Gene expression profiling identifies novel key players involved in the cytotoxic effect of Artesunate on pancreatic cancer cells

Biochemical Pharmacology

Volumn 78, Issue 3, 2009, Pages 273-283

  Youns, Mahmoud ^a,c   Efferth, Thomas ^a   Reichling, Jürgen ^b   Fellenberg, Kurt ^a   Bauer, Andrea ^a   Hoheisel, Jörg D ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c Ein Helwan   (Egypt)

Author keywords

Artesunate; Ingenuity Pathway Analysis; Microarray; Pancreatic cancer; Topoisomerase

Indexed keywords

ARTESUNATE; CASPASE 3; CASPASE 7; COMPLEMENTARY DNA; TETRAZOLIUM;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PANCREAS CANCER; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARTEMISININS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 65749103049     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.04.014     Document Type: Article

References (49)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. Cancer statistics. CA Cancer J Clin 58 (2008) 71-96
2. Burris III H.A., Moore M.J., Andersen J., Green M.R., Rothenberg M.L., Modiano M.R., et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 15 (1997) 2403-2413
3. Burris H., and Storniolo A.M. Assessing clinical benefit in the treatment of pancreas cancer: gemcitabine compared to 5-fluorouracil. Eur J Cancer 33 Suppl 1 (1997) S18-22
4. Shore S., Vimalachandran D., Raraty M.G., and Ghaneh P. Cancer in the elderly: pancreatic cancer. Surg Oncol 13 (2004) 201-210
5. Saif M.W. Controversies in the adjuvant treatment of pancreatic adenocarcinoma. JOP 8 (2007) 545-552
6. Klayman D.L. Qinghaosu (artemisinin): an antimalarial drug from China. Science 228 (1985) 1049-1055
7. Price R.N. Artemisinin drugs: novel antimalarial agents. Expert Opin Investig Drugs 9 (2000) 1815-1827
8. Hien T.T., Phu N.H., Mai N.T., Chau T.T., Trang T.T., Loc P.P., et al. An open randomized comparison of intravenous and intramuscular artesunate in severe falciparum malaria. Trans R Soc Trop Med Hyg 86 (1992) 584-585
9. Hien T.T., and White N.J. Qinghaosu. Lancet 341 (1993) 603-608
10. Fishwick J., McLean W.G., Edwards G., and Ward S.A. The toxicity of artemisinin and related compounds on neuronal and glial cells in culture. Chem Biol Interact 96 (1995) 263-271
11. Efferth T., Dunstan H., Sauerbrey A., Miyachi H., and Chitambar C.R. The anti-malarial artesunate is also active against cancer. Int J Oncol 18 (2001) 767-773
12. Singh N.P., and Lai H. Selective toxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci 70 (2001) 49-56
13. 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 68 (2004) 2359-2366
14. Chen H.H., Zhou H.J., and Fang X. Inhibition of human cancer cell line growth and human umbilical vein endothelial cell angiogenesis by artemisinin derivatives in vitro. Pharmacol Res 48 (2003) 231-236
15. Li L.N., Zhang H.D., Yuan S.J., Tian Z.Y., Wang L., and Sun Z.X. Artesunate attenuates the growth of human colorectal carcinoma and inhibits hyperactive Wnt/beta-catenin pathway. Int J Cancer 121 (2007) 1360-1365
16. Efferth T., Sauerbrey A., Olbrich A., Gebhart E., Rauch P., Weber H.O., et al. Molecular modes of action of artesunate in tumor cell lines. Mol Pharmacol 64 (2003) 382-394
17. Zhang F., Gosser Jr. D.K., and Meshnick S.R. Hemin-catalyzed decomposition of artemisinin (qinghaosu). Biochem Pharmacol 43 (1992) 1805-1809
18. Efferth T., Benakis A., Romero M.R., Tomicic M., Rauh R., Steinbach D., et al. Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron. Free Radic Biol Med 37 (2004) 998-1009
19. Kelter G., Steinbach D., Konkimalla V.B., Tahara T., Taketani S., Fiebig H.H., et al. Role of transferrin receptor and the ABC transporters ABCB6 and ABCB7 for resistance and differentiation of tumor cells towards artesunate. PLoS ONE 2 (2007) e798
20. Anderson K.M., Seed T., Ou D., and Harris J.E. Free radicals and reactive oxygen species in programmed cell death. Med Hypotheses 52 (1999) 451-463
21. Efferth T., Giaisi M., Merling A., Krammer P.H., and Li-Weber M. Artesunate induces ROS-mediated apoptosis in doxorubicin-resistant T leukemia cells. PLoS ONE 2 (2007) e693
22. Jiao Y., Ge C.M., Meng Q.H., Cao J.P., Tong J., and Fan S.J. Dihydroartemisinin is an inhibitor of ovarian cancer cell growth. Acta Pharmacol Sin 28 (2007) 1045-1056
23. Konkimalla V.B., Blunder M., Korn B., Soomro S.A., Jansen H., Chang W., et al. Effect of artemisinins and other endoperoxides on nitric oxide-related signaling pathway in RAW 264.7 mouse macrophage cells. Nitric Oxide 19 (2008) 184-191
24. Li P.C., Lam E., Roos W.P., Zdzienicka M.Z., Kaina B., and Efferth T. Artesunate derived from traditional Chinese medicine induces DNA damage and repair. Cancer Res 68 (2008) 4347-4351
25. Beier V., Bauer A., Baum M., and Hoheisel J.D. Fluorescent sample labeling for DNA microarray analyses. Methods Mol Biol 283 (2004) 127-135
26. Esposito I., Bauer A., Hoheisel J.D., Kleeff J., Friess H., Bergmann F., et al. Microcystic tubulopapillary carcinoma of the pancreas: a new tumor entity?. Virchows Arch 444 (2004) 447-453
27. Fellenberg K., Hauser N.C., Brors B., Neutzner A., Hoheisel J.D., and Vingron M. Correspondence analysis applied to microarray data. Proc Natl Acad Sci USA 98 (2001) 10781-10786
28. Fellenberg K., Busold C.H., Witt O., Bauer A., Beckmann B., Hauser N.C., et al. Systematic interpretation of microarray data using experiment annotations. BMC Genomics 7 (2006) 319
29. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M.A., Lassota P., et al. Features of apoptotic cells measured by flow cytometry. Cytometry 13 (1992) 795-808
30. Igney F.H., and Krammer P.H. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2 (2002) 277-288
31. Brazma A., Hingamp P., Quackenbush J., Sherlock G., Spellman P., Stoeckert C., et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29 (2001) 365-371
32. Toyoda E., Kagaya S., Cowell I.G., Kurosawa A., Kamoshita K., Nishikawa K., et al. NK314, a topoisomerase II inhibitor that specifically targets the alpha isoform. J Biol Chem 283 (2008) 23711-23720
33. Hutt A.M., and Kalf G.F. Inhibition of human DNA topoisomerase II by hydroquinone and p-benzoquinone, reactive metabolites of benzene. Environ Health Perspect 104 Suppl 6 (1996) 1265-1269
34. Gantchev T.G., and Hunting D.J. The ortho-quinone metabolite of the anticancer drug etoposide (VP-16) is a potent inhibitor of the topoisomerase II/DNA cleavable complex. Mol Pharmacol 53 (1998) 422-428
35. Goan Y.G., Zhou B., Hu E., Mi S., and Yen Y. Overexpression of ribonucleotide reductase as a mechanism of resistance to 2,2-difluorodeoxycytidine in the human KB cancer cell line. Cancer Res 59 (1999) 4204-4207
36. Duxbury M.S., Ito H., Zinner M.J., Ashley S.W., and Whang E.E. RNA interference targeting the M2 subunit of ribonucleotide reductase enhances pancreatic adenocarcinoma chemosensitivity to gemcitabine. Oncogene 23 (2004) 1539-1548
37. Newman D.J., Cragg G.M., and Snader K.M. Natural products as sources of new drugs over the period 1981-2002. J Nat Prod 66 (2003) 1022-1037
38. Batty K.T., Davis T.M., Thu L.T., Binh T.Q., Anh T.K., and Ilett K.F. Selective high-performance liquid chromatographic determination of artesunate and alpha- and beta-dihydroartemisinin in patients with falciparum malaria. J Chromatogr B Biomed Appl 677 (1996) 345-350
39. Berger J.M., Gamblin S.J., Harrison S.C., and Wang J.C. Structure and mechanism of DNA topoisomerase II. Nature 379 (1996) 225-232
40. Topcu Z. DNA topoisomerases as targets for anticancer drugs. J Clin Pharm Ther 26 (2001) 405-416
41. Fulda S., and Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25 (2006) 4798-4811
42. Kim D.G., You K.R., Liu M.J., Choi Y.K., and Won Y.S. GADD153-mediated anticancer effects of N-(4-hydroxyphenyl)retinamide on human hepatoma cells. J Biol Chem 277 (2002) 38930-38938
43. Kelman Z. PCNA: structure, functions and interactions. Oncogene 14 (1997) 629-640
44. Hu W.G., Wang C.Y., Liu T., Xiong J.X., and Yang Z.Y. Expression of sonic hedgehog, EGFR and PCNA proteins in pancreatic cancer and their correlations to cell proliferation. Ai Zheng 26 (2007) 947-951
45. Makinen K., Loimas S., Hakala T., and Eskelinen M. Tumour suppressor protein (p53), apoptosis inhibiting protein (Bcl-2) and proliferating cell nuclear antigen (PCNA) expressions in a rat pancreatic tumour model. Anticancer Res 27 (2007) 23-26
46. Baek S.J., Kim J.S., Nixon J.B., DiAugustine R.P., and Eling T.E. Expression of NAG-1, a transforming growth factor-beta superfamily member, by troglitazone requires the early growth response gene EGR-1. J Biol Chem 279 (2004) 6883-6892
47. Lee S.H., Kim J.S., Yamaguchi K., Eling T.E., and Baek S.J. Indole-3-carbinol and 3,3'-diindolylmethane induce expression of NAG-1 in a p53-independent manner. Biochem Biophys Res Commun 328 (2005) 63-69
48. Song X., Lin H.P., Johnson A.J., Tseng P.H., Yang Y.T., Kulp S.K., et al. Cyclooxygenase-2, player or spectator in cyclooxygenase-2 inhibitor-induced apoptosis in prostate cancer cells. J Natl Cancer Inst 94 (2002) 585-591
49. Nutter L.M., and Cheng Y.C. Nature and properties of mammalian ribonucleoside diphosphate reductase. Pharmacol Ther 26 (1984) 191-207