An antitumor drug-induced topoisomerase cleavage complex blocks a bacteriophage T4 replication fork in vivo

Molecular and Cellular Biology

Volumn 20, Issue 2, 2000, Pages 594-603

  Hong, George ^a   Kreuzer, Kenneth N ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BACTERIAL DNA; DNA TOPOISOMERASE;

ARTICLE; BACTERIOPHAGE T4; DNA CLEAVAGE; DNA DAMAGE; ENZYME INHIBITION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; VIRUS INHIBITION; VIRUS REPLICATION;

AMSACRINE; ANTINEOPLASTIC AGENTS; BACTERIOPHAGE T4; BASE SEQUENCE; BINDING SITES; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA REPAIR; DNA REPLICATION; DNA TOPOISOMERASES, TYPE II; DNA, VIRAL; ESCHERICHIA COLI; MUTATION; NUCLEIC ACID CONFORMATION; PLASMIDS; RECOMBINATION, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; REPLICATION ORIGIN; VIRUS REPLICATION;

BACTERIA (MICROORGANISMS);

EID: 0033970936     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.2.594-603.2000     Document Type: Article

References (68)

1. Bastia, D., and B. Mohanty. 1996. Mechanisms for completing replication, p. 177-215. In M. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
2. Belanger, K. G. 1997. Origin-dependent DNA replication in bacteriophage T4. Ph.D. thesis. Duke University, Durham, N.C.
3. Belanger, K. G., and K. N. Kreuzer. 1998. Bacteriophage T4 initiates bidirectional DNA replication through a two-step process. Mol. Cell 2:693-701.
4. Belanger, K. G., C. Mirzayan, H. E. Kreuzer, B. M. Alberts, and K. N. Kreuzer. 1996. Two-dimensional gel analysis of rolling circle replication in the presence and absence of bacteriophage T4 primase. Nucleic Acids Res. 24:2166-2175.
5. Berger, C. A., and H. J. Edenberg. 1996. Pyrimidine dimers block simian virus 40 replication forks. Mol. Cell. Biol. 6:3443-3450.
6. Berger, J. M. 1998. Type II DNA topoisomerases. Curr. Opin. Struct. Biol. 8:26-32.
7. Bierne, H., and B. Michel. 1994. When replication forks stop. Mol. Microbiol. 13:17-23.
8. Brewer, B. J., and W. L. Fangman. 1987. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51:463-471.
9. Brewer, B. J., D. Lockshon, and W. L. Fangman. 1992. The arrest of replication forks in the rDNA of yeast occurs independently of transcription. Cell 71:267-276.
10. Burden, D. A., and N. Osheroff. 1998. Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400:139-154.
11. Catapano, C. V., G. M. R. Carbone, F. Pisani, J. Qiu, and D. J. Fernandes. 1997. Arrest of replication fork progression at sites of topoisomerase II-mediated DNA cleavage in human leukemia CEM cells incubated with VM-26. Biochemistry 36:5739-5748.
12. Chakraverty, R. K., and I. D. Hickson. 1999. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays 21:286-294.
13. Chen, A. Y., and L. F. Liu. 1994. DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 34:191-218.
14. Cox, M. M. 1999. Recombinational DNA repair in bacteria and the RecA protein. Nucleic Acids Res. Mol. Biol. 63:310-366.
15. D'Arpa, P., C. Beardmore, and L. F. Liu. 1990. Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res. 50:6919-6924.
16. Defossez, P. A., R. Prusty, M. Kaeberlein, S. J. Lin, P. Ferrigno, P. A. Silver, R. L. Keil, and L. Guarente. 1999. Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell 3:447-455.
17. Drlica, K., and X. L. Zhao. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Rev. 61:377-392.
18. Eng, W.-K., L. Faucette, R. K. Johnson, and R. Sternglanz. 1989. Evidence that DNA topoisomerase I is necessary for the cytotoxic effects of camptothecin. Mol. Pharmacol. 34:755-760.
19. Freudenreich, C. H., and K. N. Kreuzer. 1993. Mutational analysis of a type II topoisomerase cleavage site: Distinct requirements for enzyme and inhibitors. EMBO J. 12:2085-2097.
20. Freudenreich, C. H., and K. N. Kreuzer. 1994. Localization of an amino-acridine antitumor agent in a type II topoisomerase-DNA complex. Proc. Natl. Acad. Sci. USA 91:11007-11011.
21. Friedman, K. L., and B. J. Brewer. 1995. Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol. 262:613-627.
22. George, J. W., and K. N. Kreuzer. 1996. Repair of double-strand breaks in bacteriophage T4 by a mechanism that involves extensive DNA replication. Genetics 143:1507-1520.
23. Greenfeder, S. A., and C. S. Newlon. 1992. Replication forks pause at yeast centromeres. Mol. Cell. Biol. 12:4056-4066.
24. Hane, M. W., and T. H. Wood. 1969. Escherichia coli K-12 mutants resistant to nalidixic acid: genetic mapping and dominance studies. J. Bacteriol. 99: 238-241.
25. Hiasa, H., D. O. Yousef, and K. J. Marians. 1996. DNA strand cleavage is required for replication fork arrest by a frozen topoisomerase-quinolone-DNA ternary complex. J. Biol. Chem. 271:26424-26429.
26. Hill, T. M. 1992. Arrest of bacterial DNA replication. Annu. Rev. Microbiol. 46:603-633.
27. Holm, C., J. M. Covey, D. Kerrigan, and Y. Pommier. 1989. Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res. 49:6365-6368.
28. Hooper, D. C. 1998. Clinical applications of quinolones. Biochim. Biophys. Acta 1400:45-61.
29. Howard, M. T., S. H. Neece, S. W. Matson, and K. N. Kreuzer. 1994. Disruption of a topoisomerase-DNA cleavage complex by a DNA helicase. Proc. Natl. Acad. Sci. USA 91:12031-12035.
30. Hsiang, Y.-H., and L. F. Liu. 1989. Evidence for the reversibility of cellular DNA lesion induced by mammalian topoisomerase II poisons. J. Biol. Chem. 264:9713-9715.
31. Huff, A. C., J. K. Leatherwood, and K. N. Kreuzer. 1989. Bacteriophage T4 DNA topoisomerase is the target of antitumor agent 4′-(9-acridinylamino) methanesulfon-m-anisidide (m-AMSA) in T4-infected Escherichia coli. Proc. Natl. Acad. Sci. USA 86:1307-1311.
32. Jeggo, P. A., K. Caldecott, S. Pidsley, and G. R. Banks. 1989. Sensitivity of Chinese hamster ovary mutants defective in DNA double strand break repair to topoisomerase II inhibitors. Cancer Res. 49:7057-7063.
33. Khodursky, A. B., and N. R. Cozzarelli. 1998. The mechanism of inhibition of topoisomerase IV by quinolone antibacterials. J. Biol. Chem. 273:27668-27677.
34. Kobayashi, T., and T. Horiuchi. 1996. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1:465-474.
35. Kreuzer, K. N., and B. M. Alberts. 1984. Site-specific recognition of bacteriophage T4 DNA by T4 type II DNA topoisomerase and Escherichia coli DNA gyrase. J. Biol. Chem. 259:5339-5346.
36. Kreuzer, K. N., and N. R. Cozzarelli. 1979. Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J. Bacteriol. 140:424-435.
37. Kreuzer, K. N., H. W. Engman, and W. Y. Yap. 1988. Tertiary initiation of replication in bacteriophage T4. Deletion of the overlapping uvsY promoter/ replication origin from the phage genome. J. Biol. Chem. 263:11348-11357.
38. Kreuzer, K. N., and S. W. Morrical. 1994. Initiation of DNA replication, p. 28-42. In J. D. Karam (ed.), Molecular biology of bacteriophage T4. ASM Press, Washington, D.C.
39. Kupfer, G., A. L. Bodley, and L. F. Liu. 1987. Involvement of intracellular ATP in cytotoxicity of topoisomerase II-targeting antitumor drugs. NCI Monogr. 4:37-40.
40. Kutter, E., and L. Snyder. 1983. Preparation of cytosine-containing T4 phage, p, 56-57. In C. K. Mathews, E. M. Kutter, G. Mosig, and P. B. Berget (ed.), Bacteriophage T4. ASM Press, Washington, D.C.
41. Kuzminov, A. 1995. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16:373-384.
42. Levine, C., H. Hiasa, and K. J. Marians. 1998. DNA gyrase and topoisomerase IV: Biochemical activities, physiological roles during chromosome replication, and drug sensitivities. Biochim. Biophys. Acta 1400:29-43.
43. Little, R. D., T. H. Platt, and C. L. Schildkraut. 1993. Initiation and termination of DNA replication in human rRNA genes. Mol. Cell. Biol. 13:6600-6613.
44. Liu, L. F. 1989. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58:351-375.
45. McCarthy, D. 1979. Gyrase-dependent initiation of bacteriophage T4 DNA replication: interactions of Escherichia coli gyrase with novobiocin, coumermycin and phage DNA-delay gene products. J. Mol. Biol. 127:265-283.
46. Menkens, A. E., and K. N. Kreuzer. 1988. Deletion analysis of bacteriophage T4 tertiary origins. J. Biol. Chem. 263:11358-11365.
47. Michel, B., S. D. Ehrlich, and M. Uzest. 1997. DNA double-strand breaks caused by replication arrest. EMBO J. 16:430-438.
48. Ming, Y. Z., X. Di, E. P. Gomez-Sanchez, and C. E. Gomez-Sanchez. 1994. Improved downward capillary transfer for blotting of DNA and RNA. Bio-Techniques 16:58-60.
49. Mueller, J. E., J. Clyman, Y. J. Huang, M. M. Parker, and M. Belfort. 1996. Intron mobility in phage T4 occurs in the context of recombination-dependent DNA replication by way of multiple pathways. Genes Dev. 10:351-364.
50. Neece, S. H., K. Carles-Kinch, D. J. Tomso, and K. N. Kreuzer. 1996. Role of recombinational repair in sensitivity to an antitumor agent that inhibits bacteriophage T4 type II DNA topoisomerase. Mol. Microbiol. 20:1145-1154.
51. Nelson, M. A., M. Ericson, L. Gold, and J. F. Pulitzer. 1982. The isolation and characterization of TabR bacteria: hosts that restrict bacteriophage T4 rII mutants. Mol. Gen. Genet. 188:60-68.
52. Nitiss, J., and J. C. Wang. 1988. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl. Acad. Sci. USA 85:7501-7505.
53. Nitiss, J. L., and J. C. Wang. 1996. Mechanisms of cell killing by drugs that trap covalent complexes between DNA topoisomerases and DNA. Mol. Pharmacol. 50:1095-1102.
54. Osheroff, N., and E. L. Zechiedrich. 1987. Calcium-promoted DNA cleavage by eukaryotic topoisomerase II: Trapping the covalent enzyme-DNA complex in an active form. Biochemistry 26:4303-4309.
55. Pommier, Y. 1993. DNA topoisomerase I and II in cancer chemotherapy: update and perspectives. Cancer Chemother. Pharmacol. 32:103-108.
56. Ripley, L. S., J. S. Dubins, J. G. deBoer, D. M. DeMarini, A. M. Bogerd, and K. N. Kreuzer. 1988. Hotspot sites for acridine-induced frameshift mutations in bacteriophage T4 correspond to sites of action of the T4 type II topoisomerase. J. Mol. Biol. 200:665-680.
57. Sander, M., and T.-S. Hsieh. 1983. Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258:8421-8428.
58. Sastry, S., and B. M. Ross. 1998. Mechanisms for the processing of a frozen topoisomerase-DNA conjugate by human cell-free extracts. J. Biol. Chem. 273:9942-9950.
59. Schneider, E., P. A. Lawson, and R. K. Ralph. 1989. Inhibition of protein synthesis reduces the cytotoxicity of 4′-(9-acridinylamino)methanesulfon-m-anisidide without affecting DNA breakage and DNA topoisomerase II in a murine mastocytoma cell line. Biochem. Pharmacol. 38:263-269.
60. Seigneur, M., V. Bidnenko, S. D. Ehrlich, and B. Michel. 1998. RuvAB acts at arrested replication forks. Cell 95:419-430.
61. Selick, H. E., K. N. Kreuzer, and B. M. Alberts. 1988. The bacteriophage T4 insertion/substitution vector system. A method for introducing site-specific mutations into the virus chromosome. J. Biol. Chem. 263:11336-11347.
62. Snustad, D. P., L. Snyder, and E. M. Kutter. 1983. Effects on host genome structure and expression, p. 40-57. In C. K. Mathews, E. M. Kutter, G. Mosig, and P. B. Berget (ed.), Bacteriophage T4. ASM Press, Washington, D.C.
63. Tewey, K. M., G. L. Chen, E. M. Nelson, and L. F. Liu. 1984. Intercalate antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259:9182-9187.
64. Villani, G., S. Boiteux, and M. Radman. 1978. Mechanism of ultraviolet-induced mutagenesis: Extent and fidelity of in vitro DNA synthesis on irradiated templates. Proc. Natl, Acad. Sci. USA 75:3037-3041.
65. Wang, J. C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635-692.
66. Wigley, D. B. 1995. Structure and mechanism of DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct. 24:185-208.
67. Wilson, W. R., and G. F. Whitmore. 1981. Cell-cycle-stage specificity of 4′-(9-acridinylamino)methanesulfon-m-anisidide (m-AMSA) and interaction with ionizing radiation in mammalian cell cultures. Radiat. Res. 87:121-136.
68. Yang, S. W., A. B. Burgin, Jr., B. N. Huizenga, C. A. Robertson, K. C. Yao, and H. A. Nash. 1996. A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc. Natl. Acad. Sci. USA 93:11534-11539.