Synergistic induction of apoptosis in A549 cells by dihydroartemisinin and gemcitabine

Apoptosis

Volumn 19, Issue 4, 2014, Pages 668-681

  Zhao, Chubiao ^a   Gao, Weijie ^a   Chen, Tongsheng ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

Author keywords

Apoptosis; Bak; Dihydroartemisinin; Fas; Gemcitabine; Synergistic action

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; DIHYDROARTEMISININ; GEMCITABINE; PROTEIN BAK; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; ARTEMISININ DERIVATIVE; BAK1 PROTEIN, HUMAN; DEOXYCYTIDINE; FAS ANTIGEN; FAS PROTEIN, HUMAN; PROTEIN BAX;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DRUG EFFICACY; DRUG POTENTIATION; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; DRUG EFFECTS; G2 PHASE CELL CYCLE CHECKPOINT; METABOLISM; TUMOR CELL LINE;

ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; ARTEMISININS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; DEOXYCYTIDINE; DRUG SYNERGISM; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84896388339     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0953-0     Document Type: Article

References (45)

1. Wang SJ, Gao Y, Chen H, Kong R, Jiang HC et al (2010) Dihydroartemisinin inactivates NF-κB and potentiates the anti-tumor effect of gemcitabine on pancreatic cancer both in vitro and in vivo. Cancer Lett 293:99-108
2. Denlinger CE, Rundall BK, Keller MD, Jones DR (2004) Proteasome inhibition sensitizes non-small-cell lung cancer to gemcitabine-induced apoptosis. Ann Thorac Surg 78:1207-1214
3. Arlt A, Gehrz A, Müerköster S, Vorndamm J, Kruse ML et al (2003) Role of NF-κB and Akt/PI3 K in the resistance of pancreatic carcinoma cell lines against gemcitabine-induced cell death. Oncogene 22:3243-3251
4. Zhou J, Chen ZM, Malysa A, Li X, Oliveira P et al (2013) A kinome screen identifies checkpoint kinase 1 (CHK1) as a sensitizer for RRM1-dependent gemcitabine efficacy. PLoS One 8:e58091
5. Dalla Pozza E, Fiorini C, Dando I, Menegazzi M, Sgarbossa A et al (2012) Role of mitochondrial uncoupling protein 2 in cancer cell resistance to gemcitabine. Biochim Biophys Acta 1823:1856-1863
6. Kanai M, Yoshimura K, Asada M, Imaizumi A, Suzuki C et al (2011) A phase I/II study of gemcitabine-based chemotherapy plus curcumin for patients with gemcitabine-resistant pancreatic cancer. Cancer Chemother Pharm 68:157-164
7. Hou J, Wang DS, Zhang RW, 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
8. Chen TS, Chen M, Chen JQ (2013) Ionizing radiation potentiates dihydroartemisinin-induced apoptosis of A549 cells via a caspase-8-dependent pathway. PLoS One 8:e59827
9. Rasheed SAK, Efferth T, Asangani IA, Allgayer H (2010) First evidence that the antimalarial drug artesunate inhibits invasion and in vivo metastasis in lung cancer by targeting essential extracellular proteases. Int J Cancer 127:1475-1485
10. Chen T, Li M, Zhang RW, Wang H (2009) Dihydroartemisinin induces apoptosis and sensitizes human ovarian cancer cells to carboplatin therapy. J Cell Mol Med 13:1358-1370
11. Mercer AE, Maggs JL, Sun XM, Cohen GM, Chadwick J et al (2007) Evidence for the involvement of carbon-centered radicals in the induction of apoptotic cell death by artemisinin compounds. J Biol Chem 282:9372-9382
12. Zhang CZ, Pan YH, Cao Y, Lai PB, Liu LL et al (2012) Histone deacetylase inhibitors facilitate dihydroartemisinin-induced apoptosis in liver cancer in vitro and in vivo. PLoS One 7:e39870
13. Gravett AM, Liu WM, Krishna S, Chan WC, Haynes RK et al (2011) In vitro study of the anti-cancer effects of artemisone alone or in combination with other chemotherapeutic agents. Cancer Chemoth Pharm 67:569-577
14. Liu WM, Gravett AM, Dalgleish AG (2011) The antimalarial agent artesunate possesses anticancer properties that can be enhanced by combination strategies. Int J Cancer 128:1471-1480
15. Berdelle N, Nikolova T, Quiros S, Efferth T, Kaina B (2011) Artesunate induces oxidative DNA damage, sustained DNA double-strand breaks, and the ATM/ATR damage response in cancer cells. Mol Cancer Ther 10:2224-2233
16. Gao WJ, Xiao FL, Wang XP, Chen TS (2013) Artemisinin induces A549 cell apoptosis dominantly via a reactive oxygen species-mediated amplification activation loop among caspase-9, -8 and -3. Apoptosis. doi: 10.1007/s10495-013- 0857-z
17. Xiao FL, Gao WJ, Wang XP, Chen TS (2012) Amplification activation loop between caspase-8 and-9 dominates artemisinin-induced apoptosis of ASTC-a-1 cells. Apoptosis 17:600-611
18. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621-681
19. Zhou CJ, Pan WL, Wang XP, Chen TS (2012) Artesunate induces apoptosis via a Bak-mediated caspase-independent intrinsic pathway in human lung adenocarcinoma cells. J Cell Physiol 227:3778-3786
20. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305-1308
21. Kim H, Tu HC, Ren D, Takeuchi O, Jeffers JR et al (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 36:487-499
22. Westphal D, Dewson G, Czabotar PE, Kluck RM (2011) Molecular biology of Bax and Bak activation and action. Biochim Biophys Acta 1813:521-531
23. Pelicano H, Carney D, Huang P (2004) ROS stress in cancer cells and therapeutic implications. Drug Resist Update 7:97-110
24. Donadelli M, Costanzo C, Beghelli S, Scupoli MT, Dandrea M et al (2007) Synergistic inhibition of pancreatic adenocarcinoma cell growth by trichostatin A and gemcitabine. Biochim Biophys Acta 1773(7):1095-1106
25. Lu YY, Chen TS, Wang XP, Li L (2010) Single-cell analysis of dihydroartemisinin-induced apoptosis through reactive oxygen species-mediated caspase-8 activation and mitochondrial pathway in ASTC-a-1 cells using fluorescence imaging techniques. J Biomed Opt 15:046028
26. Mu D, Zhang W, Chu D et al (2008) The role of calcium, P38 MAPK in dihydroartemisinin-induced apoptosis of lung cancer PC-14 cells. Cancer Chemother Pharmacol 61(4):639-645
27. Chen H, Sun B, Pan S et al (2009) Dihydroartemisinin inhibits growth of pancreatic cancer cells in vitro and in vivo. Anticancer Drugs 20(2):131-140
28. Aung W, Sogawa C, Furukawa T et al (2011) Anticancer effect of dihydroartemisinin (DHA) in a pancreatic tumor model evaluated by conventional methods and optical imaging. Anticancer Res 31(5):1549-1558
29. Wang SJ, Sun B, Cheng ZX et al (2011) Dihydroartemisinin inhibits angiogenesis in pancreatic cancer by targeting the NF-κB pathway. Cancer Chemother Pharmacol 68(6):1421-1430
30. Chang GC, Hsu SL, Tsai JR et al (2004) Extracellular signal-regulated kinase activation and Bcl-2 downregulation mediate apoptosis after gemcitabine treatment partly via a p53-independent pathway. Eur J Pharmacol 502(3):169-183
31. Ng SSW, Tsao MS, Chow S et al (2000) Inhibition of phosphatidylinositide 3-kinase enhances gemcitabine-induced apoptosis in human pancreatic cancer cells. Cancer Res 60(19):5451-5455
32. Nakashima M, Adachi S, Yasuda I et al (2011) Phosphorylation status of heat shock protein 27 plays a key role in gemcitabine-induced apoptosis of pancreatic cancer cells. Cancer Lett 313(2):218-225
33. Vandana M, Sahoo SK (2010) Long circulation and cytotoxicity of PEGylated gemcitabine and its potential for the treatment of pancreatic cancer. Biomaterials 31(35):9340-9356
34. Efferth T (2006) Molecular pharmacology and pharmacogenomics of artemisinin and its derivatives in cancer cells. Curr Drug Targets 7:407-421
35. Beekman AC, Wierenga PK, Woerdenbag HJ, Van Uden W, Pras N et al (1998) Artemisinin-derived sesquiterpene lactones as potential antitumour compounds: cytotoxic action against bone marrow and tumour cells. Planta Med 64:615-619
36. Mercer AE, Copple IM, Maggs JL, O'Neill PM, Park BK (2011) The role of heme and the mitochondrion in the chemical and molecular mechanisms of mammalian cell death induced by the artemisinin antimalarials. J Biol Chem 286:987-996
37. Firestone GL, Sundar SN (2009) Anticancer activities of artemisinin and its bioactive derivatives. Expert Rev Mol Med 11:e32
38. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S (2002) Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 99:1259-1263
39. Lu YY, Chen TS, Wang XP, Qu JL, Chen M (2010) The JNK inhibitor SP600125 enhances dihydroartemisinin-induced apoptosis by accelerating Bax translocation into mitochondria in human lung adenocarcinoma cells. FEBS Lett 584:4019-4026
40. Ghibelli L, Diederich M (2010) Multistep and multitask Bax activation. Mitochondrion 10:604-613
41. Willis SN, Chen L, Dewson G, Wei A, Naik E et al (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Gene Dev 19:1294-1305
42. Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D et al (2011) Bcl-xL retrotranslocates Bax from the mitochondria into the cytosol. Cell 145:104-116
43. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC et al (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 6:1389-1399
44. Handrick R, Ontikatze T, Bauer KD, Freier F, Rübel A et al (2010) Dihydroartemisinin induces apoptosis by a Bak-dependent intrinsic pathway. Mol Cancer Ther 9:2497-2510
45. Krammer PH, Arnold R, Lavrik IN (2007) Life and death in peripheral T cells. Nat Rev Immunol 7:532-542