A dual mechanism of action of the anticancer agent F 11782 on human topoisomerase II α

Biochemical Pharmacology

Volumn 66, Issue 4, 2003, Pages 623-631

  Jensen, Lars H ^a,b   Renodon Cornière, Axelle ^a   Nitiss, Karin C ^c   Hill, Bridget T ^d   Nitiss, John L ^c   Jensen, Peter B ^b   Sehested, Maxwell ^a  

^a Rigshospitalet   (Denmark)

^b FINSEN LABORATORY   (Denmark)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

Chemotherapy; DNA damage; Epipodophyllotoxin; Mutation; Surface plasmon resonance; Topoisomerase II

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE (ATP HYDROLYSING); EPIPODOPHYLLOTOXIN DERIVATIVE; F 11782; PIPERAZINE DERIVATIVE; PROTEIN SUBUNIT;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CATALYSIS; CHO CELL; CONTROLLED STUDY; COVALENT BOND; DRUG MECHANISM; DRUG STRUCTURE; ENZYME PURIFICATION; FEMALE; HUMAN; LUNG SMALL CELL CANCER; MUTATION; NONHUMAN; PRIORITY JOURNAL;

EID: 0142134349     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00342-3     Document Type: Article

References (37)

1. Wang J.C. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys. 31:1998;107-144.
2. Champoux J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70:2001;369-413.
3. Nitiss J.L. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta. 1400:1998;63-81.
4. Wang J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3:2002;430-440.
5. Chen A.Y., Liu L.F. DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 34:1994;191-218.
6. Fortune J.M., Osheroff N. Topoisomerase II as a target for anticancer drugs: when enzymes stop being nice. Prog. Nucleic Acid Res. Mol. Biol. 64:2000;221-253.
7. Andoh T., Ishida R. Catalytic inhibitors of DNA topoisomerase II. Biochim. Biophys. Acta. 1400:1998;155-171.
8. Fortune J.M., Osheroff N. Merbarone inhibits the catalytic activity of human topoisomerase II alpha by blocking DNA cleavage. J. Biol. Chem. 273:1998;17643-17650.
9. Jensen P.B., Sorensen B.S., Demant E.J., Sehested M., Jensen P.S., Vindelov L., Hansen H.H. Antagonistic effect of aclarubicin on the cytotoxicity of etoposide and 4′-(9-acridinylamino)methanesulfon-m-anisidide in human small cell lung cancer cell lines and on topoisomerase II-mediated DNA cleavage. Cancer Res. 50:1990;3311-3316.
10. Jensen P.B., Jensen P.S., Demant E.J., Friche E., Sorensen B.S., Sehested M., Wassermann K., Vindelov L., Westergaard O., Hansen H.H. Antagonistic effect of aclarubicin on daunorubicin-induced cytotoxicity in human small cell lung cancer cells: relationship to DNA integrity and topoisomerase II. Cancer Res. 51:1991;5093-5099.
11. Jensen L.H., Renodon-Cornière A., Wessel I., Langer S.W., Sokilde B., Carstensen E.V., Sehested M., Jensen P.B. Maleimide is a potent inhibitor of topoisomerase II in vitro and in vivo: a new mode of catalytic inhibition. Mol. Pharmacol. 61:2002;1235-1243.
12. Chowdhury A., Mandal S., Mittra B., Sharma S., Mukhopadhyay S., Majumder H. Betulinic acid, a potent inhibitor of eukaryotic topoisomerase I: identification of the inhibitory step, the major functional group responsible and development of more potent derivatives. Med. Sci. Monit. 8:2002;BR254-BR265.
13. Poddevin B., Riou J.F., Lavelle F., Pommier Y. Dual topoisomerase I and II inhibition by intoplicine (RP-60475), a new antitumor agent in early clinical trials. Mol. Pharmacol. 44:1993;767-774.
14. Trask D.K., Muller M.T. Stabilization of type I topoisomerase-DNA covalent complexes by actinomycin D. Proc. Natl. Acad. Sci. U.S.A. 85:1988;1417-1421.
15. Wassermann K., Markovits J., Jaxel C., Capranico G., Kohn K.W., Pommier Y. Effects of morpholinyl doxorubicins, doxorubicin, and actinomycin D on mammalian DNA topoisomerases I and II. Mol. Pharmacol. 38:1990;38-45.
16. Nitiss J.L., Pourquier P., Pommier Y. Aclacinomycin A stabilizes topoisomerase I covalent complexes. Cancer Res. 57:1997;4564-4569.
17. Perrin D., van Hille B., Barret J.M., Kruczynski A., Etievant C., Imbert T., Hill B.T. F 11782, a novel epipodophylloid non-intercalating dual catalytic inhibitor of topoisomerases I and II with an original mechanism of action. Biochem. Pharmacol. 59:2000;807-819.
18. Etievant C., Kruczynski A., Barret J.M., Perrin D., van Hille B., Guminski Y., Hill B.T. F 11782, a dual inhibitor of topoisomerases I and II with an original mechanism of action in vitro and markedly superior in vivo antitumour activity, relative to three other dual topoisomerase inhibitors, intoplicin, aclarubicin and TAS-103. Cancer Chemother. Pharmacol. 46:2000;101-113.
19. Barret J.M., Montaudon D., Etievant C., Perrin D., Kruczynski A., Robert J., Hill B.T. Detection of DNA-strand breaks in cells treated with F 11782, a catalytic inhibitor of topoisomerases I and II. Anticancer Res. 20:2000;4557-4562.
20. Barret J.M., Hill B.T., Olive P.L. Characterization of DNA-strand breakage induced in V79 cells by F 11782, a catalytic inhibitor of topoisomerases. Br. J. Cancer. 83:2000;1740-1746.
21. Barret J.M., Cadou M., Hill B.T. Inhibition of nucleotide excision repair and sensitisation of cells to DNA cross-linking anticancer drugs by F 11782, a novel fluorinated epipodophylloid. Biochem. Pharmacol. 63:2002;251-258.
22. Barret J.M., Kruczynski A., Etievant C., Hill B.T. Synergistic effects of F 11782, a novel dual inhibitor of topoisomerases I and II, in combination with other anticancer agents. Cancer Chemother. Pharmacol. 49:2002;479-486.
23. Wessel I., Jensen L.H., Renodon-Cornière A., Sorensen T.K., Nitiss J.L., Jensen P.B., Sehested M. Human small cell lung cancer NYH cells resistant to the bisdioxopiperazine ICRF-187 exhibit a functional dominant Tyr165Ser mutation in the Walker A ATP binding site of topoisomerase II alpha. FEBS Lett. 520:2002;161-166.
24. Sehested M., Wessel I., Jensen L.H., Holm B., Oliveri R.S., Kenwrick S., Creighton A.M., Nitiss J.L., Jensen P.B. Chinese hamster ovary cells resistant to the topoisomerase II catalytic inhibitor ICRF-159: a Tyr49Phe mutation confers high-level resistance to bisdioxopiperazines. Cancer Res. 58:1998;1460-1468.
25. Jensen P.B., Christensen I.J., Sehested M., Hansen H.H., Vindelov L. Differential cytotoxicity of 19 anticancer agents in wild-type and etoposide-resistant small cell lung cancer cell lines. Br. J. Cancer. 67:1993;311-320.
26. Wasserman R.A., Austin C.A., Fisher L.M., Wang J.C. Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant human DNA topoisomerase II alpha in yeast. Cancer Res. 53:1993;3591-3596.
27. Wessel I., Jensen L.H., Jensen P.B., Falck J., Rose A., Roerth M., Nitiss J.L., Sehested M. Human small cell lung cancer NYH cells selected for resistance to the bisdioxopiperazine topoisomerase II catalytic inhibitor ICRF-187 demonstrate a functional R162Q mutation in the Walker A consensus ATP binding domain of the alpha isoform. Cancer Res. 59:1999;3442-3450.
28. Sahai B.M., Kaplan J.G. A quantitative decatenation assay for type II topoisomerases. Anal. Biochem. 156:1986;364-379.
29. Renodon-Cornière A., Jensen L.H., Nitiss J.L., Jensen P.B., Sehested M. Interaction of human DNA topoisomerase II alpha with DNA: quantification by surface plasmon resonance. Biochemistry. 41:2002;13395-13402.
30. Morris S.K., Baird C.L., Lindsley J.E. Steady-state and rapid kinetic analysis of topoisomerase II trapped as the closed-clamp intermediate by ICRF-193. J. Biol. Chem. 275:2000;2613-2618.
31. Jensen L.H., Nitiss K.C., Rose A., Dong J., Zhou J., Hu T., Osheroff N., Jensen P.B., Sehested M., Nitiss J.L. A novel mechanism of cell killing by antitopoisomerase II bisdioxopiperazines. J. Biol. Chem. 275:2000;2137-2146.
32. Morris S.K., Harkins T.T., Tennyson R.B., Lindsley J.E. Kinetic and thermodynamic analysis of mutant type II DNA topoisomerases that cannot covalently cleave DNA. J. Biol. Chem. 274:1999;3446-3452.
33. Roca J., Ishida R., Berger J.M., Andoh T., Wang J.C. Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. U.S.A. 91:1994;1781-1785.
34. Roca J., Wang J.C. The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell. 71:1992;833-840.
35. Lee M.P., Hsieh T. Incomplete reversion of double stranded DNA cleavage mediated by Drosophila topoisomerase II: formation of single stranded DNA cleavage complex in the presence of an antitumour drug VM26. Nucleic Acids Res. 20:1992;5027-5033.
36. van Hille B., Etievant C., Barret J.M., Kruczynski A., Hill B.T. Characterization of the biological and biochemical activities of F 11782 and the bisdioxopiperazines, ICRF-187 and ICRF-193, two types of topoisomerase II catalytic inhibitors with distinctive mechanisms of action. Anticancer Drugs. 11:2000;829-841.
37. Kruczynski A., Ricome C., Waud W.R., Hill B.T. In vivo antitumor activity of F 11782, a non-intercalating dual catalytic inhibitor of topoisomerases I and II, against a panel of human tumour xenografts. J. Exp. Ther. Oncol. 2:2002;219-227.