Inhibition of topoisomerase II by the marine alkaloid ascididemin and induction of apoptosis in leukemia cells

Biochemical Pharmacology

Volumn 60, Issue 4, 2000, Pages 527-537

  Dassonneville, Laurent ^a   Wattez, Nicole ^a   Baldeyrou, Brigitte ^a   Mahieu, Christine ^a   Lansiaux, Amélie ^a   Banaigs, Bernard ^b   Bonnard, Isabelle ^b   Bailly, Christian ^a  

^a IRCL   (France)

^b UNIVERSITÉ DE PERPIGNAN   (France)

Author keywords

Antitumor agent; Apoptosis; Ascididemin; Cell cycle; DNA cleavage; Marine products; Topoisomerase

Indexed keywords

ANTINEOPLASTIC AGENT; ASCIDIDEMIN; CAMPTOTHECIN; DNA FRAGMENT; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); ETOPOSIDE; MITOXANTRONE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CELL STRAIN HL 60; CONTROLLED STUDY; CYTOTOXICITY; DNA CLEAVAGE; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL;

ALKALOIDS; ANIMALS; APOPTOSIS; DNA TOPOISOMERASES, TYPE I; DNA TOPOISOMERASES, TYPE II; HL-60 CELLS; HUMANS; LEUKEMIA; OCEANS AND SEAS; PHENANTHROLINES; PLANKTON; QUINOLINES; TUMOR CELLS, CULTURED;

EID: 0034664192     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(00)00351-8     Document Type: Article

References (42)

1. Bonnard I., Bontemps N., Lahmy S., Banaigs B., Combaut G., Francisco C., Colson P., Houssier C., Waring M.J., Bailly C. Binding to DNA and cytotoxic evaluation of ascididemin, the major alkaloid from the Mediterranean ascidian Cystodytes dellechiajei. Anticancer Drug Des. 10:1995;333-346.
2. Kobayashi J., Cheng J., Nakamura Y., Ohizumi Y., Hirata Y., Sasaki T., Otha T., Nozoe S. Ascididemin, a novel pentacyclic aromatic alkaloid with potent antileukemic activity from the Okinawan tunicate Didemnum sp. Tetrahedron Lett. 29:1988;1177-1180.
3. Bracher F. Polycyclic aromatic alkaloids. XII In vitro-and in vivo-investigations of the cytotoxic marine alkaloid 2-bromoleptoclinidone . Pharmazie. 52:1997;57-60.
4. Schmitz F.J., de Guzman F.S., Hossain M.B., van der Helm D. Cytotoxic aromatic alkaloids from the ascidian Amphicarpa meridiana and Leptoclinides sp. Meridine and 11-hydroxyascididemine . Chem. 56:1991;804-808.
5. Molinski T.F. Marine pyridoacridine alkaloids Structure, synthesis, and biological chemistry . Chem Rev. 93:1993;1825-1838.
6. Ding Q., Chichak K., Lown J.W. Pyrroloquinoline and pyridoacridine alkaloids from marine sources. Curr Med Chem. 6:1999;1-27.
7. Lindsay B., Barrows L., Copp B. Structural requirements for biological activity of the marine alkaloid ascididemin. Bioorg Med Chem Lett. 5:1995;739-742.
8. Wilson WD, DNA and RNA intercalators. In: DNA and Aspects of Molecular Biology (Ed. Kool E), Vol. 7, Chapter 12, Elsevier, Amsterdam, 1999.
9. Wang J.C. DNA topoisomerases. Annu Rev Biochem. 65:1996;635-691.
10. Burden D.A., Osheroff N. Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim Biophys Acta. 1400:1998;139-154.
11. Wang H.K., Morris-Natschke S.L., Lee K.H. Recent advances in the discovery and development of topoisomerase inhibitors as antitumor agents. Med Res Rev. 17:1997;367-425.
12. Fujii N., Yamashita Y., Saitoh Y., Nakano H. Induction of mammalian topoisomerase I-mediated DNA cleavage and DNA unwinding by bulgarein. J Biol Chem. 268:1993;13160-13165.
13. Gatto B., Sanders M.M., Yu C., Wu H.-Y., Makhey D., LaVoie E.J., Liu L.F. Identification of topoisomerase I as the cytotoxic target of the protoberherine alkaloid coralyne. Cancer Res. 56:1996;2795-2800.
14. Bailly C., Riou J.F., Colson P., Houssier C., Rodrigues-Pereira E., Prudhomme M. DNA cleavage by topoisomerase I in the presence of indolocarbazole derivatives of rebeccamycin. Biochemistry. 36:1997;3917-3929.
15. Makhey D., Gatto B., Yu C., Liu A., Liu L.F., LaVoie E. Protoberbine alkaloids and related compounds as dual inhibitors of mammalian topoisomerases I and II. Med Chem Res. 5:1994;1-12.
16. 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.
17. Riou J.F., Fossé P., Nguyen C.H., Larsen A.K., Bissery M.C., Grondard L., Saucier J.M., Bisagni E., Lavelle F. Intoplicine (RP 60475) and its derivatives, a new class of antitumor agents inhibiting both topoisomerase I and II activities. Cancer Res. 53:1993;5987-5993.
18. Leteurtre F., Fujimori A., Tanizawa A., Chabra A., Mazumder A., Kohlhagen G., Nakano H., Pommier Y. Saintopin, a dual inhibitor of topoisomerases I and II, as a probe for drug-enzyme interactions. J Biol Chem. 269:1994;28702-28707.
19. McDonald L.A., Eldredge G.S., Barrows L.R., Ireland C.M. Inhibition of topoisomerase II catalytic activity by pyridoacridine alkaloids from a Cystodytes sp. ascidian A mechanism for the apparent intercalator-induced inhibition of topoisomcrase II . Med Chem. 37:1994;3819-3827.
20. Kokoshka J.M., Capson T.L., Holden J.A., Ireland C.M., Barrows L.R. Differences in the topoisomerase I cleavage complexes formed by camptothecin and wakayin, a DNA-intercalating marine natural product. AntiCancer Drugs. 7:1996;758-765.
21. Bracher F. Total synthesis of the pentacyclic alkaloid ascididemin. Heterocycles. 29:1989;2093-2095.
22. Drew H.R., Weeks J.R., Travers A.A. Negative supercoiling induces unwinding of bacterial promoter. EMBO J. 4:1985;1025-1032.
23. Kerckaert J.P., Deweindt C., Tilly H., Quiet S., Lecocq G., Bastard C. LAZ3, a novel zinc-finger encoding gene, is disrupted by recurring chromosome 3q27 translocations in human lymphomas. Nat Genet. 5:1993;66-70.
24. Madelaine J., Prost S., Naudin A., Riou G., Lavelle F., Riou J.F. Sequential modifications of topoisomerase I activity in a camptothecin-resistant cell line established by progressive adaptation. Biochem Pharmacol. 45:1993;339-348.
25. Cory A.H., Owen T.C., Barltrop J.A., Cory J.G. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3:1991;207-212.
26. Papanicolaou G.N. A new procedure for staining vaginal smears. Science. 95:1942;438-439.
27. Ben-Sasson S.A., Sherman Y., Gavrieli Y. Identification of dying cells-in situ staining. Method Cell Biol. 46:1995;29-39.
28. Harker W.G., Slade D.L., Drake F.H., Parr R.L. Mitoxantrone resistance in HL-60 leukemia cells Reduced nuclear topoisomerase activity and drug-induced DNA cleavage in association with reduced expression of topoisomerase IIβ isoform . Biochemistry. 30:1991;9953-9961.
29. Dassonneville L., Bonjean K., De Pauw-Gillet M.C., Colson P., Houssier C., Quetin-Leclercq J., Angenot L., Bailly C. Stimulation of topoisomerase II-mediated DNA cleavage by three DNA-intercalating plant alkaloids Cryptolepine, matadine, and serpentine . Biochemistry. 38:1999;7719-7726.
30. Walker P.R., Smith C., Youdale T., Leblanc J., Whitfield J.F., Sikorska M. Topoisomerase II-reactive chemotheurapeutic drugs induce apoptosis in thymocytes. Cancer Res. 51:1991;1078-1085.
31. Solary E., Bertrand R., Kohn K.W., Pommier Y. Differential induction of apoptosis in undifferentiated and differentiated HL-60 cells by DNA topoisomerases I and II inhibitors. Blood. 81:1993;1359-1368.
32. Barry M.A., Reynolds J.E., Eastman A. Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res. 53:1993;2349-2357.
33. Bertrand R., Solary E., Jenkins J., Pommier Y. Apoptosis and its modulation in human promyelocytic HL-60 cells treated with DNA topoisomerase I and II inhibitors. Exp Cell Res. 207:1993;388-397.
34. Palissot V., Belhoussine R., Carpentier Y., Sebille S., Morjani H., Manfait M., Dufer J. Resistance to apoptosis induced by topoisomerase I inhibitors in multidrug-resistant HL60 leukemic cells. Biochem Biophys Res Commun. 245:1998;918-922.
35. Kaufman S.H. Cell death induced by topoisomerase-targeted drugs More questions than answers . Biochim Biophys Acta. 1400:1998;195-211.
36. Compton M.M. A biochemical hallmark of apoptosis Internucleosomal degradation of the genome . Cancer Metastasis Rev. 11:1992;105-119.
37. Woo S.H., Reynolds M.C., Sun N.J., Cassady J.M., Snapka R.M. Inhibition of topoisomerase II by liriodenine. Biochem Pharmacol. 54:1997;467-473.
38. Woo S.H., Sun N.J., Cassady J.M., Snapka R.M. Topoisomerase II inhibition by aporphine alkaloids. Biochem Pharmacol. 57:1999;1141-1145.
39. Yamashita Y., Kawada S.Z., Fujii N., Nakano H. Induction of mammalian topoisomerases I and II DNA cleavage by saintopin, a new aniitumor agent from fungus. Biochemistry. 30:1991;5838-5845.
40. Larsen A.K., Grondard L., Couprie J., Desoize B., Comoe L., Jardillier J.C., Riou J.F. The antileukemic alkaloid fagaronine is an inhibitor of DNA topoisomerases I and II. Biochem Pharmacol. 46:1993;1403-1412.
41. Capranico G., Binaschi M. DNA sequence selectivity of topoisomerases and topoisomerase poisons. Biochem Biophys Acta. 1400:1998;185-194.
42. Matsumoto S.S., Schmehl D.M., Copp B.R., Holden J.A., Barrows L.R. Mechanism of ascididemin cytotoxicity. Proc Am Assoc Cancer Res. 40:1999;A1914.