The interaction of DNA gyrase with the bacterial toxin CcdB: Evidence for the existence of two Gyrase-CcdB complexes

Journal of Molecular Biology

Volumn 293, Issue 3, 1999, Pages 733-744

  Kampranis, Sotirios C ^a   Howells, Alison J ^a   Maxwell, Anthony ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

CcdA; Proteolysis; Supercoiling; Surface plasmon resonance; Topoisomerase

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL TOXIN; DNA TOPOISOMERASE (ATP HYDROLYSING);

AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0032756532     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3182     Document Type: Article

References (49)

1. 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.
2. Bahassi E. M., O'Dea M. H., Allali N., Messens J., Gellert M., Couturier M. Interaction of CcdB with DNA gyrase. Inactivation of GyrA, poisoning of the gyrase-DNA complex, and the antidote action of CcdA. J. Biol. Chem. 274:1999;10936-10944.
3. 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.
4. 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.
5. 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.
6. Couturier M., Bahassi E. M., Van Melderen L. Bacterial death by DNA gyrase poisoning. Trends Microbiol. 6:1998;269-275.
7. Cove M. E., Tingey A. P., Maxwell A. DNA gyrase can cleave short DNA fragments in the presence of quinolone drugs. Nucl. Acids Res. 25:1997;2716-2722.
8. Critchlow S. E. The molecular basis of quinolone drug action on DNA gyrase, PhD thesis. 1996;University of Leicester.
9. Critchlow S. E., O'Dea M. H., Howells A. J., Couturier M., Gellert M., Maxwell A. The interaction of the F-plasmid killer protein, CcdB, with DNA gyrase: induction of DNA cleavage and blocking of transcription. J. Mol. Biol. 273:1997;826-839.
10. de Feyter R., Wallace C., Lane D. Autoregulation of the ccd operon in the F plasmid. Mol. Gen. Genet. 218:1989;481-486.
11. 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.
12. 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.
13. Hammonds T. R., Maxwell A. The DNA dependence of the ATPase activity of human DNA topoisomerase IIα J. Biol. Chem. 272:1997;32696-32703.
14. Howard M. T., Neece S. H., Matson S. W., Kreuzer K. N. Disruption of a topoisomerase-DNA cleavage complex by a DNA helicase. Proc. Natl Acad. Sci. USA. 91:1994;12031-12035.
15. Jaffé A., Ogura T., Hiraga S. Effects of the ccd function of the F plasmid on bacterial growth. J. Bacteriol. 163:1985;841-849.
16. Kampranis S. C., Maxwell A. Conformational changes in DNA gyrase revealed by limited proteolysis. J. Biol. Chem. 273:1998a;22606-22614.
17. Kampranis S. C., Maxwell A. The DNA gyrase-quinolone complex: ATP hydrolysis and the mechanism of DNA cleavage. J. Biol. Chem. 273:1998b;22615-22626.
18. Kampranis S. C., Bates A. D., Maxwell A. A model for the mechanism of strand passage by DNA gyrase. Proc. Natl Acad. Sci. USA. 96:1999a;8414-8419.
19. Kampranis S. C., Gormley N. A., Tranter R., Orphanides G., Maxwell A. Probing the binding of coumarins and cyclothialidines to DNA gyrase. Biochemistry. 38:1999b;1967-1976.
20. Karoui H., Bex F., Drèze P., Couturier M. Ham22, a miniF mutation which is lethal to host cell and promotes recA-dependent induction of lambdoid prophage. EMBO J. 2:1983;1863-1868.
21. Loris R., Dao-Thi M.-H., Bahassi E. M., Van Melderen L. V., Poortmans F., Liddington R. C., Couturier M., Wyns L. Crystal structure of CcdB, a topoisomerase poison from E. coli. J. Mol. Biol. 285:1999;1667-1677.
22. Maki S., Takiguchi S., Miki T., Horiuchi T. Modulation of DNA supercoiling activity of Escherichia coli DNA gyrase by F plasmid proteins. J. Biol. Chem. 267:1992;12244-12251.
23. Maki S., Takiguchi S., Horiuchi T., Sekimizu J., Miki T. Partner switching mechanisms in activation and rejuvenation of Escherichia coli DNA gyrase by F plasmid proteins, LetD (CcdB) and LetA (CcdA). J. Mol. Biol. 256:1996;473-482.
24. Maxwell A. DNA gyrase as a drug target. Trends Microbiol. 5:1997;102-109.
25. Maxwell A., Critchlow S. E. Mode of action. Kuhlmann J., Dalhoff A., Zeiler H.-J. Handbook of Experimental Pharmacology-Quinolone Antibacterials. 1998;119-166 Springer-Verlag, Berlin.
26. Maxwell A., Gellert M. The DNA dependence of the ATPase activity of DNA gyrase. J. Biol. Chem. 259:1984;14472-14480.
27. Maxwell A., Howells A. J. Overexpression and purification of bacterial DNA gyrase. Bjornsti M.-A., Osheroff N. Protocols for DNA Topoisomerases I: DNA Topology and Enzyme Purification. 1999;135-144 Humana Press, Towata, New Jersey.
28. Maxwell A., Rau D. C., Gellert M. Mechanistic studies of DNA gyrase. Sarma R. H., Sarma M. H. Biomolecular Stereodynamics III. Proceedings of the Fourth Conversation in the Discipline of Biomolecular Stereodynamics. 1986;137-146 Adenine Press, Albany.
29. Miki T., Yoshioka K., Horiuchi T. Control of cell division by sex factor F in Escherichia coli I. The 42.84-43.6 F segment couples cell division of the host bacteria with replication of plasmid DNA. J. Mol. Biol. 174:1984;605-625.
30. Miki T., Park J. A., Nagao K., Murayama N., Horiuchi T. Control of segregation of chromosomal DNA by sex factor F in Escherichia coli. J. Mol. Biol. 225:1992;39-52.
31. 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.
32. 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.
33. Reece R. J., Maxwell A. Tryptic fragments of the Escherichia coli DNA gyrase A protein. J. Biol. Chem. 264:1989;19648-19653.
34. Reece R. J., Maxwell A. DNA gyrase: structure and function. CRC Crit. Rev. Biochem. Mol. Biol. 26:1991a;335-375.
35. Reece R. J., Maxwell A. Probing the limits of the DNA breakage-reunion domain of the Escherichia coli DNA gyrase A protein. J. Biol. Chem. 266:1991b;3540-3546.
36. Roca J., Wang J. C. The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell. 71:1992;833-840.
37. Schacht P. Clinical use of quinolones. Kuhlmann J., Dalhoff A., Zeiler H.-J. Handbook of Experimental Pharmacology-Quinolone Antibacterials. 1997;421-453 Springer-Verlag, Berlin.
38. Scheirer K., Higgins N. P. The DNA cleavage reaction of DNA gyrase. Comparison of stable ternary complexes formed with enoxacin and CcdB protein. J. Biol. Chem. 272:1997;27202-27209.
39. Sugino A., Peebles C. L., Kruezer K. N., Cozzarelli N. R. Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc. Natl Acad. Sci. USA. 74:1977;4767-4771.
40. Tam J. E., Kline B. C. Control of the ccd operon in plasmid F. J. Bacteriol. 171:1989a;2353-2360.
41. Tam J. E., Kline B. C. The F plasmid ccd autorepressor is a complex of CcdA and ccdB proteins. Mol. Gen. Genet. 219:1989b;26-32.
42. 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.
43. 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.
44. 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.
45. Wang J. C. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Quart. Rev. Biophys. 31:1998;107-144.
46. Wigley D. B. Structure and mechanism of DNA gyrase. Eckstein F., Lilley D. M. J. Nucleic Acids and Molecular Biology. 1995;165-176 Springer-Verlag, Berlin, Heidelberg.
47. Williams N. L., Maxwell A. Locking the DNA gate of DNA gyrase: investigating the effects on DNA cleavage and ATP hydrolysis. Biochemistry. in the press:1999a.
48. Williams N. L., Maxwell A. Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking. Biochemistry. in the press:1999b.
49. 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.