The anti-malaria drug artesunate inhibits replication of cytomegalovirus in vitro and in vivo

Antiviral Research

Volumn 69, Issue 2, 2006, Pages 60-69

  Kaptein, Suzanne J F ^b   Efferth, Thomas ^c   Leis, Martina ^a   Rechter, Sabine ^a   Auerochs, Sabrina ^a   Kalmer, Martina ^a   Bruggeman, Cathrien A ^b   Vink, Cornelis ^b   Stamminger, Thomas ^a   Marschall, Manfred ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Artesunate; Combined antiviral therapy; Cytomegalovirus; Drug development; Ferrous iron

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISIN; ARTESUNATE; CELL ADHESION MOLECULE; CIDOFOVIR; FERROSANOL; FERROUS ION; FOSCARNET; GANCICLOVIR; PACLITAXEL; THY 1 ANTIGEN; TRANSFERRIN; VIRUS DNA;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG INHIBITION; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALIVARY GLAND; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; ANTIMALARIALS; ANTIVIRAL AGENTS; ARTEMISININS; CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DRUG THERAPY, COMBINATION; FERROUS COMPOUNDS; FIBROBLASTS; HERPESVIRIDAE INFECTIONS; HUMANS; IMMUNOCOMPROMISED HOST; MALE; MUROMEGALOVIRUS; RATS; RATS, INBRED LEW; SESQUITERPENES; SPECIFIC PATHOGEN-FREE ORGANISMS; TRANSFERRIN; VIRUS REPLICATION;

ANIMALIA; ARTESUNATE; CYTOMEGALOVIRUS; DNA VIRUSES; HUMAN HERPESVIRUS 5; MURID HERPESVIRUS 2;

EID: 31444451671     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2005.10.003     Document Type: Article

References (53)

1. M. Adjuik, A. Babiker, P. Garner, P. Olliaro, W. Taylor, N. White, and International Artemisinin Study Group Artesunate combinations for treatment of malaria: meta-analysis Lancet 363 2004 9 17
2. E. Alejo Resistance of human cytomegalovirus to antiviral drugs Clin. Microbiol. Rev. 12 1999 286 297
3. A. Benakis, M. Paris, L. Loutan, C.T. Plessas, and S.T. Plessas Pharmacokinetics of artemisinin and artesunate after oral administration in healthy volunteers Am. J. Trop. Med. Hyg. 56 1997 17 23
4. C.A. Bruggeman, W.M.H. Debie, G.E.L.M. Grauls, G. Majoor, and C.P.A. van Boven Infection of laboratory rats with a new cytomegalo-like virus Arch. Virol. 76 1983 189 199
5. C.A. Bruggeman, H. Meijer, P.H.J. Dormans, W.M.H. Debie, G.E.L.M. Grauls, and C.P.A. van Boven Isolation of a cytomegalovirus-like agent from wild rats Arch. Virol. 73 1982 231 241
6. C.A. Bruggeman, H. Meijer, F. Bosman, and C.P.A. van Boven Biology of rat cytomegalovirus infection Intervirology 24 1985 1 9
7. J. Cinatl Jr., R. Kotchetkov, E. Weimer, R.A. Blaheta, M. Scholz, J.U. Vogel, H.O. Gumbel, and H.W. Doerr The antisense oligonucleotide ISIS 2922 prevents cytomegalovirus-induced upregulation of IL-8 and ICAM-1 in cultured human fibroblasts J. Med. Virol. 60 2000 313 323
8. J.L. Craigen, and J.E. Grundy Cytomegalovirus induced up-regulation of LFA-3 (CD58) and ICAM-1 (CD54) is a direct viral effect that is not prevented by ganciclovir or foscarnet treatment Transplantation 62 1996 1102 1108
9. J.N. Cumming, P. Ploypradith, and G.H. Posner Antimalarial activity of artemisinin (qinghaosu) and related trioxanes: mechanism(s) of action Adv. Pharmacol. 37 1997 253 297
10. R. Dell'Eva, U. Pfeffer, R. Vene, L. Anfosso, A. Forlani, A. Albini, and T. Efferth Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial artesunate Biochem. Pharmacol. 68 2004 2359 2366
11. P.J. de Vries, and T.K. Dien Clinical pharmacology and therapeutic potential of artemisinin and its derivatives in the treatment of malaria Drugs 52 1996 818 836
12. P.O. Edlund, D. Westerlund, J. Carlqvist, B.L. Wu, and J.H. Jin Determination of artesunate and dihydroartemisinin in plasma by liquid chromatography with post-column derivatization and UV-detection Acta Pharm. Suec. 21 1984 223 234
13. T. Efferth, H. Dunstan, A. Sauerbrey, H. Miyachi, and C.R. Chitambar The anti-malarial artesunate is also active against cancer Int. J. Oncol. 18 2001 767 773
14. T. Efferth, M. Marschall, X. Wang, S.M. Huong, I. Hauber, A. Olbrich, M. Kronschnabl, T. Stamminger, and E.S. Huang Antiviral activity of artesunate towards wild-type, recombinant, and ganciclovir-resistant human cytomegaloviruses J. Mol. Med. 80 2002 233 242
15. T. Efferth, A. Sauerbrey, A. Olbrich, E. Gebhart, P. Rauch, H.O. Weber, J.G. Hengstler, M.E. Halatsch, M. Volm, K.D. Tew, D.D. Ross, and J.O. Funk Molecular modes of action of artesunate in tumor cell lines Mol. Pharmacol. 64 2003 382 394
16. T. Efferth, A. Benakis, M.R. Romero-Rodriguez, M. Tomicic, R. Rauh, D. Steinbach, R. Häfer, T. Stamminger, F. Oesch, B. Kaina, and M. Marschall Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron Free Radic. Biol. Med. 37 2004 998 1009
17. H. Einsele, H.D. Waller, P. Weber, N. Frickhofen, S. Dette, H.P. Horny, A. Roos, H. Roos, H. Hebart, and H. Schmidt Cytomegalovirus in liver biopsies of marrow transplant recipients: detection methods, clinical, histological and immunohistological features Med. Microbiol. Immunol. 183 1994 205 216
18. A. Erice Resistance of human cytomegalovirus to antiviral drugs Clin. Microbiol. Rev. 12 1999 286 297
19. W.P. Faulk, B.L. Hsi, and P.J. Stevens Transferrin and transferrin receptors in carcinoma of the breast Lancet ii 1980 390 392
20. K.C. Gatter, G. Brown, I.S. Trowbridge, R.E. Woolston, and D.Y. Mason Transferrin receptors in human tissues: their distribution and possible clinical relevance J. Clin. Pathol. 36 1983 539 545
21. R.F. Genovese, D.B. Newman, and T.G. Brewer Behavioral and neural toxicity of the artemisinin antimalarial, arteether, but not artesunate and artelinate, in rats Pharmacol. Biochem. Behav. 67 2000 37 44
22. Y. Kabe, K. Ando, S. Hirao, M. Yoshida, and H. Handa Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus Antioxid. Redox. Signal. 7 2005 395 403
23. S.J.F. Kaptein, P.S. Beisser, Y.K. Gruijthuijsen, K.G.M. Savelkouls, K.W.R. van Cleef, E. Beuken, G.E.L.M. Grauls, C.A. Bruggeman, and C. Vink The rat cytomegalovirus R78 G protein-coupled receptor gene is required for production of infectious virus in the spleen J. Gen. Virol. 84 2003 2517 2530
24. S.J.F. Kaptein, K.W.R. van Cleef, Y.K. Gruijthuijsen, E.V.H. Beuken, L. Van Buggenhout, P.S. Beisser, F.R.M. Stassen, C.A. Bruggeman, and C. Vink The r131 gene of rat cytomegalovirus encodes a proinflammatory CC chemokine homolog which is essential for the production of infectious virus in the salivary glands Virus Genes 29 2004 43 61
25. P. Kollia, N. Stavroyianni, K. Stamatopoulos, K. Zoi, N. Viniou, M. Mantzourani, C.T. Noguchi, G. Paterakis, D. Abazis, C. Pangalos, D. Loukopoulos, and X. Yataganas Molecular analysis of transferrin receptor mRNA expression in acute myeloid leukaemia Br. J. Haematol. 115 2001 19 24
26. P.K. Koskinen, S. Yilmaz, E. Kallio, C.A. Bruggeman, P.J. Häyry, and K. Lemström Rat cytomegalovirus infection and chronic kidney allograft rejection Transpl. Int. 9 Suppl. 1 1996 S3 S4
27. I. Lautenschlager, A. Soots, L. Krogerus, K. Inkinen, J. Kloover, R. Loginov, K. Holma, H. Kauppinen, C. Bruggeman, and J. Ahonen Time-related effects of cytomegalovirus infection on the development of chronic renal allograft rejection in a rat model Intervirology 42 1999 279 284
28. M. Leis, M. Marschall, and T. Stamminger Downregulation of the cellular adhesion molecule Thy-1 (CD90) by cytomegalovirus infection of human fibroblasts J. Gen. Virol. 85 2004 1995 2000
29. K. Lemström, P. Koskinen, L. Krogerus, M. Daemen, C.A. Bruggeman, and P. Häyry Cytomegalovirus antigen expression, endothelial cell proliferation, and intimal thickening in rat cardiac allografts after cytomegalovirus infection Circulation 92 1995 2594 2604
30. Q-G. Li, J.O. Peggins, L.L. Fleckenstein, K. Masonic, M.H. Heiffer, and T.G. Brewer The pharmacokinetics and bioavailability of dihydroartemisinin, arteether, artemether, artesunic acis and artelinic acid in rats J. Pharm. Pharmacol. 50 1998 173 182
31. T. Maisch, B. Kropff, C. Sinzger, and M. Mach Upregulation of CD40 expression on endothelial cells infected with human cytomegalovirus J. Virol. 76 2002 12803 12812
32. M. Marschall, P. Alliger, F. Schwarzmann, C. Bogedain, M. Brand, B. Reichelt, G. Glaser, and H. Wolf The lytic transition of Epstein-Barr virus is imitated by recombinant B-cells Arch. Virol. 129 1993 23 33
33. M. Marschall, M. Freitag, S. Weiler, G. Sorg, and T. Stamminger Recombinant green fluorescent protein-expressing human cytomegalovirus as a tool for screening antiviral agents Antimicrob. Agents Chemother. 44 2000 1588 1597
34. T. Martelius, L. Krogerus, K. Höckerstedt, C.A. Bruggeman, and I. Lautenschlager Cytomegalovirus infection is associated with increased inflammation and severe bile duct damage in rat liver allografts Hepatology 27 1998 996 1002
35. S.R. Meshnick Artemisinin: mechanisms of action, resistance and toxicity Int. J. Parasitol. 32 2002 1655 1660
36. A. Nontprasert, S. Pukrittayakamee, M. Nosten-Bertrand, S. Vanijanonta, and N.J. White Studies of the neurotoxicity of oral artemisinin derivatives in mice Am. J. Trop. Med. Hyg. 62 2000 409 412
37. P.L. Olliaro, N.K. Nair, K. Sathasivam, S.M. Mansor, and V. Navaratnam Pharmacokinetics of artesunate after single oral administration to rats BMC Pharmacol. 1 2001 12
38. I.M. Onorato, D.M. Morens, W.J. Martone, and S.K. Stansfield Epidemiology of cytomegaloviral infections: recommendations for prevention and control Rev. Infect. Dis. 7 1985 479 497
39. I.R. Ribeiro, and P. Olliaro Safety of artemisinin and its derivatives. A review of published and unpublished clinical trials Med. Trop. (Mars) 58 1998 50 53
40. D. Sadava, T. Phillips, C. Lin, and S.E. Kane Transferrin overcomes drug resistance to artemisinin in human small-cell lung carcinoma cells Cancer Lett. 179 2002 151 156
41. N. Shterman, B. Kupfer, and C. Moroz Comparison of transferrin receptors, iron content and isoferritin profile in normal and malignant human breast cell lines Pathobiology 59 1991 19 25
42. N.P. Singh, and H. Lai Selective toxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells Life Sci. 70 2001 49 56
43. F.S. Stals, F. Bosman, C.P. van Boven, and C.A. Bruggeman An animal model for therapeutic intervention studies of CMV infection in the immunocompromised host Arch. Virol. 114 1990 91 107
44. G. Steinhoff, X.M. You, C. Steinmüller, K. Boeke, F.S. Stals, C.A. Bruggeman, and A. Haverich Induction of endothelial adhesion molecules by rat cytomegalovirus in allogeneic lung transplantation in the rat Scand. J. Infect. Dis. Suppl. 99 1995 58 60
45. R. Sutherland, D. Delia, C. Schneider, R. Newman, J. Kemshead, and M. Greaves Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin Proc. Natl. Acad. Sci. U.S.A. 78 1981 4515 4519
46. T.H. The, A.M. Kas-Deelen, E.F. de Maar, C. Driessen, M.C. Harmsen, and W.J. van Son Cellular and humoral parameters for vascular damage in blood during cytomegalovirus infections Transplant. Proc. 33 2001 1813
47. I.S. Trowbridge, and M.B. Omary Human cell surface glycoprotein related to cell proliferation is the receptor for transferrin Proc. Natl. Acad. Sci. U.S.A. 78 1981 3039 3043
48. M.A. van Agtmael, T.A. Eggelte, and C.J. van Boxtel Artemisinin drugs in the treatment of malaria: from medicinal herb to registered medication Trends Pharmacol. Sci. 20 1999 199 205
49. J.L. Vennerstrom, S. Arbe-Barnes, R. Brun, S.A. Charman, F.C. Chiu, J. Chollet, Y. Dong, A. Dorn, D. Hunziker, H. Matile, K. McIntosh, M. Padmanilayam, J. Santo Tomas, C. Scheurer, B. Scorneaux, Y. Tang, H. Urwyler, S. Wittlin, and W.N. Charman Identification of an antimalarial synthetic trioxolane drug development candidate Nature 430 2004 900 904
50. W.J. Waldman, D.A. Knight, and E.H. Huang An in vitro model of T cell activation by autologous cytomegalovirus (CMV)-infected human adult endothelial cells: contribution of CMV-enhanced endothelial ICAM-1 J. Immunol. 160 1998 3143 3151
51. H.J. Woerdenbag, T.A. Moskal, N. Pras, T.M. Malingre, F.S. el-Feraly, H.H. Kampinga, and A.W. Konings Cytotoxicity of artemisinin-related endoperoxides to Ehrlich ascites tumor cells J. Nat. Prod. 56 1993 849 856
52. D.C. Yang, F. Wang, R.L. Elliott, and J.F. Head Expression of transferrin receptor and ferritin H-chain mRNA are associated with clinical and histopathological prognostic indicators in breast cancer Anticancer Res. 21 2001 541 549
53. S. Yilmaz, P.K. Koskinen, E. Kallio, C.A. Bruggeman, P.J. Häyry, and K.B. Lemström Cytomegalovirus infection-enhanced chronic kidney allograft rejection is linked with intercellular adhesion molecule-1 expression Kidney Int. 50 1996 526 537