Localization of an Aminoacridine Antitumor Agent in a Type II Topoisomerase-DNA Complex

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1994 Nov 8

PMID 7971998

Citations 18

Authors

C H Freudenreich

K N Kreuzer

Affiliations

Soon will be listed here.

Abstract

Type II topoisomerases are the targets of several classes of chemotherapeutic agents that stabilize an intermediate of the catalytic cycle with the enzyme covalently linked to cleaved DNA. We have used 3-azido-AMSA [4'-(3-azido-9-acridinylamino)methanesulfon-m-anisidide], a photo-activatible analog of the inhibitor m-AMSA [4'-(9-acridinylamino)methanesulfon-m-anisidide], to localize the inhibitor binding site in a cleavage complex consisting of an oligonucleotide substrate and the bacteriophage T4 type II DNA topoisomerase. Upon photoactivation, the inhibitor covalently attached to the substrate only in the presence of topoisomerase. Sites of inhibitor attachment were detected by primer-extension analysis and by piperidine-induced cleavage of the covalently modified substrate. 3-Azido-AMSA reacted with bases immediately adjacent to the two phosphodiester bonds cleaved by the enzyme. Therefore, topoisomerase creates or stabilizes preferential binding sites for the inhibitor precisely at the two sites of DNA cleavage.

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References

Maxam A, Gilbert W . Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980; 65(1):499-560. DOI: 10.1016/s0076-6879(80)65059-9. View

Capranico G, Kohn K, Pommier Y . Local sequence requirements for DNA cleavage by mammalian topoisomerase II in the presence of doxorubicin. Nucleic Acids Res. 1990; 18(22):6611-9. PMC: 332618. DOI: 10.1093/nar/18.22.6611. View

Lockshon D, Morris D . Sites of reaction of Escherichia coli DNA gyrase on pBR322 in vivo as revealed by oxolinic acid-induced plasmid linearization. J Mol Biol. 1985; 181(1):63-74. DOI: 10.1016/0022-2836(85)90324-9. View

Maxwell A, Gellert M . Mechanistic aspects of DNA topoisomerases. Adv Protein Chem. 1986; 38:69-107. DOI: 10.1016/s0065-3233(08)60526-4. View

Clark J, Joyce C, Beardsley G . Novel blunt-end addition reactions catalyzed by DNA polymerase I of Escherichia coli. J Mol Biol. 1987; 198(1):123-7. DOI: 10.1016/0022-2836(87)90462-1. View

Drlica K, FRANCO R . Inhibitors of DNA topoisomerases. Biochemistry. 1988; 27(7):2253-9. DOI: 10.1021/bi00407a001. View

Shen L, Kohlbrenner W, Weigl D, Baranowski J . Mechanism of quinolone inhibition of DNA gyrase. Appearance of unique norfloxacin binding sites in enzyme-DNA complexes. J Biol Chem. 1989; 264(5):2973-8. View

Hsiang Y, Liu L . Evidence for the reversibility of cellular DNA lesion induced by mammalian topoisomerase II poisons. J Biol Chem. 1989; 264(17):9713-5. View

Shen L, Mitscher L, Sharma P, ODonnell T, Chu D, Cooper C . Mechanism of inhibition of DNA gyrase by quinolone antibacterials: a cooperative drug--DNA binding model. Biochemistry. 1989; 28(9):3886-94. DOI: 10.1021/bi00435a039. View

10.

Liu L . DNA topoisomerase poisons as antitumor drugs. Annu Rev Biochem. 1989; 58:351-75. DOI: 10.1146/annurev.bi.58.070189.002031. View

11.

Sullivan D, Latham M, Rowe T, Ross W . Purification and characterization of an altered topoisomerase II from a drug-resistant Chinese hamster ovary cell line. Biochemistry. 1989; 28(13):5680-7. DOI: 10.1021/bi00439a051. View

12.

Zwelling L, Hinds M, Chan D, Mayes J, Sie K, Parker E . Characterization of an amsacrine-resistant line of human leukemia cells. Evidence for a drug-resistant form of topoisomerase II. J Biol Chem. 1989; 264(28):16411-20. View

13.

DArpa P, Liu L . Topoisomerase-targeting antitumor drugs. Biochim Biophys Acta. 1989; 989(2):163-77. DOI: 10.1016/0304-419x(89)90041-3. View

14.

Shieh T, Hoyos P, Kolodziej E, Stowell J, Baird W, Byrn S . Properties of the nucleic acid photoaffinity labeling agent 3-azidoamsacrine. J Med Chem. 1990; 33(4):1225-30. DOI: 10.1021/jm00166a022. View

15.

Huff A, Ward 4th R, Kreuzer K . Mutational alteration of the breakage/resealing subunit of bacteriophage T4 DNA topoisomerase confers resistance to antitumor agent m-AMSA. Mol Gen Genet. 1990; 221(1):27-32. DOI: 10.1007/BF00280363. View

16.

De Isabella P, Capranico G, Zunino F . The role of topoisomerase II in drug resistance. Life Sci. 1991; 48(23):2195-205. DOI: 10.1016/0024-3205(91)90333-7. View

17.

Fosse P, Rene B, Le Bret M, Paoletti C, Saucier J . Sequence requirements for mammalian topoisomerase II mediated DNA cleavage stimulated by an ellipticine derivative. Nucleic Acids Res. 1991; 19(11):2861-8. PMC: 328243. DOI: 10.1093/nar/19.11.2861. View

18.

Reece R, Maxwell A . DNA gyrase: structure and function. Crit Rev Biochem Mol Biol. 1991; 26(3-4):335-75. DOI: 10.3109/10409239109114072. View

19.

Jaxel C, Capranico G, Kerrigan D, Kohn K, Pommier Y . Effect of local DNA sequence on topoisomerase I cleavage in the presence or absence of camptothecin. J Biol Chem. 1991; 266(30):20418-23. View

20.

Pommier Y, Capranico G, Orr A, Kohn K . Local base sequence preferences for DNA cleavage by mammalian topoisomerase II in the presence of amsacrine or teniposide. Nucleic Acids Res. 1991; 19(21):5973-80. PMC: 329055. DOI: 10.1093/nar/19.21.5973. View