Artesunate induces G2/M cell cycle arrest through autophagy induction in breast cancer cells

Anti-Cancer Drugs

Volumn 25, Issue 6, 2014, Pages 652-662

  Chen, Kai ^a   Shou, Liu Mei ^a   Lin, Fang ^b   Duan, Wei Ming ^a   Wu, Meng Yao ^a   Xie, Xin ^a   Xie, Yu Feng ^a   Li, Wei ^a   Tao, Min ^a,c  

^a THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c Institute of Clinical Immunology of Jiangsu Province   (China)

Author keywords

Artesunate; Autophagy; Breast cancer; Cell cycle

Indexed keywords

ARTESUNATE; BECLIN 1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DOCETAXEL; EPIRUBICIN; MESSENGER RNA; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; ARTEMISININ DERIVATIVE; BECN1 PROTEIN, HUMAN; MEMBRANE PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BREAST CANCER; BREAST CANCER CELL LINE; CANCER CELL; CELL VIABILITY; CHEMOSENSITIZATION; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MDA MB 231 CELL LINE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; BREAST TUMOR; DRUG EFFECTS; FEMALE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS REGULATORY PROTEINS; ARTEMISININS; AUTOPHAGY; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG SYNERGISM; EPIRUBICIN; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MEMBRANE PROTEINS;

EID: 84901622826     PISSN: 09594973     EISSN: 14735741     Source Type: Journal    
DOI: 10.1097/CAD.0000000000000089     Document Type: Article

References (63)

1. Efferth T. Willmar Schwabe Award 2006: Antiplasmodial and antitumor activity of artemisinin-from bench to bedside. Planta Med 2007; 73:299-309. (Pubitemid 46910410)
2. Taylor WR, White NJ. Antimalarial drug toxicity: A review. Drug Saf 2004; 27:25-61. (Pubitemid 38186936)
3. Jiang Z, Chai J, Chuang HH, Li S, Wang T, Cheng Y, et al. Artesunate induces G0/G1 cell cycle arrest and iron-mediated mitochondrial apoptosis in A431 human epidermoid carcinoma cells. Anticancer Drugs 2012; 23:606-613.
4. Li PC, Lam E, Roos WP, Zdzienicka MZ, Kaina B, Efferth T. Artesunate derived from traditional Chinese medicine induces DNA damage and repair. Cancer Res 2008; 68:4347-4351.
5. Berdelle N, Nikolova T, Quiros S, Efferth T, Kaina B. Artesunate induces oxidative DNA damage, sustained DNA double-strand breaks, and the ATM/ATR damage response in cancer cells. Mol Cancer Ther 2011; 10:2224-2233.
6. Chen HH, Zhou HJ, Fang X. Inhibition of human cancer cell line growth and human umbilical vein endothelial cell angiogenesis by artemisinin derivatives in vitro. Pharmacol Res 2003; 48:231-236. (Pubitemid 36818928)
7. Dell'Eva R, Pfeffer U, Vene R, Anfosso L, Forlani A, Albini A, et al. Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial artesunate. Biochem Pharmacol 2004; 68:2359-2366. (Pubitemid 39535108)
8. Huan-huan C, Li-Li Y, Shang-Bin L. Artesunate reduces chicken chorioallantoic membrane neovascularisation and exhibits antiangiogenic and apoptotic activity on human microvascular dermal endothelial cell. Cancer Lett 2004; 211:163-173. (Pubitemid 38824630)
9. Anfosso L, Efferth T, Albini A, Pfeffer U. Microarray expression profiles of angiogenesis-related genes predict tumor cell response to artemisinins. Pharmacogenomics J 2006; 6:269-278. (Pubitemid 44137954)
10. Efferth T, Olbrich A, Bauer R. mRNA expression profiles for the response of human tumor cell lines to the antimalarial drugs artesunate, arteether, and artemether. Biochem Pharmacol 2002; 64:617-623.
11. Efferth T, Sauerbrey A, Olbrich A, Gebhart E, Rauch P, Weber HO, et al. Molecular modes of action of artesunate in tumor cell lines. Mol Pharmacol 2003; 64:382-394. (Pubitemid 36910002)
12. Efferth T, Giaisi M, Merling A, Krammer PH, Li-Weber M. Artesunate induces ROS-mediated apoptosis in doxorubicin-resistant T leukemia cells. PloS one 2007; 2:e693.
13. Steinbruck L, Pereira G, Efferth T. Effects of artesunate on cytokinesis and G(2)/M cell cycle progression of tumour cells and budding yeast. Cancer Genomics Proteomics 2010; 7:337-346.
14. Zhao Y, Jiang W, Li B, Yao Q, Dong J, Cen Y, et al. Artesunate enhances radiosensitivity of human non-small cell lung cancer A549 cells via increasing NO production to induce cell cycle arrest at G2/M phase. Int Immunopharmacol 2011; 11:2039-2046.
15. Eichhorn T,Winter D, Buchele B, Dirdjaja N, Frank M, Lehmann WD, et al. Molecular interaction of artemisinin with translationally controlled tumor protein (TCTP) of Plasmodium falciparum. Biochem Pharmacol 2013; 85:38-45.
16. Pandey AV, Tekwani BL, Singh RL, Chauhan VS. Artemisinin, an endoperoxide antimalarial, disrupts the hemoglobin catabolism and heme detoxification systems in malarial parasite. J Biol Chem 1999; 274:19383-19388.
17. Mizushima N. Autophagy: Process and function. Genes Dev 2007; 21:2861-2873. (Pubitemid 350133435)
18. Hamacher-Brady A, Stein HA, Turschner S, Toegel I, Mora R, Jennewein N, et al. Artesunate activates mitochondrial apoptosis in breast cancer cells via iron-catalyzed lysosomal reactive oxygen species production. J Biol Chem 2011; 286:6587-6601.
19. Zhu BS, Xing CG, Lin F, Fan XQ, Zhao K, Qin ZH. Blocking NF-kappaB nuclear translocation leads to p53-related autophagy activation and cell apoptosis. World J Gastroenterol 2011; 17:478-487.
20. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2001; 2:330-335. (Pubitemid 32401529)
21. Negri T, Tarantino E, Orsenigo M, Reid JF, Gariboldi M, Zambetti M, et al. Chromosome band 17q21 in breast cancer: Significant association between beclin 1 loss and HER2/NEU amplification. Genes Chromosomes Cancer 2010; 49:901-909.
22. Wang W, Fan H, Zhou Y, Duan P, Zhao G,Wu G. Knockdown of autophagyrelated gene BECLIN1 promotes cell growth and inhibits apoptosis in the A549 human lung cancer cell line. Mol Med Rep 2013; 7:1501-1505.
23. Shen Y, Liang LZ, Hong MH, Xiong Y,Wei M, Zhu XF. Expression and clinical significance of microtubule-Associated protein 1 light chain 3 (LC3) and Beclin1 in epithelial ovarian cancer. Ai zheng 2008; 27:595-599.
24. Chang SH, Minai-Tehrani A, Shin JY, Park S, Kim JE, Yu KN, et al. Beclin1-induced autophagy abrogates radioresistance of lung cancer cells by suppressing osteopontin. J Radiat Res 2012; 53:422-432.
25. Sun Y, Liu JH, Sui YX, Jin L, Yang Y, Lin SM, et al. Beclin1 overexpression inhibitis proliferation, invasion and migration of CaSki cervical cancer cells. Asian Pac J Cancer Prev 2011; 12:1269-1273.
26. Sun Y, Liu JH, Jin L, Lin SM, Yang Y, Sui YX, et al. Over-expression of the Beclin1 gene upregulates chemosensitivity to anti-cancer drugs by enhancing therapy-induced apoptosis in cervix squamous carcinoma CaSki cells. Cancer Lett 2010; 294:204-210.
27. Duan ZL, Peng ZL,Wang ZH. Growth inhibitory effects of Beclin1 gene on epithelial ovarian cancer SKOV3 cells. Nan Fang Yi Ke Da Xue Xue Bao 2010; 30:672-676.
28. Efferth T, Ramirez T, Gebhart E, Halatsch ME. Combination treatment of glioblastoma multiforme cell lines with the anti-malarial artesunate and the epidermal growth factor receptor tyrosine kinase inhibitor OSI-774. Biochem Pharmacol 2004; 67:1689-1700. (Pubitemid 38479847)
29. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-676. (Pubitemid 129516338)
30. Torricelli C, Salvadori S, Valacchi G, Soucek K, Slabakova E, Muscettola M, et al. Alternative pathways of cancer cell death by Rottlerin: Apoptosis versus autophagy. Evid Based Complement Alternat Med 2012; 2012:980658.
31. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell J. Evaluation of a tetrazolium-based semiautomated colorimetric assay: Assessment of chemosensitivity testing. Cancer Res 1987; 47:936-942. (Pubitemid 17027905)
32. Li W, Xie L, Chen Z, Zhu Y, Sun Y, Miao Y, et al. Cantharidin, a potent and selective PP2A inhibitor, induces an oxidative stress-independent growth inhibition of pancreatic cancer cells through G2/M cell-cycle arrest and apoptosis. Cancer Sci 2010; 101:1226-1233.
33. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-175. (Pubitemid 351231180)
34. Chen Y, Azad MB, Gibson SB. Methods for detecting autophagy and determining autophagy-induced cell death. Can J Physiol Pharmacol 2010; 88:285-295.
35. Geng QR, Xu DZ, He LJ, Lu JB, Zhou ZW, Zhan YQ, et al. Beclin-1 expression is a significant predictor of survival in patients with lymph node-positive gastric cancer. PloS One 2012; 7:e45968.
36. Debnath J. The multifaceted roles of autophagy in tumors-implications for breast cancer. J Mammary Gland Biol Neoplasia 2011; 16:173-187.
37. Van Den Heuvel S. Cell-cycle regulation. Worm Book 2005; 21:1-16.
38. Stark GR, Taylor WR. Control of the G2/M transition. Mol Biotechnol 2006; 32:227-248.
39. Li X, Wang J, Ye Z, Li JC. Oridonin up-regulates expression of P21 and induces autophagy and apoptosis in human prostate cancer cells. Int J Biol Sci 2012; 8:901-912.
40. Ouyang DY, Zeng LH, Pan H, Xu LH,Wang Y, Liu KP, et al. Piperine inhibits the proliferation of human prostate cancer cells via induction of cell cycle arrest and autophagy. Food Chem Toxicol 2013; 60:424-430.
41. Efferth T, Briehl MM, Tome ME. Role of antioxidant genes for the activity of artesunate against tumor cells. Int J Oncol 2003; 23:1231-1235.
42. Efferth T, Benakis A, Romero MR, Tomicic M, Rauh R, Steinbach D, et al. Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron. Free Radic Biol Med 2004; 37:998-1009. (Pubitemid 39164582)
43. Kelter G, Steinbach D, Konkimalla VB, Tahara T, Taketani S, Fiebig HH, et al. Role of transferrin receptor and the ABC transporters ABCB6 and ABCB7 for resistance and differentiation of tumor cells towards artesunate. PloS One 2007; 2:e798.
44. Mercer AE, Copple IM, Maggs JL, O'Neill PM, Park BK. 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 2011; 286:987-996.
45. Efferth T, Rucker G, Falkenberg M, Manns D, Olbrich A, Fabry U, et al. Detection of apoptosis in KG-1a leukemic cells treated with investigational drugs. Arzneimittelforschung 1996; 46:196-200. (Pubitemid 26079152)
46. Li S, Xue F, Cheng Z, Yang X,Wang S, Geng F, Pan L. Effect of artesunate on inhibiting proliferation and inducing apoptosis of SP2/0 myeloma cells through affecting NFkappaB p65. Int J Hematol 2009; 90:513-521.
47. Ramacher M, Umansky V, Efferth T. Effect of artesunate on immune cells in ret-Transgenic mouse melanoma model. Anticancer Drugs 2009; 20:910-917.
48. Thanaketpaisarn O, Waiwut P, Sakurai H, Saiki I. Artesunate enhances TRAIL-induced apoptosis in human cervical carcinoma cells through inhibition of the NF-kappaB and PI3K/Akt signaling pathways. Int J Oncol 2011; 39:279-285.
49. Wu GD, Zhou HJ, Wu XH. Apoptosis of human umbilical vein endothelial cells induced by artesunate. Vascul Pharmacol 2004; 41:205-212.
50. Yu HC, Lin CS, Tai WT, Liu CY, Shiau CW, Chen KF. Nilotinib induces autophagy in hepatocellular carcinoma through AMPK activation. J Biol Chem 2013; 288:18249-18259.
51. Roy S, Debnath J. Autophagy and tumorigenesis. Semin Immunopathol 2010; 32:383-396.
52. Bao XX, Xie BS, Li Q, Li XP, Wei LH, Wang JL. Nifedipine induced autophagy through Beclin1 and mTOR pathway in endometrial carcinoma cells. Chin Med J (Engl) 2012; 125:3120-3126.
53. Kang MR, Kim MS, Oh JE, Kim YR, Song SY, Kim SS, et al. Frameshift mutations of autophagy-related genes ATG2B, ATG5, ATG9B and ATG12 in gastric and colorectal cancers with microsatellite instability. J Pathol 2009; 217:702-706.
54. Capparelli C, Chiavarina B, Whitaker-Menezes D, Pestell TG, Pestell RG, Hulit J, et al. CDK inhibitors (p16/p19/p21) induce senescence and autophagy in cancer-Associated fibroblasts, 'fueling' tumor growth via paracrine interactions, without an increase in neo-Angiogenesis. Cell Cycle 2012; 11:3599-3610.
55. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010; 465:942-946.
56. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-580.
57. He C, Levine B. The Beclin 1 interactome. Curr Opin Cell Biol 2010; 22:140-149.
58. Mao ZG, Zhou J, Wang H, He DS, Xiao WW, Liao GZ, et al. Artesunate inhibits cell proliferation and decreases growth hormone synthesis and secretion in GH3 cells. Mol Biol Rep 2012; 39:6227-6234.
59. Andreopoulou E, Sparano JA. Chemotherapy in patients with anthracyclineand taxane-pretreated metastatic breast cancer: An overview. Curr Breast Cancer Rep 2013; 5:42-50.
60. Thundimadathil J. Cancer treatment using peptides: Current therapies and future prospects. J Amino Acids 2012; 2012:967347.
61. Efferth T, Davey M, Olbrich A, Rucker G, Gebhart E, Davey R. Activity of drugs from traditional Chinese medicine toward sensitive and MDR1-or MRP1-overexpressing multidrug-resistant human CCRF-CEM leukemia cells. Blood Cells Mol Dis 2002; 28:160-168. (Pubitemid 34743750)
62. Millour J, de Olano N, Horimoto Y, Monteiro LJ, Langer JK, Aligue R, et al. ATM and p53 regulate FOXM1 expression via E2F in breast cancer epirubicin treatment and resistance. Mol Cancer Ther 2011; 10:1046-1058.
63. Fung C, Chen X, Grandis JR, Duvvuri U. EGFR tyrosine kinase inhibition induces autophagy in cancer cells. Cancer Biol Ther 2012; 13:1417-1424..