Mechanism of DNA gyrase-mediated illegitimate recombination: Characterization of Escherichia coli gyrA mutations that confer hyper-recombination phenotype

Journal of Molecular Biology

Volumn 289, Issue 3, 1999, Pages 447-458

  Ashizawa, Yuki ^a   Yokochi, Tomoki ^a   Ogata, Yasuyuki ^a   Shobuike, Yuko ^a   Kato, Jun ichi ^a   Ikeda, Hideo ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b KITASATO INSTITUTE   (Japan)

Author keywords

Cleavable complex; gyrA mutation; Short homology independent illegitimate recombination; SOS induction; bio transducing phage

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); ISOLEUCINE; LEUCINE; PROLINE; VALINE;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIOPHAGE LAMBDA; ENZYME MECHANISM; ESCHERICHIA COLI; GENE MUTATION; GENETIC RECOMBINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; TEMPERATURE SENSITIVE MUTANT;

BACTERIOPHAGE LAMBDA; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0033546124     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2758     Document Type: Article

References (42)

1. Albertini, A. M., Hofer, M., Calos, M. P. & Miller, J. H. (1982). On the formation of spontaneous deletions: The importance of short sequence homologies in the generation of large deletions. Cell, 29, 319-328.
2. Berger, J. M., Gamblin, S. J., Harrison, S. C. & Wang, J. C. (1996). Structure and mechanism of DNA topoisomerase II. Nature, 379, 225-232.
3. Cabral, J. H. M., Jackson, A. P., Smith, C. V., Shikotra, N., Maxwell, A. & Liddington, R. C. (1997). Crystal structure of the breakage-reunion domain of DNA gyrase. Nature, 388, 903-906.
4. Colishaw, J. & Ginoza, W. (1970). Induction of prophage by nalidixic acid. Virology, 41, 244-255.
5. DeMarini, D. M. & Lawrence, B. K. (1992). Prophage induction by DNA topoisomerase II poisons and reactive-oxygen species: Role of DNA breaks. Mutat. Res. 267, 1-17.
6. Gellert, M. (1981). DNA topoisomerases. Annu. Rev. Biochem. 50, 879-910.
7. Gellert, M., Mizuuchi, K., O'Dea, M. H. & Nash, H. A. (1976). DNA gyrase: An enzyme that introduces superhelical turns into DNA. Proc. Natl Acad. Sci. USA, 73, 3872-3876.
8. Gellert, M., Mizuuchi, K., O'Dea, M. H., Itoh, T. & Tomizawa, J. (1977). Nalidixic acid resistance: A second genetic character involved in DNA gyrase activity. Proc. Natl Acad. Sci. USA, 74, 4772-4776.
9. Hanada, K., Ukita, T., Kohno, Y., Saito, K., Kato, J. & Ikeda, H. (1997). RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 3860-3865.
10. Higgins, N. P., Peebles, C. L., Sugino, A. & Cozzarelli, N. R. (1978). Purification of subunits of Escherichia coli DNA gyrase and reconstitution of enzymatic activity. Proc. Natl Acad. Sci. USA, 75, 1773-1777.
11. Hillyard, D. R., Edlund, M., Hughes, K. T., Marsh, M. & Higgins, N. P. (1990). Subunit-specific phenotypes of Salmonella typhimurium HU mutants. J. Bacteriol. 172, 5402-5407.
12. Hsieh, L. S., Rouviere-Yaniv, J. & Drlica, K. (1991). Bacterial DNA supercoiling and [ATP]/[ADP] ratio: Changes associated with salt shock. J. Bacteriol. 173, 3914-3917.
13. Hsieh, T. (1990). Mechanistic aspects of type-II DNA topoisomerases. In DNA Topology and Its Biological Implications (Cozzarelli, N. & Wang, J. C., eds), pp. 243-263, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
14. Ikeda, H., Moriya, K. & Matsumoto, T. (1980). In Vitro study of illegitimate recombination: Involvement of DNA gyrase. Cold Spring Harbor Symp. Quant. Biol. 45, 399-408.
15. Ikeda, H., Aoki, K. & Naito, A. (1982). Illegitimate recombination mediated in vitro by DNA gyrase of Escherichia coli: Structure of recombinant DNA molecules. Proc. Natl Acad. Sci. USA, 79, 3724-3728.
16. Kato, J. & Ikeda, H. (1996). Construction of mini-F plasmid vectors for plasmid shuffling in Escherichia coli. Gene, 170, 141-142.
17. Kato, J., Nishimura, Y., Yamada, M., Suzuki, H. & Hirota, Y. (1988). Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli. J. Bacteriol. 170, 3967-3977.
18. Kato, J., Nishimura, Y., Imamura, R., Niki, H., Hiraga, S. & Suzuki, H. (1990). New topoisomerase essential for chromosome segregation in E. Coli. Cell, 63, 393-404.
19. Kato, J., Suzuki, H. & Ikeda, H. (1992). Purification and characterization of DNA topoisomerase IV in Escherichia coli. J. Biol. Chem. 267, 25676-25684.
20. Kumagai, M. & Ikeda, H. (1991). Molecular analysis of the recombination junctions of λbio transducing phages. Mol. Gen. Genet. 230, 60-64.
21. Lynn, R., Giaever, G., Swanberg, S. L. & Wang, J. C. (1986). Tandem regions of yeast DNA topoisomerase II share homology with different subunits of bacterial gyrase. Science, 233, 647-649.
22. Malik, M., Bensaid, A., Rouviere-Yaniv, J. & Drlica, K. (1996). Histone-like protein HU and bacterial DNA topology: Suppression of an HU deficiency by gyrase mutations. J. Mol. Biol. 256, 66-76.
23. Marvo, S. L., King, S. R. & Jaskunas, S. R. (1983). Role of short regions of homology in intermolecular illegitimate recombination events. Proc. Natl Acad. Sci. USA, 80, 2452-2456.
24. Mizuuchi, K., O'Dea, M. H. & Gellert, M. (1978). DNA gyrase: Subunit structure and ATPase activity of the purified enzyme. Proc. Natl Acad. Sci. USA, 75, 5960-5963.
25. Naito, A., Naito, S. & Ikeda, H. (1984). Homology is not required for recombination mediated by DNA gyrase of Escherichia coli. Mol. Gen. Genet. 193, 238-243.
26. Peebles, C. L., Higgins, N. P., Kreuzer, K. N., Morrison, A., Brown, P. O., Sugino, A. & Cozzarelli, N. R. (1978). Structure and activities of Escherichia coli DNA gyrase. Cold Spring Harbor Symp. Quant. Biol. 43, 41-52.
27. Peng, H. & Marians, K. J. (1993). Escherichia coli topoisomerase IV. Purification, characterization, subunit structure, and subunit interactions. J. Biol. Chem. 268, 24481-24490.
28. Roca, J. & Wang, J. C. (1994). DNA transport by a type II DNA topoisomerase: Evidence in favor of a two-gate mechanism. Cell, 77, 609-616.
29. Roca, J., Berger, J. M., Harrison, S. C. & Wang, J. C. (1996). DNA transport by a type II topoisomerase: Direct evidence for a two-gate mechanism. Proc. Natl Acad. Sci. USA, 93, 4057-4062.
30. Rose, R. E. (1988). The nucleotide sequence of pACYC184. Nucl. Acids Res. 16, 355.
31. Shanado, Y., Kato, J. & Ikeda, H. (1998). Escherichia coli HU protein suppresses DNA-gyrase-mediated illegitimate recombination and SOS induction. Genes Cells, 3, 511-520.
32. Shimizu, H., Yamaguchi, H. & Ikeda, H. (1995). Molecular analysis of λbio transducing phage produced by oxolinic acid-induced illegitimate recombination in vivo. Genetics, 140, 889-896.
33. Shimizu, H., Yamaguchi, H., Ashizawa, Y., Kohno, Y., Asami, M., Kato, J. & Ikeda, H. (1997). Short-homology-independent illegitimate recombination in Escherichia coli: Distinct mechanism from short-homology-dependent illegitimate recombination. J. Mol. Biol. 266, 297-305.
34. Sugino, A., Peebles, C. L., Kreuzer, K. N. & Cozzarelli, N. R. (1977). 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, 4767-4771.
35. Tomono, M., Shiozaki, M. & Ikeda, H. (1989). Formation of λ transducing phage in vitro: Involvement of DNA gyrase. J. Biochem. 105, 423-428.
36. Uemura, T., Morikawa, K. & Yanagida, M. (1986). The nucleotide sequence of the fission yeast DNA topoisomerase II gene: Structural and functional relationships to other DNA topoisomerases. EMBO J. 5, 2355-2361.
37. Ukita, T. & Ikeda, H. (1996). Role of the recJ gene product in UV-induced illegitimate recombination at the hotspot. J. Bacteriol. 178, 2362-2367.
38. Wang, J. C. (1985). DNA topoisomerases. Annu. Rev. BioChem. 54, 665-697.
39. Wyckoff, E., Natalie, D., Nolan, J. M., Lee, M. & Hsieh, T. (1989). Structure of the Drosophila DNA topoisomerase II gene. Nucleotide sequence and homology among topoisomerases II. J. Mol. Biol. 205, 1-13.
40. Yamaguchi, H., Yamashita, T., Shimizu, H. & Ikeda, H. (1995). A hotspot of spontaneous and UV-induced illegitimate recombination during formation of λbio transducing phage. Mol. Gen. Genet. 248, 637-643.
41. Yi, T.-M., Stearns, D. & Demple, B. (1988). Illegitimate recombination in an Escherichia coli plasmid: Modulation by DNA damage and a new bacterial gene. J. Bacteriol. 170, 2898-2903.
42. Yokochi, T., Kato, J. & Ikeda, H. (1996). DNA nicking by Escherichia coli topoisomerase IV with a substitution mutation from tyrosine to histidine at the active site. Genes Cells, 1, 1069-1075.