The interaction of the F plasmid killer protein, CcdB, with DNA gyrase: Induction of DNA cleavage and blocking of transcription

Journal of Molecular Biology

Volumn 273, Issue 4, 1997, Pages 826-839

  Critchlow, Susan E ^a   O'Dea, Mary H ^b   Howells, Alison J ^a   Couturier, Martine ^c   Gellert, Martin ^b   Maxwell, Anthony ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Quinolone; RNA polymerase; Supercoiling; Topoisomerase

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); QUINOLONE; RNA POLYMERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DNA CLEAVAGE; DNA SUPERCOILING; HYDROLYSIS; MOLECULAR INTERACTION; PLASMID; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

EID: 0031558807     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1357     Document Type: Article

References (59)

1. Adachi T., Mizuuchi M., Robinson E. A., Appella E., O'Dea M. H., Gellert M., Mizuuchi K. DNA sequence of theE. coli gyrB. Nucl. Acids Res. 15:1987;771-784.
2. Ali J. A., Jackson A. P., Howells A. J., Maxwell A. The 43-kDa N-terminal fragment of the gyrase B protein hydrolyses ATP and binds coumarin drugs. Biochemistry. 32:1993;2717-2724.
3. Bates A. D., Maxwell A. DNA gyrase can supercoil DNA circles as small as 174 base pairs. EMBO J. 8:1989;1861-1866.
4. Bates A. D., O'Dea M. H., Gellert M. Energy coupling inEscherichia coli. Biochemistry. 35:1996;1408-1416.
5. Berger J. M., Gamblin S. J., Harrison S. C., Wang J. C. Structure at 2.7 Å resolution of a 92 K yeast DNA topoisomerase II fragment. Nature. 379:1996;225-232.
6. Bernard P., Couturier M. Cell killing by the F plasmid CcdB protein involves poisoning of the DNA-topoisomerase II complex. J. Mol. Biol. 226:1992;735-745.
7. Bernard P., Kézdy K. E., Van Melderen L., Steyaert J., Wyns L., Pato M. L., Higgins N. P., Couturier M. The F plasmid CcdB protein induces efficient ATP-dependent DNA cleavage by gyrase. J. Mol. Biol. 234:1993;534-541.
8. Brown P. O., Peebles C. L., Cozzarelli N. R. A topoisomerase fromEscherichia coli. Proc. Natl Acad. Sci. USA. 76:1979;6110-6114.
9. Cove M. E., Tingey A. P., Maxwell A. DNA gyrase can cleave short DNA fragments in the presence of quinolone drugs. Nucl. Acids Res. 14:1997;2716-2722.
10. Critchlow S. E., Maxwell A. DNA cleavage is not required for the binding of quinolone drugs to the DNA gyrase-DNA complex. Biochemistry. 35:1996;7387-7393.
11. Cullis P. M., Maxwell A., Weiner D. P. Exploiting nucleoside thiophosphates to probe mechanistic aspects ofEscherichia coli. Biochemistry. 36:1997;6059-6068.
12. Dobbs S. T., Cullis P. M., Maxwell A. The cleavage of DNA at phosphorothioate internucleotidic linkages by DNA gyrase. Nucl. Acids Res. 20:1992;3567-3573.
13. Froelich-Ammon S. J., Osheroff N. Topoisomerase poisons: harnessing the dark side of enzyme mechanism. J. Biol. Chem. 270:1995;21429-21432.
14. Gellert M., Mizuuchi K., O'Dea M. H., Itoh T., Tomizawa J. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl Acad. Sci. USA. 74:1977;4772-4776.
15. Gellert M., Fisher L. M., O'Dea M. H. DNA gyrase: purification and catalytic properties of a fragment of gyrase B protein. Proc. Natl Acad. Sci. USA. 76:1979;6289-6293.
16. Gmünder H., Kuratli K., Keck W. In the presence of subunit A inhibitors DNA gyrase cleaves DNA fragments as short as 20 bp at specific sites. Nucl. Acids Res. 25:1997;604-611.
17. Gudas L. J., Pardee A. B. DNA synthesis and the induction of protein X inEscherichia coli. J. Mol. Biol. 101:1976;459-477.
18. Hallett P., Grimshaw A. J., Wigley D. B., Maxwell A. Cloning of the DNA gyrase genes undertac. Gene. 93:1990;139-142.
19. Hane M. W., Wood T. H. Escherichia coli . J. Bacteriol. 99:1969;238-241.
20. Horowitz D. S., Wang J. C. Mapping the active site tyrosine ofEscherichia coli. J. Biol. Chem. 262:1987;5339-5344.
21. Jackson A. P., Maxwell A. Identifying the catalytic residue of the ATPase reaction of DNA gyrase. Proc. Natl Acad. Sci. USA. 90:1993;11232-11236.
22. Jaffé A., Ogura T., Hiraga S. Effects of theccd. J. Bacteriol. 163:1985;841-849.
23. Jensen R. B., Gerdes K. Programmed cell death in bacteria: proteic plasmid stabilization systems. Mol. Microbiol. 17:1995;205-210.
24. Kampranis S. C., Maxwell A. Conversion of DNA gyrase into a conventional type II topoisomerase. Proc. Natl Acad. Sci. USA. 93:1996;14416-14421.
25. Karoui H., Bex F., Drèze P., Couturier M. Ham22recA. EMBO J. 2:1983;1863-1868.
26. Kreuzer K. N., Cozzarelli N. R. Escherichia coli. J. Bacteriol. 140:1979;424-435.
27. Liu L. F. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58:1989;351-375.
28. Maki S., Takiguchi S., Miki T., Horiuchi T. Modulation of DNA supercoiling activity ofEscherichia coli. J. Biol. Chem. 267:1992;12244-12251.
29. Maki S., Takiguchi S., Horiuchi T., Sekimizu J., Miki T. Partner switching mechanisms in activation and rejuvenation ofEscherichia coli. J. Mol. Biol. 256:1996;473-482.
30. Maxwell A. The molecular basis of quinolone action. J. Antimicrob. Chemother. 30:1992;409-416.
31. Maxwell A. DNA gyrase as a drug target. Trends Microbiol. 5:1997;102-109.
32. Maxwell A., Gellert M. The DNA dependence of the ATPase activity of DNA gyrase. J. Biol. Chem. 259:1984;14472-14480.
33. Menzel R., Gellert M. Regulation of the genes forE. coli. Cell. 34:1983;105-113.
34. Miki T., Yoshioka K., Horiuchi T. Control of cell division by sex factor F inEscherichia coli. J. Mol. Biol. 174:1984;605-625.
35. Miki T., Park J. A., Nagao K., Murayama N., Horiuchi T. Control of segregation of chromosomal DNA by sex factor F inEscherichia coli. J. Mol. Biol. 225:1992;39-52.
36. Mizuuchi K., Mizuuchi M., O'Dea M. H., Gellert M. Cloning and simplified purification ofEscherichia coli. J. Biol. Chem. 259:1984;9199-9201.
37. Morais Cabral J. H., Jackson A. P., Smith C. V., Shikotra N., Maxwell A., Liddington R. C. Structure of the DNA breakage-reunion domain of DNA gyrase. Nature. 388:1997;903-906.
38. Morrison A., Cozzarelli N. R. Site-specific cleavage of DNA byE. coli. Cell. 17:1979;175-184.
39. Ogura T., Hiraga S. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc. Natl Acad. Sci. USA. 80:1983;4784-4788.
40. Orphanides G., Maxwell A. Evidence for a conformational change in the DNA gyrase-DNA complex from hydroxyl radical footprinting. Nucl. Acids Res. 22:1994;1567-1575.
41. Pato M. L., Howe M. M., Higgins N. P. A DNA gyrase-binding site at the center of the bacteriophage Mu genome is required for efficient transposition. Proc. Natl Acad. Sci. USA. 87:1990;8716-8720.
42. Reece R. J., Maxwell A. Tryptic fragments of theEscherichia coli. J. Biol. Chem. 264:1989;19648-19653.
43. Reece R. J., Maxwell A. The C-terminal domain of theEscherichia coli. Nucl. Acids Res. 19:1991a;1399-1405.
44. Reece R. J., Maxwell A. DNA gyrase: structure and function. CRC Crit. Rev. Biochem. Mol. Biol. 26:1991b;335-375.
45. Reece R. J., Maxwell A. Probing the limits of the DNA breakage-reunion domain of theEscherichia coli. J. Biol. Chem. 266:1991c;3540-3546.
46. Sommer S., Bailone A., Devoret R. SOS induction by thermosensitive mutants of miniF plasmid. Mol. Gen. Genet. 198:1985;456-464.
47. Steck T. R., Franco R. J., Wang J.-Y., Drlica K. Topoisomerase mutations affect the relative abundance of manyEscherichia coli. Mol. Microbiol. 10:1993;473-481.
48. Sugino A., Peebles C. L., Kruezer K. N., Cozzarelli N. R. Mechanism of action of nalidixic acid: purification ofEscherichia coli nal. Proc. Natl Acad. Sci. USA. 74:1977;4767-4771.
49. Sugino A., Higgins N. P., Brown P. O., Peebles C. L., Cozzarelli N. R. Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc. Natl Acad. Sci. USA. 75:1978;4838-4842.
50. Tingey A. P., Maxwell A. Probing the role of the ATP-operated clamp in the strand-passage reaction of DNA gyrase. Nucl. Acids Res. 24:1996;4868-4873.
51. Tse-Dinh Y.-C. Regulation of theEscherichia coli. Nucl. Acids Res. 13:1985;4751-4763.
52. Van Melderen L., Bernard P., Couturier M. Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol. Microbiol. 11:1994;1151-1157.
53. Van Melderen L., Dao Thi M. H., Lecchi P., Gottesman S., Couturier M., Maurizi M. R. ATP-dependent degradation of CcdA by Lon protease. J. Biol. Chem. 271:1996;27730-27738.
54. Vizán J., Hernandex-Chico C., del Castillo I., Moreno F. The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated byE. coli. EMBO J. 10:1991;467-476.
55. Walker G. C. Mutagenesis and inducible responses to deoxyribonucleic acid damage inEscherichia coli. Microbiol. Rev. 48:1984;60-93.
56. Wigley D. B. Structure and mechanism of DNA gyrase. Nucleic Acids and Molecular Biology. 1995;Springer-Verlag, Berlin, Heidelberg.
57. Willmott C. J. R., Maxwell A. A single point mutation in the DNA gyrase A protein greatly reduces the binding of fluoroquinolones to the gyrase-DNA complex. Antimicrob. Agents Chemother. 37:1993;126-127.
58. Willmott C. J. R., Critchlow S. E., Eperon I. C., Maxwell A. The complex of DNA gyrase and quinolone drugs with DNA forms a barrier to transcription by RNA polymerase. J. Mol. Biol. 242:1994;351-363.
59. Yoshida H., Bogaki M., Nakamura M., Nakamura S. Quinolone resistance-determining region in the DNA gyrasegyrAEscherichia coli. Antimicrob. Agents Chemother. 34:1990;1271-1272.