On the structural basis and design guidelines for type II topoisomerase-targeting anticancer drugs

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10630-10640

  Wu, Chyuan Chuan ^a   Li, Yi Ching ^a,b   Wang, Ying Ren ^a   Li, Tsai Kun ^a,c   Chan, Nei Li ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMETANTRONE; AMSACRINE; ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE (ATP HYDROLYSING); DOXORUBICIN; ETOPOSIDE; MITOXANTRONE;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA CLEAVAGE; DNA FRAGMENTATION; DRUG DNA BINDING; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; INTERCALATION COMPLEX; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

AMSACRINE; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; DRUG DESIGN; GUIDELINES AS TOPIC; HUMANS; MITOXANTRONE; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP; TOPOISOMERASE II INHIBITORS;

EID: 84890387239     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt828     Document Type: Article

References (40)

1. Wang, J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 3, 430-440.
2. Schoeffler, A.J. and Berger, J.M. (2008) DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys., 41, 41-101.
3. Vos, S.M., Tretter, E.M., Schmidt, B.H. and Berger, J.M. (2011) All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol., 12, 827-841.
4. Hartman Chen, S., Chan, N.L. and Hsieh, T.S. (2013) New mechanistic and functional insights into DNA topoisomerases. Annu. Rev. Biochem., 82, 139-170.
5. Schmidt, B.H., Osheroff, N. and Berger, J.M. (2012) Structure of a topoisomerase II-DNA-nucleotide complex reveals a new control mechanism for ATPase activity. Nat. Struct. Mol. Biol., 19, 1147-1154.
6. Deweese, J.E. and Osheroff, N. (2009) The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res., 37, 738-748.
7. McClendon, A.K. and Osheroff, N. (2007) DNA topoisomerase II, genotoxicity, and cancer. Mutat. Res., 623, 83-97.
8. Nitiss, J.L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer, 9, 338-350.
9. Pommier, Y., Leo, E., Zhang, H. and Marchand, C. (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol., 17, 421-433.
10. Wu, C.C., Li, T.K., Farh, L., Lin, L.Y., Lin, T.S., Yu, Y.J., Yen, T.J., Chiang, C.W. and Chan, N.L. (2011) Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide. Science, 333, 459-462.
11. Laponogov, I., Sohi, M.K., Veselkov, D.A., Pan, X.S., Sawhney, R., Thompson, A.W., McAuley, K.E., Fisher, L.M. and Sanderson, M.R. (2009) Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat. Struct. Mol. Biol., 16, 667-669.
12. Laponogov, I., Pan, X.S., Veselkov, D.A., McAuley, K.E., Fisher, L.M. and Sanderson, M.R. (2010) Structural basis of gate-DNA breakage and resealing by type II topoisomerases. PLoS One, 5, e11338.
13. Wohlkonig, A., Chan, P.F., Fosberry, A.P., Homes, P., Huang, J., Kranz, M., Leydon, V.R., Miles, T.J., Pearson, N.D., Perera, R.L. et al. (2010) Structural basis of quinolone inhibition of type IIA topoisomerases and target-mediated resistance. Nat. Struct. Mol. Biol., 17, 1152-1153.
14. Azarova, A.M., Lyu, Y.L., Lin, C.P., Tsai, Y.C., Lau, J.Y., Wang, J.C. and Liu, L.F. (2007) Roles of DNA topoisomerase II isozymes in chemotherapy and secondary malignancies. Proc. Natl Acad. Sci.USA, 104, 11014-11019.
15. Lyu, Y.L., Kerrigan, J.E., Lin, C.P., Azarova, A.M., Tsai, Y.C., Ban, Y. and Liu, L.F. (2007) Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res., 67, 8839-8846.
16. Seiter, K. (2005) Toxicity of the topoisomerase II inhibitors. Expert Opin. Drug Saf., 4, 219-234.
17. Denny, W.A. (2002) Acridine derivatives as chemotherapeutic agents. Curr. Med. Chem., 9, 1655-1665.
18. Demeunynck, M., Charmantray, F. and Martelli, A. (2001) Interest of acridine derivatives in the anticancer chemotherapy. Curr. Pharm. Des., 7, 1703-1724.
19. Ketron, A.C., Denny, W.A., Graves, D.E. and Osheroff, N. (2012) Amsacrine as a topoisomerase II poison: importance of drug-DNA interactions. Biochemistry, 51, 1730-1739.
20. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr., 276(Pt A), 307-326.
21. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
22. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
23. Schrodinger, L.L.C. (2010), The PyMOL Molecular Graphics System, Version 1.3r1.
24. Dong, K.C. and Berger, J.M. (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature, 450, 1201-1205.
25. Wendorff, T.J., Schmidt, B.H., Heslop, P., Austin, C.A. and Berger, J.M. (2012) The structure of DNA-bound human topoisomerase II alpha: conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage. J. Mol. Biol., 424, 109-124.
26. Liu, L.F. (1989) DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem., 58, 351-375.
27. Zheng, S., Chen, Y., Donahue, C.P., Wolfe, M.S. and Varani, G. (2009) Structural basis for stabilization of the tau pre-mRNA splicing regulatory element by novantrone (mitoxantrone). Chem Biol, 16, 557-566.
28. Leontiou, C., Lakey, J.H. and Austin, C.A. (2004) Mutation E522K in human DNA topoisomerase IIbeta confers resistance to methyl N-(4'-(9-acridinylamino)- phenyl)carbamate hydrochloride and methyl N-(4'-(9-acridinylamino)-3-methoxy- phenyl) methane sulfonamide but hypersensitivity to etoposide. Mol. Pharmacol., 66, 430-439.
29. Wasserman, R.A. and Wang, J.C. (1994) Analysis of yeast DNA topoisomerase II mutants resistant to the antitumor drug amsacrine. Cancer Res., 54, 1795-1800.
30. Alderton, P.M., Gross, J. and Green, M.D. (1992) Comparative study of doxorubicin, mitoxantrone, and epirubicin in combination with ICRF-187 (ADR-529) in a chronic cardiotoxicity animal model. Cancer Res., 52, 194-201.
31. Kapuscinski, J. and Darzynkiewicz, Z. (1985) Interactions of antitumor agents Ametantrone and Mitoxantrone (Novatrone) with double-stranded DNA. Biochem. Pharmacol., 34, 4203-4213.
32. De Isabella, P., Capranico, G., Palumbo, M., Sissi, C., Krapcho, A.P. and Zunino, F. (1993) Sequence selectivity of topoisomerase II DNA cleavage stimulated by mitoxantrone derivatives: relationships to drug DNA binding and cellular effects. Mol. Pharmacol., 43, 715-721.
33. De Isabella, P., Palumbo, M., Sissi, C., Capranico, G., Carenini, N., Menta, E., Oliva, A., Spinelli, S., Krapcho, A.P., Giuliani, F.C. et al. (1995) Topoisomerase II DNA cleavage stimulation, DNA binding activity, cytotoxicity, and physico-chemical properties of 2-aza-and 2-aza-oxide-anthracenedione derivatives. Mol. Pharmacol., 48, 30-38.
34. Lee, C.H., Hsieh, M.Y., Hsin, L.W., Chen, H.C., Lo, S.C., Fan, J.R., Chen, W.R., Chen, H.W., Chan, N.L. and Li, T.K. (2012) Anthracenedione- methionine conjugates are novel topoisomerase II-targeting anticancer agents with favorable drug resistance profiles. Biochem. Pharmacol., 83, 1208-1216.
35. Frederick, C.A., Williams, L.D., Ughetto, G., van der Marel, G.A., van Boom, J.H., Rich, A. and Wang, A.H. (1990) Structural comparison of anticancer drug-DNA complexes: adriamycin and daunomycin. Biochemistry, 29, 2538-2549.
36. Zhang, S., Liu, X., Bawa-Khalfe, T., Lu, L.S., Lyu, Y.L., Liu, L.F. and Yeh, E.T. (2012) Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med., 18, 1639-1642.
37. Cowell, I.G., Sondka, Z., Smith, K., Lee, K.C., Manville, C.M., Sidorczuk-Lesthuruge, M., Rance, H.A., Padget, K., Jackson, G.H., Adachi, N. et al. (2012) Model for MLL translocations in therapyrelated leukemia involving topoisomerase IIbeta-mediated DNA strand breaks and gene proximity. Proc. Natl Acad. Sci. USA, 109, 8989-8994.
38. Minotti, G., Menna, P., Salvatorelli, E., Cairo, G. and Gianni, L. (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev., 56, 185-229.
39. Howerton, S.B., Nagpal, A. and Williams, L.D. (2003) Surprising roles of electrostatic interactions in DNA-ligand complexes. Biopolymers, 69, 87-99.
40. Capranico, G., Kohn, K.W. and Pommier, Y. (1990) Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin. Nucleic Acids Res., 18, 6611-6619.