated resistance to TRAIL and cooperates with TRAIL to suppress pancreatic cancer growth in vitro and in vivo. Cancer Res 68: 7956-7965.
26. Prasad S, Ravindran J, Sung B, Pandey MK, Aggarwal BB, (2010) Garcinol potentiates TRAIL-induced apoptosis through modulation of death receptors and antiapoptotic proteins. Mol Cancer Ther 9: 856-868.
27. Huang S, Okumura K, Sinicrope FA, (2009) BH3 Mimetic Obatoclax Enhances TRAIL-Mediated Apoptosis in Human Pancreatic Cancer Cells. Clin Cancer Res 15: 150-159.
28. Mizutani Y, Nakao M, Ogawa O, Yoshida O, Bonavida B, et al. (2001) Enhanced sensitivity of bladder cancer cells to tumor necrosis factor related apoptosis inducing ligand mediated apoptosis by cisplatin and carboplatin. J Urol 165: 263-270.
29. Yasuda T, Yoshida T, Goda AE, Horinaka M, Yano K, et al. (2008) Anti-Gout Agent Allopurinol Exerts Cytotoxicity to Human Hormone-Refractory Prostate Cancer Cells in Combination with Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand. Mol Cancer Res 6: 1852-1860.
30. Wang SJ, Gao Y, Chen H, Kong R, Jiang HC, et al. (2010) Dihydroartemisinin inactivates NF-kappaB and potentiates the anti-tumor effect of gemcitabine on pancreatic cancer both in vitro and in vivo. Cancer Lett 293: 99-108.
31. Lu YY, Chen TS, Qu JL, Pan WL, Sun L, et al. (2009) Dihydroartemisinin (DHA) induces caspase-3-dependent apoptosis in human lung adenocarcinoma ASTC-a-1 cells. J Biomed Sci 16: 16.
32. Hou J, Wang D, Zhang R, Wang H, (2008) Experimental Therapy of Hepatoma with Artemisinin and Its Derivatives: In vitro and In vivo Activity, Chemosensitization, and Mechanisms of Action. Clin Cancer Res 14: 5519-5530.
33. White SJ, Kasman LM, Kelly MM, Lu P, Spruill L, et al. (2007) Doxorubicin generates a proapoptotic phenotype by phosphorylation of elongation factor 2. Free Radic Biol Med 43: 1313-1321.
34. White-Gilbertson SJ, Kasman L, McKillop J, Tirodkar T, Lu P, et al. (2009) Oxidative stress sensitizes bladder cancer cells to TRAIL-mediated apoptosis by down-regulating anti-apoptotic proteins. J Urol 182: 1178-1185.
35. Schumacker PT, (2006) Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10: 175-176.
36. Chandra J, (2009) Oxidative stress by targeted agents promotes cytotoxicity in hematologic malignancies. Antioxid Redox Signal 11: 1123-1137.
37. Gina Manda, Marina Tamara Nechifor, Teodora-Monica Neagu, (2009) Reactive Oxygen Species, Cancer and Anti-Cancer Therapies. Curr Chem Biol 3: 22-46.
38. Hien TT, White NJ, (1993) Qinghaosu. Lancet 341: 603-608.
39. Posner GH, O'Neill PM, (2004) Knowledge of the proposed chemical mechanism of action and cytochrome P450 metabolism of antimalarial trioxanes like artemisinin allows rational design of new antimalarial peroxides. Acc Chem Res 37: 397-404.
40. Cabello CM, Lamore SD, Bair WB 3rd, Qiao S, Azimian S, et al. (2011) The redox antimalarial dihydroartemisinin targets human metastatic melanoma cells but not primary melanocytes with induction of NOXA-dependent apoptosis. Invest New Drugs [Epub ahead of print].
41. Izeradjene K, Douglas L, Tillman DM, Delaney AB, Houghton JA, (2005) Reactive oxygen species regulate caspase activation in tumor necrosis factor-related apoptosis-inducing ligand-resistant human colon carcinoma cell lines. Cancer Res 65: 7436-7445.
42. Hengartner MO, (2000) The biochemistry of apoptosis. Nature 407: 770-776.
43. Fulda S, (2009) Apoptosis pathways and their therapeutic exploitation in pancreatic cancer. J Cell Mol Med 13: 1221-1227.
44. Chen T, Li M, Zhang R, Wang H, (2009) Dihydroartemisinin induces apoptosis and sensitizes human ovarian cancer cell. J Cell Mol Med 13: 1358-1370.
45. Yang X, Merchant MS, Romero ME, Tsokos M, Wexler LH, et al. (2003) Induction of caspase 8 by interferon γ renders some neuroblastoma (NB) cells sensitive to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) but reveals that a lack of membrane TR1/TR2 also contributes to TRAIL resistance in NB. Cancer Res 63: 1122-1129.
46. Schüler S, Fritsche P, Diersch S, Arlt A, Schmid RM, et al. (2010) Research HDAC2 attenuates TRAIL-induced apoptosis of pancreatic cancer cells. Mol Cancer 9: 80.
47. Jung EM, Lim JH, Lee TJ, Park JW, Choi KS, et al. (2005) Curcumin sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis through reactive oxygen species-mediated upregulation of death receptor 5 (DR5). Carcinogenesis 26: 1905-1913.
48. Kim H, Kim EH, Eom YW, Kim WH, Kwon TK, et al. (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.
49. Shiraishi T, Yoshida T, Nakata S, Horinaka M, Wakada M, et al. (2005) Tunicamycin Enhances Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand-Induced Apoptosis in Human Prostate Cancer Cells. Cancer Res 65: 6364-6370.
50. Kim YH, Jung EM, Lee TJ, Kim SH, Choi YH, et al. (2008) Rosiglitazone promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP. Free Radic Biol Med 44: 1055-1068.
51. Chou TC, Talalay P, (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55.
52. Chou TC, (2010) Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 70: 440-446.
53. Wang S, Ei-Deiry WS, (2003) Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci USA 100: 15095-15100.
54. Kong R, Sun B, Jiang H, Pan S, Chen H, et al. (2010) Downregulation of nuclear factor-kappaB p65 subunit by small interfering RNA synergizes with gemcitabine to inhibit the growth of pancreatic cancer. Cancer Lett 291: 90-98.