Dihydroartemisinin inhibits the human erythroid cell differentiation by altering the cell cycle

Toxicology

Volumn 300, Issue 1-2, 2012, Pages 57-66

  Finaurini, Sara ^a   Basilico, Nicoletta ^a   Corbett, Yolanda ^a   D'Alessandro, Sarah ^a   Parapini, Silvia ^a   Olliaro, Piero ^b   Haynes, Richard K ^c   Taramelli, Donatella ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b WORLD HEALTH ORGANIZATION   (Switzerland)

^c HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Cytotoxicity; Dihydroartemisinin; Erythro toxicity; K562 erythroid cell differentiation; Malaria in pregnancy

Indexed keywords

10 DEOXOARTEMISININ; ANTINEOPLASTIC AGENT; ARTEMISIN DERIVATIVE; ARTEMISONE; ARTESUNATE; CHLOROQUINE; DIHYDROARTEMISININ; GAMMA GLOBIN; GLYCOPHORIN A; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DOWN REGULATION; ERYTHROID CELL; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; S PHASE CELL CYCLE CHECKPOINT; STRUCTURE ACTIVITY RELATION;

ARTEMISININS; CELL CYCLE; CELL DIFFERENTIATION; ERYTHROID CELLS; FLOW CYTOMETRY; HUMANS; K562 CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRUCTURE-ACTIVITY RELATIONSHIP;

ANIMALIA; ARTESUNATE;

EID: 84863811798     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.05.024     Document Type: Article

References (69)

1. 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.
2. Berger J. Alternative haematotoxicological testing. J. Appl. Biomed. 2010, 8:11-18.
3. Chen H.-H., Zhou H.-J., Wang W.-Q., Wu G.-D. Antimalarial dihydroartemisinin also inhibits angiogenesis. Cancer Chemother. Pharmacol. 2004, V53:423-432.
4. Chenais B., Molle I., Trentesaux C., Jeannesson P. Time-course of butyric acid-induced differentiation in human K562 leukemic cell line: rapid increase in gamma-globin, porphobilinogen deaminase and NF-E2 mRNA levels. Leukemia 1997, 11:1575-1579.
5. Chukwuani M.C., Bolaji O.O., Onyeji C.O., Makinde O.N., Ogunbona F.A. Evidence for increased metabolism of chloroquine during the early third trimester of human pregnancy. Trop. Med. Int. Health 2004, 9:601-605.
6. Clark R.L. Embryotoxicity of the artemisinin antimalarials and potential consequences for use in women in the first trimester. Reprod. Toxicol. 2009, 28:285-296.
7. Clark R.L., Arima A., Makori N., Nakata Y., Bernard F., Gristwood W., Harrell A., White T.E., Wier P.J. Artesunate: developmental toxicity and toxicokinetics in monkeys. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:418-434.
8. Clark R.L., Brannen K.C., Sanders J.E., Hoberman A.M. Artesunate and artelinic acid: association of embryotoxicity, reticulocytopenia, and delayed stimulation of hematopoiesis in pregnant rats. Birth Defects Res. B: Dev. Reprod. Toxicol. 2011, 92:52-68.
9. Clark R.L., Gristwood W.E., Lewsley R., Wilson R., Harrell A.W. Localization of artesunate and its derivatives in the pregnant rat and fetus following oral administration and relationship to developmental toxicity. Birth Defects Res. B: Dev. Reprod. Toxicol. 2010, 89:364-375.
10. Clark R.L., Lerman S.A., Cox E.M., Gristwood W.E., White T.E. Developmental toxicity of artesunate in the rat: comparison to other artemisinins, comparison of embryotoxicity and kinetics by oral and intravenous routes, and relationship to maternal reticulocyte count. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:397-406.
11. Clark R.L., White T.E., Clode S.A., Gaunt I., Winstanley P., Ward S.A. Developmental toxicity of artesunate and an artesunate combination in the rat and rabbit. Birth Defects Res. B: Dev. Reprod. Toxicol. 2004, 71:380-394.
12. D'Alessandro S., Basilico N., Corbett Y., Scaccabarozzi D., Omodeo-Sale F., Saresella M., Marventano I., Vaillant M., Olliaro P., Taramelli D. Hypoxia modulates the effect of dihydroartemisinin on endothelial cells. Biochem. Pharmacol. 2011, 82:476-484.
13. D'Alessandro S., Gelati M., Basilico N., Parati E.A., Haynes R.K., Taramelli D. Differential effects on angiogenesis of two antimalarial compounds, dihydroartemisinin and artemisone: implications for embryotoxicity. Toxicology 2007, 241:66-74.
14. Dean A., Erard F., Schneider A.P., Schechter A.N. Induction of hemoglobin accumulation in human K562 cells by haemin is reversible. Science 1981, 212:459-461.
15. Dell'Eva R., Pfeffer U., Vene R., Anfosso L., Forlani A., Albini A., Efferth T. Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial artesunate. Biochem. Pharmacol. 2004, 68:2359-2366.
16. Efferth T. Mechanistic perspectives for 1,2,4-trioxanes in anti-cancer therapy. Drug Resist. Update 2005, 8:85-97.
17. Efferth T. Willmar Schwabe Award 2006: antiplasmodial and antitumor activity of artemisinin-from bench to bedside. Planta Med. 2007, 73:299-309.
18. Efferth T., Benakis A., Romero M.R., Tomicic M., Rauh R., Steinbach D., Hafer R., Stamminger T., Oesch F., Kaina B., Marschall M. Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron. Free Radic. Biol. Med. 2004, 37:998-1009.
19. Efferth T., Kaina B. Toxicity of the antimalarial artemisinin and its derivatives. Crit. Rev. Toxicol. 2010, 40:405-421.
20. Fibach E., Manor D., Oppenheim A., Rachmilewitz E.A. Proliferation and maturation of human erythroid progenitors in liquid culture. Blood 1989, 73:100-103.
21. Finaurini S., Ronzoni L., Colancecco A., Cattaneo A., Cappellini M.D., Ward S.A., Taramelli D. Selective toxicity of dihydroartemisinin on human CD34+ erythroid cell differentiation. Toxicology 2010, 276:128-134.
22. Fontana S., Alessandro R., Barranca M., Giordano M., Corrado C., Zanella-Cleon I., Becchi M., Kohn E.C., De Leo G. Comparative proteome profiling and functional analysis of chronic myelogenous leukemia cell lines. J. Proteome Res. 2007, 6:4330-4342.
23. Gao J.L., Ding X.P., Li Q.J., Xia Z.L., Xia Q.J. [Effect of dihydroartemisinin on the expression of BCR/ABL fusion gene in leukemia K562 cells]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2012, 29:19-22.
24. Grebenova D., Kuzelova K., Pluskalova M., Peslova G., Halada P., Hrkal Z. The proteomic study of sodium butyrate antiproliferative/cytodifferentiation effects on K562 cells. Blood Cells. Mol. Dis. 2006, 37:210-217.
25. Handrick R., Ontikatze T., Bauer K.D., Freier F., Rubel A., Durig J., Belka C., Jendrossek V. Dihydroartemisinin induces apoptosis by a Bak-dependent intrinsic pathway. Mol. Cancer Ther. 2010, 9:2497-2510.
26. Haynes R.K. From artemisinin to new artemisinin antimalarials: biosynthesis, extraction, old and new derivatives, stereochemistry and medicinal chemistry requirements. Curr. Top. Med. Chem. 2006, 6:509-537.
27. Haynes R.K., Cheu K.W., Tang M.M., Chen M.J., Guo Z.F., Guo Z.H., et al. Reactions of antimalarial peroxides with each of leucomethylene blue and dihydroflavins: flavin reductase and the cofactor model exemplified. ChemMedChem 2011, 6:279-291.
28. Haynes R.K., Fugmann B., Stetter J., Rieckmann K., Heilmann H.-D., Chan H.-W., Man-Ki Cheung Lam W.-L., Wong H.-N., Croft S.L., Vivas L., Rattray L., Stewart L., Peters W., Robinson B.L., Edstein M.D., Kotecka B., Kyle D.E., Beckermann B., Gerisch M., Radtke M., Schmuck G., Steinke W., Wollborn U., Schmeer K., Römer A. Artemisone - a highly active antimalarial drug of the artemisinin class. Angew. Chem. Int. Ed. Engl. 2006, 45:2082-2088.
29. Iyamu E., Perdew H., Woods G. Growth inhibitory and differentiation effects of chloroquine and its analogue on human leukemic cells potentiate fetal hemoglobin production by targeting the polyamine pathway. Biochem. Pharmacol. 2009, 77:1021-1028.
30. Jeannesson P., Lahlil R., Chenais B., Devy L., Gillet R., Aries A., Morceau F., Trentesaux C. Anthracyclines as tumor cell differentiating agents: effects on the regulation of erythroid gene expression. Leuk. Lymphoma 1997, 26:575-587.
31. Jiang P.D., Zhao Y.L., Shi W., Deng X.Q., Xie G., Mao Y.Q., Li Z.G., Zheng Y.Z., Yang S.Y., Wei Y.Q. Cell growth inhibition, G2/M cell cycle arrest, and apoptosis induced by chloroquine in human breast cancer cell line Bcap-37. Cell. Physiol. Biochem. 2008, 22:431-440.
32. Kamchonwongpaisan S., Meshnick S.R. The mode of action of the antimalarial artemisinin and its derivatives. Gen. Pharmacol. 1996, 27:587-592.
33. Krishna S., Bustamante L., Haynes R.K., Staines H.M. Artemisinins: their growing importance in medicine. Trends Pharmacol. Sci. 2008, 29:520-527.
34. Lee J., Zhou H.J., Wu X.H. Dihydroartemisinin downregulates vascular endothelial growth factor expression and induces apoptosis in chronic myeloid leukemia K562 cells. Cancer Chemother. Pharmacol. 2006, 57:213-220.
35. Li J., Zhou H.J. Dihydroartemisinin inhibits the expression of vascular endothelial growth factor in K562 cells. Yao Xue Xue Bao 2005, 40:1041-1045.
36. Li L., Zhang G., Zhang Y., Tan J., Huang H., Huang B., Lu J. Sodium butyrate-induced upregulation of p18(INK4C) gene affects K562 cell G (0)/G (1) arrest and differentiation. Mol. Cell. Biochem. 2008, 319:9-15.
37. Li P.C., Lam E., Roos W.P., Zdzienicka M.Z., Kaina B., Efferth T. Artesunate derived from traditional Chinese medicine induces DNA damage and repair. Cancer Res. 2008, 68:4347-4351.
38. Li Q., Weina P.J. Severe embryotoxicity of artemisinin derivatives in experimental animals, but possibly safe in pregnant women. Molecules 2010, 15:40-57.
39. Longo M., Zanoncelli S., Brughera M., Colombo P., Wittlin S., Vennerstrom J.L., Moehrle J., Craft J.C. Comparative embryotoxicity of different antimalarial peroxides: in vitro study using the rat whole embryo culture model (WEC). Reprod. Toxicol. 2010, 30:583-590.
40. Longo M., Zanoncelli S., Della Torre P., Rosa F., Giusti A., Colombo P., Brughera M., Mazue G., Olliaro P. Investigations of the effects of the antimalarial drug dihydroartemisinin (DHA) using the Frog Embryo Teratogenesis Assay-Xenopus (FETAX). Reprod. Toxicol. 2008, 25:433-441.
41. Longo M., Zanoncelli S., Manera D., Brughera M., Colombo P., Lansen J., Mazue G., Gomes M., Taylor W.R., Olliaro P. Effects of the antimalarial drug dihydroartemisinin (DHA) on rat embryos in vitro. Reprod. Toxicol. 2006, 21:83-93.
42. Longo M., Zanoncelli S., Torre P.D., Riflettuto M., Cocco F., Pesenti M., Giusti A., Colombo P., Brughera M., Mazue G., Navaratman V., Gomes M., Olliaro P. In vivo and in vitro investigations of the effects of the antimalarial drug dihydroartemisinin (DHA) on rat embryos. Reprod. Toxicol. 2006, 22:797-810.
43. Lozzio B.B., Lozzio C.B. Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. Int. J. Cancer 1977, 19:136.
44. Lozzio B.B., Lozzio C.B., Krauss S., Wust C.J., Girardi A. Leukemia-associated antigens detected by a nonhuman primate antiserum to a Ph1+ myeologenous leukemia cell line. Blood 1977, 50:115-124.
45. Lozzio C.B., Lozzio B.B. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 1975, 45:321-334.
46. Lozzio C.B., Lozzio B.B., Machado E.A., Fuhr J.E., Lair S.V., Bamberger E.G. Effects of sodium butyrate on human chronic myelogenous leukaemia cell line K562. Nature 1979, 281:709-710.
47. Mackenzie A.H. Antimalarial drugs for rheumatoid arthritis. Am. J. Med. 1983, 75:48-58.
48. Marks P.A., Rifkind R.A. Erythroleukemic differentiation. Annu. Rev. Biochem. 1978, 47:419-448.
49. McGready R., Stepniewska K., Lindegardh N., Ashley E.A., La Y., Singhasivanon P., White N.J., Nosten F. The pharmacokinetics of artemether and lumefantrine in pregnant women with uncomplicated falciparum malaria. Eur. J. Clin. Pharmacol. 2006, 62:1021-1031.
50. McGready R., Stepniewska K., Ward S.A., Cho T., Gilveray G., Looareesuwan S., White N.J., Nosten F. Pharmacokinetics of dihydroartemisinin following oral artesunate treatment of pregnant women with acute uncomplicated falciparum malaria. Eur. J. Clin. Pharmacol. 2006, 62:367-371.
51. Meshnick S.R. The mode of action of antimalarial endoperoxides. Trans. R. Soc. Trop. Med. Hyg. 1994, 88(Suppl. 1):S31-S32.
52. Meunier B., Robert A. Haeme as trigger and target for trioxane-containing antimalarial drugs. Acc. Chem. Res. 2010, 43:1444-1451.
53. Nakajima O., Hashimoto Y., Iwasaki S. Erythroid differentiation-inducing activity of protoporphyrin IX and its analogs on human leukemia K562 cell line. Biochem. Biophys. Res. Commun. 1994, 198:720-727.
54. Nosten F., McGready R., d'Alessandro U., Bonell A., Verhoeff F., Menendez C., Mutabingwa T., Brabin B. Antimalarial drugs in pregnancy: a review. Curr. Drug Safety 2006, 1:1-15.
55. O'Neill P.M., Posner G.H. A medicinal chemistry perspective on artemisinin and related endoperoxides. J. Med. Chem. 2004, 47:2945-2964.
56. Parapini S., Basilico N., Mondani M., Olliaro P., Taramelli D., Monti D. Evidence that haem iron in the malaria parasite is not needed for the antimalarial effects of artemisinin. FEBS Lett. 2004, 575:91-94.
57. Ribeiro I.R., Olliaro P. Safety of artemisinin and its derivatives. A review of published and unpublished clinical trials. Med. Trop. (Mars.) 1998, 58:50-53.
58. Robert A., Coppel Y., Meunier B. Alkylation of haeme by the antimalarial drug artemisinin. Chem Commun (Camb.) 2002, 414-415.
59. Rodgers G.P., Saunthararajah Y. Advances in experimental treatment of beta-thalassaemia. Expert Opin. Invest. Drug 2001, 10:925-934.
60. Rombo L., Bergqvist Y., Hellgren U. Chloroquine and desethylchloroquine concentrations during regular long-term malaria prophylaxis. Bull. World Health Organ. 1987, 65:879-883.
61. Rutherford T.R., Clegg J.B., Weatherall D.J. K562 human leukaemic cells synthesise embryonic haemoglobin in response to haemin. Nature 1979, 280:164-165.
62. Ward S.A., Sevene E.J., Hastings I.M., Nosten F., McGready R. Antimalarial drugs and pregnancy: safety, pharmacokinetics, and pharmacovigilance. Lancet Infect. Dis. 2007, 7:136-144.
63. Watanabe T., Mitchell T., Sariban E., Sabbath K., Griffin J., Kufe D. Effects of 1-beta-d-arabinofuranosylcytosine and phorbol ester on differentiation of human K562 erythroleukemia cells. Mol. Pharmacol. 1985, 27:683-688.
64. White N.J. Qinghaosu (artemisinin): the price of success. Science 2008, 320:330-334.
65. White T.E., Clark R.L. Sensitive periods for developmental toxicity of orally administered artesunate in the rat. Birth Defects Res. B: Dev. Reprod. Toxicol. 2008, 83:407-417.
66. WHO, 2006. Assessment of the safety of artemisinin compounds in pregnancy.
67. WHO, 2006. Guidelines for the treatment of malaria.
68. WHO, 2007. Technical expert group meeting on intermittent preventive treatment in pregnancy (IPTp).
69. WHO, 2009. World Malaria Report 2010.