The power and potential of doxorubicin-DNA adducts

IUBMB Life

Volumn 57, Issue 2, 2005, Pages 73-81

  Cutts, Suzanne M ^a   Nudelman, Abraham ^b   Rephaeli, Ada ^c   Phillips, Don R ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b BAR ILAN UNIVERSITY   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Anthracyclines; Anticancer drugs; Doxorubicin; Doxorubicin DNA adducts; Formaldehyde; Formaldehyde releasing prodrugs

Indexed keywords

AN 158; AN 188; AN 37; AN 38; AN 7; AN 88; CELL DNA; DAUNOFORM; DNA METHYLTRANSFERASE; DOXOFORM; DOXORUBICIN; DOXORUBICIN DERIVATIVE; EPIDOXOFORM; FORMALDEHYDE; METHENAMINE; PIVALOYLOXYMETHYL BUTYRATE; PRODRUG; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; BASE MISPAIRING; CANCER INHIBITION; CANCER RESISTANCE; CELL STRAIN MCF 7; DNA ADDUCT; DRUG CYTOTOXICITY; DRUG DNA BINDING; DRUG STABILITY; ENZYME INHIBITION; HUMAN; IC 50; NONHUMAN; REVIEW; STRUCTURE ACTIVITY RELATION;

ANTHRACYCLINES; DNA ADDUCTS; DOXORUBICIN; FORMALDEHYDE; HUMANS; MODELS, MOLECULAR; NEOPLASMS; PRODRUGS;

EID: 18244369481     PISSN: 15216543     EISSN: None     Source Type: Journal    
DOI: 10.1080/15216540500079093     Document Type: Review

References (57)

1. Arcamone, F. (1982) Doxorubicin: Anticancer Antibiotics. Academic Press, San Diego.
2. Lown, J. W. (1988) Anthracycline and Anthracenedione-based Anticancer Agents. Elsevier, Amsterdam.
3. DeVita, V. T., Hellman, S. and Rosenberg, S. A. (2001) Cancer: Principles and Practice of Oncology, 6th ed. Lippincott Williams and Wilkins, Baltimore.
4. Weiss, R. B. (1992) The anthracyclines: will we ever find a better doxorubicin? Seminars Oncol. 19, 670-686.
5. Phillips, D. R., Greif, P. C., and Boston, R. C. (1988) Daunomycin-DNA dissociation kinetics. Mol. Pharmacol. 33, 8, 225-230.
6. Phillips, D. R., and Cullinane, C. (1999) Adriamycin. In Encyclopedia of Molecular Biology, vol. 1 (Creighton, T. E., ed.). pp. 68-72. John Wiley and Sons, New York.
7. Gewirtz, D. A. (1999) A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics Adriamycin and daunorubicin. Biochem. Pharmacol. 57, 727-741.
8. Minotti, G., Menna, P., Salvatorelli, E., Cairo, G., and Gianni, L. (2004) Anthracyclines: Molecular advances and pharmacologic development in antitumor activity and cardiotoxicity. Pharmacol. Rev. 56, 185-229.
9. Wilstermann, A. M., and Osheroff, N. (2003) Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem. 3, 321-338.
10. Sordet, O., Khan, Q. A., Kohn, K. W., and Pommier, Y. (2003) Apoptosis induced by topoisomerase inhibitors. Curr. Med. Chem. Anti-Canc. Agents 3, 271-290.
11. Larsen, A. K., Escargueil, A. E., and Skladanowski, A. (2003) Catalytic topoisomerase II inhibitors in cancer therapy. Pharmacol. Ther. 99, 167-181.
12. Scherf, U., Ross, D. T., Waltham, M., Smith, L. H., Lee, J. K., Tanabe, L., Kohn, K. W., Reinhold, W. C., Myers, T. G., Andrews, D. T., Scudiero, D. A., Eisen, M. B., Sausville, E. A., Pommier, Y., Botstein, D., Brown, P. O., and Weinstein, J. N. (2000) A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 24, 236-244.
13. Cutts, S. M., Rephaeli, A., Nudelman, A., Hmelnitsky, I., and Phillips, D. R. (2001) Molecular basis for the synergistic interaction of Adriamycin with the formaldehyde-releasing prodrug pivaloyloxymethyl butyrate (AN-9). Cancer Res. 61, 8194-8202.
14. Yokochi, T., and Robertson, K. D. (2004) Doxorubicin inhibits DNMT1 resulting in conditional apoptosis. Mol. Pharmacol., 66, 1415-1420.
15. Myers, C. E., Mimnaugh, E. G., Yen, G. C. and Sinha, B. K. (1988) Biochemical mechanisms of tumor cell kill by the anthracyclines. In Anthracycline and Anthracenedione-Based Anticancer Agents (Lown, J. W. ed.), p. 527. Elsevier, Amsterdam.
16. Phillips, D. R., Cullinane, C., Trist, H., and White, R. J. (1990) In vitro transcription analysis of the sequence specificity of reversible and irreversible complexes of adriamycin with DNA. In Molecular Basis of Specificity in Nucleic Acid-Drug Interactions (Pullman, B. and Jortner, J., eds). Pp. 137-155. Kluwer Academic Publishers, Dordrecht, The Netherlands.
17. Cummings, J., Anderson, L., Willmott, N., and Smyth, J. F. (1991) The molecular pharmacology of doxorubicin in vivo. Eur. J. Cancer 27, 532-535.
18. Cullinane, C., and Phillips, D. R. (1990) Induction of stable transcriptional blockage sites by Adriamycin: GpC specificity of apparent Adriamycin-DNA adducts and dependence on iron(III) ions. Biochemistry 29, 5638-5646.
19. Cullinane, C., van Rosmalen, A., and Phillips, D. R. (1994) Does Adriamycin induce interstrand crosslinks in DNA? Biochemistry 33, 4632-4638.
20. Cutts, S. M., and Phillips, D. R. (1995) Use of oligonucleotides to define the site of interstrand crosslinks induced by Adriamycin. Nucleic Acids Res. 23, 2450-2456.
21. Skladanowski, A., and Konopa, J. (1994) Interstrand DNA cross-linking induced by anthracyclines in tumour cells. Biochem. Pharmacol. 47, 2269-2278.
22. Cullinane, C., Cutts, S. M., Panousis, C., and Phillips, D. R. (2000) Interstrand crosslinking by Adriamycin in nuclear and mitochondrial DNA of MCF-7 cells. Nucleic Acids Res. 28, 1019-1025.
23. Taatjes, D. J., Gaudiano, G., Resing, K., and Koch, T. H. (1996) Alkylation of DNA by the anthracycline, antitumor drugs adriamycin and daunomycin. J. Med. Chem. 39, 4135-4138.
24. Taatjes, D. J., Gaudiano, G., Resing, K., and Koch, T. H. (1997) Redox pathway leading to the alkylation of DNA by the anthracycline, antitumor drugs adriamycin and daunomycin. J. Med. Chem. 40, 1276-1286.
25. Zeman, S. M., Phillips, D. R., and Crothers, D. M. (1998) Characterisation of covalent Adriamycin-DNA adducts. Proc. Natl. Acad. Sci. USA 95, 11561-11565.
26. Luce, R. A., Sigurdsson, S. Th., and Hopkins, P. B. (1999) Quantification of formaldehyde-mediated covalent adducts of Adriamycin with DNA. Biochemistry 38, 8682-8690.
27. Wang, A. H., Gao, Y. G., Liaw, Y. C. and Li, Y. K. (1991) Formaldehyde cross-links daunorubicin and DNA efficiently: HPLC and X-ray diffraction studies. Biochemistry 30, 3812-3815.
28. Moufarij, M. A., Cutts, S. M., Neumann, G. M., Kimura, K.-I., and Phillips, D. R. (2001) Barminomycin functions as a potent preactivated analogue of Adriamycin. Chem. Biol. Interact. 138, 137-153.
29. Cutts, S. M., Parker, B. S., Swift, L. P., Kimura, K.-I., and Phillips, D. R. (2000) Structural requirements for the formation of anthracycline-DNA adducts. Anti-Cancer Drug Des. 15, 373-386.
30. Leng, F., Savkur, R., Fokt, I., Przewloka, T., Priebe, W., and Chaires, J. B. (1996) Base specific and regio-selective chemical crosslinking of daunorubicin to DNA. J. Am. Chem. Soc. 20, 4731-4738.
31. Chaires, J. B., Leng, F., Przewloka, T., Fokt, I., Ling, Y. H., Perez-Soler, R., and Priebe, W. (1997) Structure-based design of a new bisintercalating anthracycline antibiotic. J. Med. Chem. 40, 261-266.
32. Taatjes, D. J., Fenick, D. J., and Koch, T. H. (1999) Nuclear targeting and nuclear retention of anthracycline-formaldehyde conjugates implicates covalent bonding in the cytotoxic mechanism of anthracyclines. Chem. Res. Toxicol. 12, 588-596.
33. Cutts, S. M., Swift, L. P., Rephaeli, A., Nudelman, A., and Phillips, D. R. (2003) Sequence specificity of Adriamycin-DNA adducts in human tumour cells. Mol. Cancer Ther. 2, 661-670.
34. Konopa, J. (1983) Adriamycin and daunomycin induce interstrand DNA crosslinks in Hela S3 cells. Biochem. Biophys. Res. Commun. 110, 819-826.
35. van Rosmalen, A., Cullinane, C., Cutts, S. M., and Phillips, D. R. (1995) Stability of adriamycin-induced DNA adducts and interstrand crosslinks. Nucleic Acids Res. 23, 42-50.
36. Cullinane, C., Cutts, S. M., van Rosmalen, A., and Phillips, D. R. (1994) Formation of adriamycin-DNA adducts in vitro. Nucleic Acids Res. 22, 2296-2303.
37. Kato, S., Burke, P. J., Koch, T. H., and Bierbaum, V. M. (2001) Formaldehyde in human cancer cells: detection by preconcentration-chemical ionization mass spectrometry. Anal. Chem. 73, 2992-2997.
38. Kato, S., Burke, P. J., Fenick, D. J., Taatjes, D. J., Bierbaum, V. M., and Koch, T. H. (2000) Mass spectrometric measurement of formaldehyde generated in breast cancer cells upon treatment with anthracycline antitumor drugs. Chem. Res. Toxicol. 13, 509-516.
39. Fenick, D. J., Taatjes, D. J., and Koch, T. H. (1997) Doxoform and Daunoform: Anthracycline-formaldehyde conjugates toxic to resistant tumor cells. J. Med. Chem. 40, 2452-2461.
40. Burke, P. J., and Koch, T. H. (2001) Doxorubicin-formaldehyde conjugate, Doxoform: Induction of apoptosis relative to doxorubicin. Anticancer Res. 21, 2753-2760.
41. Taatjes, D. J., and Koch, T. H. (1999) Growth inhibition, nuclear uptake and retention of anthracycline-formaldehyde conjugates in prostate cancer cells relative to clinical anthracyclines. Anticancer Res. 19, 1201-1208.
42. Nudelman, A., Ruse, M., Aviram, A., Rabizadeh, E., Shaklai, M., Zimra, Y., and Rephaeli, A. (1992) Novel anticancer prodrugs of butyric acid. J. Med. Chem. 35, 687-694.
43. Nudelman, A., Gnizi, E., Katz, Y., Azulai, R., Cohen-Ohana, M., Zhuk, R., Sampson, S. R., Langzam, L., Fibach, E., Prus, E., Pugach, V., and Rephaeli A. (2001) Prodrugs of butyric acid. Novel derivatives possessing increased aqueous solubility and potential for treating cancer and blood diseases. Eur. J. Med. Chem. 36, 63-74.
44. Zimra, Y., Nudelman, A., Zhuk, R., Rabizadeh, E., Shaklai, M., Aviram, A., and Rephaeli A. (2000) Uptake of pivaloyloxymethyl butyrate into leukemic cells and its intracellular esterase-catalyzed hydrolysis. J. Cancer Res. Clin. Oncol. 126, 693-698.
45. Reid, T., Valone, F., Lipera, W., Irwin, D., Paroly, W., Natale, R., Sreedharan, S., Keer, H., Lum, B., Scappaticci, F., and Bhatnagar A. (2004) Phase II trial of the histone deacetylase inhibitor pivaloyloxymethyl butyrate (Pivanex, AN-9) in advanced non-small cell lung cancer. Lung Cancer 45, 381-386.
46. Kasukabe, T., Rephaeli, A., and Honma, Y. (1997) An anti-cancer derivative of butyric acid (pivaloyloxymethyl-butyrate) and daunorubicin cooperatively prolong survival of mice inoculated with monocytic leukemia cells. Br. J. Cancer 75, 850-854.
47. Phillips, D. R., Cutts, S. M., Rephaeli, A., and Nudelman, A. (2002) Aldehyde-releasing compounds. International Patent Number WO 02/28345 A2.
48. Cutts, S. M., Nudelman, A., Pillay, V., Spencer, D. M. S., Levovich, I., Rephaeli, A., and Phillips, D. R. Formaldehyde-releasing prodrugs in combination with Adriamycin can overcome cellular drug resistance, in press.
49. Swift, L. P., Cutts, S. M., Rephaeli, A. Nudelman, A., and Phillips, D. R. (2003) Activation of Adriamycin by the pH dependent formaldehyde-releasing prodrug hexamethylenetetramine. Mol. Cancer Ther. 2, 189-198.
50. Dernell, W. S., Powers, B. E., Taatjes, D. J., Cogan, P., Gaudiano, G., and Koch, T. H. (2002) Evaluation of the epidoxorubicin-formaldehyde conjugate, epidoxoform, in a mouse mammary carcinoma model. Cancer Investig. 20, 712-723.
51. Skladanowski, A., and Konopa, J. (1994) Relevance of interstrand DNA crosslinking induced by anthracyclines for their biological activity. Biochem. Pharmacol. 47, 2279-2287.
52. Cutts, S. M., Parsons, P. G., Sturm, R. A. and Phillips, D. R. (1996) Adriamycin-induced DNA adducts inhibit the DNA interactions of transcription factors and RNA polymerase. J. Biol. Chem. 271, 5422-5429.
53. Swift, L. (2004) Anthracycline-DNA adducts. PhD Thesis, La Trobe University.
54. Patnaik, A., Rowinsky, E. K., Villalona, M. A., Hammond, L. A., Britten, C. D., Siu, L. L., Goetz, A., Felton, S. A., Burton, S., Valone, F. H., and Eckhardt, S. G. (2002) A phase I study of pivaloyloxymethyl butyrate, a prodrug of the differentiating agent butyric acid in patients with advanced solid malignancies. Clin. Cancer Res. 8, 2142-2148.
55. Panousis, C., and Pietersz G. A. (1999) Monoclonal antibody-directed cytotoxic therapy: potential in malignant diseases of aging. Drugs Aging 15, 1-13.
56. Burke, P. J., and Koch, T. H. (2004) Design, synthesis and biological evaluation of doxorubicin-formaldehyde conjugates targeted to breast cancer cells. J. Med. Chem. 47, 1193-1206.
57. Cogan P. S., and Koch, T. H. (2003) Rational design and synthesis of androgen receptor-targeted nonsteroidal anti-androgen ligands for the tumor-specific delivery of a doxorubicin-formaldehyde conjugate. J. Med. Chem. 46, 5258-5270.