Thiols alter the partitioning of calicheamicin-induced deoxyribose 4′-oxidation reactions in the absence of DNA radical repair

Chemical Research in Toxicology

Volumn 14, Issue 5, 2001, Pages 528-535

  Lopez Larraza, Daniel M ^a,b   Moore Jr , Kenneth ^a,c   Dedon, Peter C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Instituto Multidisciplinario de Biologia Celular   (Argentina)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' PHOSPHOGLYCOLATE; 4' DEOXYRIBOSE; 4' KETO 1' ALDEHYDE; ALDEHYDE DERIVATIVE; CALICHEAMICIN; DEOXYRIBOSE; DITHIOTHREITOL; DNA; GLYCOLIC ACID DERIVATIVE; MERCAPTOETHANOL; NUCLEIC ACID BASE; O ETHYLGLUTATHIONE; PHOSPHATE; RNA; SINGLE STRANDED DNA; THIOGLYCOLIC ACID METHYL ESTER; THIOL DERIVATIVE; UNCLASSIFIED DRUG; ZINOSTATIN;

ARTICLE; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; DNA DAMAGE; DNA REPAIR; OXIDATION; PARTITION COEFFICIENT;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; DEOXYRIBOSE; DNA DAMAGE; DNA REPAIR; DNA TOPOISOMERASES, TYPE I; ENEDIYNES; FREE RADICAL SCAVENGERS; OXIDATION-REDUCTION; PLASMIDS; SULFHYDRYL COMPOUNDS;

EID: 0035008498     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx0100082     Document Type: Article

References (47)

1. Alper, T., and Howard-Flanders, P. (1956) Role of oxygen in modifying the radiosensitivity of E. coli B. Nature 178, 978-979.
2. Willson, R. L. (1971) Pulse radiolysis studies on reaction of triacetoneamine-N-oxyl with radiation-induced free radicals. Trans. Faraday Soc. 67, 3008-3019.
3. Held, K. D., Harrop, H. A., and Michael, B. D. (1984) Effects of oxygen and sulphydryl-containing compounds on irradiated transforming DNA. III. Reaction rates. Int. J. Radiat. Biol. 45, 627-636.
4. Prise, K. M., Gillies, N. E., Whelan, A., Newton, G. L., Fahey, R. C., and Michael, B. D. (1995) Role of charge in the radioprotection of E. coli by thiols. Int. J. Radiat. Biol. 67, 393-401.
5. Fahey, R. C., Prise, K. M., Stratford, M. R. L., Watfa, R. R., and Michael, B. D. (1991) Rates of repair of pBR322 DNA radicals by thiols as measured by the gas exploson technique: evidence that counter-ion condensation and co-ion depletion are significant at physiological ionic strength. Int. J. Radiat. Biol. 59, 901-907.
6. Dussy, A., Meggers, E., and Giese, B. (1998) Spontaneous cleavage of 4′-DNA radicals under aerobic conditions: Apparent discrepancy between trapping rates and cleavage products. J. Am. Chem. Soc. 120, 7399-7403.
7. Kappen, L. S., Goldberg, I. H., Frank, B. L., Worth, L. J., Christner, D. F., Kozarich, J. W., and Stubbe, J. (1991) Neocarzinostatin-induced hydrogen atom abstraction from C-4′ and C-5′ of the T residue at a d(GT) step in oligonucleotides: shuttling between deoxyribose attack sites based on isotope selection effects. Biochemistry 30, 2034-2042.
8. Dedon, P. C., and Goldberg, I. H. (1992) Influence of thiol structure on neocarzinostatin activation and expression of DNA damage. Biochemistry 31, 1909-1917.
9. Epstein, J. L., Zhang, X., Doss, G. A., Liesch, J. M., Krishnan, B., Stubbe, J., and Kozarich, J. W. (1997) Interplay of hydrogen abstraction and radical repair in the generation of single- and double-strand DNA damage by the esperamicins. J. Am. Chem. Soc. 119, 6731-6738.
10. Chin, D.-H., and Goldberg, I. H. (1992) Internal hydrogen abstraction by activated neocarzinostatin: Quenching of the radical at C2 by hydrogen atom transfer from the a carbon of the adducted thiol. J. Am. Chem. Soc. 114, 1914-1915.
11. Dedon, P. C., and Goldberg, I. H. (1992) Free-radical mechanisms involved in the formation of sequence-dependent bistranded DNA lesions by the antitumor antibiotics bleomycin, neocarzinostatin, and calicheamicin. Chem. Res. Toxicol. 5, 311-332.
12. Doyle, T. W., and Borders, D. B. (1995) Enediyne antitumor antibiotics. In Enediyne Antibiotics as Antitumor Agents (Borders, D. B., and Doyle, T. W., Eds.) pp 1-15, Marcel Dekker, New York.
13. Dedon, P. C., Salzberg, A. A., and Xu, J. (1993) Exclusive production of bistranded DNA damage by calicheamicin. Biochemistry 32, 3617-3622.
14. Dedon, P. C., and Goldberg, I. H. (1990) Sequence-specific double-strand breakage of DNA by neocarzinostatin within a staggered cleavage site. J. Biol. Chem. 265, 14713-14716.
15. I and DNA: molecular recognition process responsible for site-specificity. Science 244, 697-699.
16. I. J. Am. Chem. Soc. 114, 9200-9202.
17. Fahey, R. C., Vojnovic, B., and Michael, B. D. (1991) The effects of counter-ion condensation and co-ion depletion upon the rates of chemical repair of poly(U) radicals by thiols. Int. J. Radiat. Biol. 59, 885-899.
18. Zheng, S., Newton, G. L., Ward, J. F., and Fahey, R. C. (1992) Aerobic radioprotection of pBR322 by thiols: Effect of thiol net charge upon scavenging of hydroxyl radicals and repair of DNA radicals. Radiat. Res. 130, 183-193.
19. Dedon, P. C., Jiang, Z.-W., and Goldberg, I. H. (1992) Neocarzinostatin-mediated DNA damage in a model AGT·ACT site: mechanistic studies of thiol-sensitive partitioning of C4′ DNA damage products. Biochemistry 31, 1917-1927.
20. Kappen, L. S., and Goldberg, I. H. (1992) Neocarzinostatin acts as a sensitive probe of DNA microheterogeneity: Switching of chemistry from C-1′ to C-4′ by a G·T mismatch 5′ to the site of DNA damage. Proc. Natl. Acad. Sci. U.S.A. 89, 6706-6710.
21. McAfee, S. E., and Ashley, G. W. (1992) Modulation of neocarzinostatin-mediated DNA double-strand damage by activated thiol: Deuterium isotope effects. Nucleic Acids Res. 20, 805-809.
22. 1: A rationally designed molecule with extremely potent and selective DNA cleaving properties and apoptosis inducing activity. Angew. Chem., Int. Ed. 33, 183-186.
23. LaMarr, W. A., Sandman, K. M., Reeve, J. N., and Dedon, P. C. (1997) Differential effects of DNA supercoiling on radical-mediated DNA strand breaks. Chem. Res. Toxicol. 10, 1118-1122.
24. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (1989) Current Protocols in Molecular Biology, John Wiley and Sons, New York.
25. Dedon, P. C. (2000) Protocols for the determination of binding mode: intercalation. In Current Protocols in Nucleic Acid Chemistry (Bergstrom, D., Ed.) John Wiley and Sons, New York.
26. Sugiyama, H., Xu, C., Murugesan, N., and Hecht, S. M. (1985) Structure of the alkali-labile product formed during iron(II)-bleomycin-mediated DNA strand scission. J. Am. Chem. Soc. 107, 4104-4105.
27. Povirk, L. F., and Houlgrave, C. W. (1988) Effect of apurinic/ apyrimidinic endonucleases and polyamines on DNA treated with bleomycin and neocarzinostatin: specific formation and cleavage of closely opposed lesions in complementary strands. Biochemistry 27, 3850-3857.
28. Lindahl, T., and Andersson, A. (1972) Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry 11, 3618-3623.
29. LaMarr, W. A., Nicolaou, K. C., and Dedon, P. C. (1998) Supercoiling affects the accessibility of glutathione to DNA-bound molecules: Positive supercoiling inhibits calicheamicin-induced DNA damage. Proc. Natl. Acad. Sci. U.S.A. 95, 102-107.
30. I complex. J. Am. Chem. Soc. 112, 9669-9670.
31. I: an antitumor antibiotic that cleaves double-stranded DNA site specifically. Science 240, 1198-1201.
32. 1 and calicheamicin T. Proc. Natl. Acad. Sci. U.S.A. 89, 4608-4612.
33. Liang, Q., Choi, D.-J., and Dedon, P. C. (1997) Calicheamicin-induced DNA damage in a reconstituted nucleosome is not affected by histone acetylation: Role of drug structure in the target recognition process. Biochemistry 36, 12653-12659.
34. Christner, D. F., Frank, B. L., Kozarich, J. W., Stubbe, J., Golik, J., Doyle, T. W., Rosenberg, I. E., and Krishnan, B. (1992) Unmasking the chemistry of DNA cleavage by the esperamicins: Modulation of 4′-hydrogen abstraction and bistranded damage by the fucose-anthranilate moiety. J. Am. Chem. Soc. 114, 8763-8767.
35. Mathur, P., Xu, J., and Dedon, P. C. (1997) Cytosine methylation enhances DNA damage produced by groove binding and intercalating enediynes: Studies with esperamicins A1 and C. Biochemistry 36, 14868-14873.
36. Yu, L., Golik, J., Harrison, R., and Dedon, P. (1994) The deoxyfucose-anthranilate of esperamicin A1 confers intercalative DNA binding and causes a switch in the chemistry of bistranded DNA lesions. J. Am. Chem. Soc. 116, 9733-9738.
37. Kappen, L. S., Goldberg, I. H., Wu, S. H., Stubbe, A., Worth, L., and Kozarich, J. W. (1990) Isotope effects on the sequence-specific cleavage of dC in d(AGC) sequences by neocarzinostatin: elucidation of chemistry of minor lesions. J. Am. Chem. Soc. 112, 2797-2798.
38. Maxam, A., and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65, 499-560.
39. Kappen, L. S., and Goldberg, I. H. (1992) Mismatch-induced switch of neocarzinostatin attack sites in the DNA minor groove. Biochemistry 31, 9081-9089.
40. Zheng, S., Newton, G. L., Gonick, G., Fahey, R. C., and Ward, J. F. (1988) Radioprotection of DNA by thiols: Relationship between the net charge of a thiol and its ability to protect DNA. Radiat. Res. 114, 11-27.
41. Paloma, L. G., Smith, J. A., Chazin, W. J., and Nicolaou, K. C. (1994) Interaction of calicheamicin with duplex DNA: Role of the oligosaccharide domain and identification of multiple binding modes. J. Am. Chem. Soc. 116, 3697-3708.
42. I-DNA complex. J. Mol. Biol. 265, 187-201.
43. I bound to DNA. Tetrahedron 50, 1351-1360.
44. Henner, W. D., Rodriguez, L. O., Hecht, S. M., and Haseltine, W. A. (1983) γ-Ray induced deoxyribonucleic acid strand breaks. 3′ Glycolate termini. J. Biol Chem. 258, 711-713.
45. Balasubramanian, B., Pogozelski, W. K., and Tullius, T. D. (1998) DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl. Acad. Sci. U.S.A. 95, 9738-9743.
46. Stubbe, J., and Kozarich, J. W. (1987) Mechanisms of bleomycin-induced DNA degradation. Chem. Rev. 87, 1107-1136.
47. Steighner, R. J., and Povirk, L. F. (1990) Bleomycin-induced DNA lesions at mutational hot spots: Implications for the mechanism of double-strand cleavage. Proc. Natl. Acad. Sci. U.S.A. 87, 8350-8354.