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Identification of DNA topoisomerases involved in immediate and transient DNA relaxation induced by heat shock inEscherichia coli

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Abstract

The linking number of plasmid DNA in exponentially growingEscherichia coli increases immediately and transiently after heat shock. The purpose of this study was to search for DNA topoisomerases that catalyze this relaxation of DNA. Neither introduction of atopA deletion mutation nor treatment of cells with DNA gyrase inhibitors affected the DNA relaxation induced by heat shock. Thus, DNA topoisomerase I and DNA gyrase are apparently not involved in the process. However, the reaction was inhibited by nalidixic acid or by oxolinic acid in thetopA mutant and the reaction was resistant to nalidixic acid in atopA mutant carrying, in addition, thenalA26 mutation. These results are interpreted as indicating that both DNA topoisomerase I and DNA gyrase are involved in the DNA relaxation induced by heat shock.

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References

  • Ashburner M (1982) The effects of heat shock and other stress o gene activity. In: Schleisinger MJ, Ashburner M, Tissières A (eds) Heat shock from bacteria to man. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 1–8

    Google Scholar 

  • Broyles SS, Pettijohn DE (1986) Interaction ofEscherichia coli HU protein with DNA, evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol 187:47–60

    Google Scholar 

  • DiNardo S, Voelkel KA, Sternglanz R, Reynolds AE, Wright A (1982)Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31:43–51

    Google Scholar 

  • Drlica K (1984) Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev 48:273–289

    Google Scholar 

  • Drlica K, Rouviere-Yaniv J (1987) Historic like proteins of bacteria. Microbiol Rev 51:301–319

    Google Scholar 

  • Goldstein E, Drlica K (1984) Regulation of bacterial DNA super-coiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci USA 81:4046–4050

    Google Scholar 

  • Haq S, Natori S, Sekimizu K (1993) Heat-induced DNA relaxationin vitro by mouse DNA topoisomerase I in the presence of ethidium bromide. J Biochem (Tokyo) 113:620–624

    Google Scholar 

  • Ikeda H, Moriya K, Matsumoto T (1981)In vitro study of illegitimate recombination: involvement of DNA gyrase. Cold Spring Harbor Symp Quant Biol 46:399–408

    Google Scholar 

  • Kato J, Suzuki H, Ikeda H (1992) Purification and characterization of DNA topoisomerase IV inEscherichia coli. J Biol Chem 267:25676–25684

    Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Mizushima T, Natori S, Sekimizu K (1992) Inhibition ofEscherichia coli DNA topoisomerase I activity by phospholipids. Biochem J 285:503–506

    Google Scholar 

  • Mizushima T, Natori S, Sekimizu K (1993) Relaxation of super-coiled DNA associated with induction of heat shock proteins inEscherichia coli. Mol Gen Genet 238:1–5

    Google Scholar 

  • Neidhardt FC, Van Bogelen RA, Vaughn V (1984) The genetics and regulation of heat-shock proteins. Annu Rev Genet 18:295–329

    Google Scholar 

  • Pulleyblank DE, Shure M, Tang D, Vinograd J, Vosberg H-P (1975) Action of nicking-closing enzyme on supercoiled and nonsupercoiled closed circular DNA: formation of a Boltzmann distribution of topological isomers. Proc Natl Acad Sci USA 72:4280–4284

    Google Scholar 

  • Sternglanz R, DiNardo S, Voelkel KA, Nishimura Y, Hirota Y, Becherer K, Zumstein L, Wang JC (1981) Mutations in the gene coding forEscherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci USA 78:2747–2751

    Google Scholar 

  • Sugino A, Peebles CL, Kreuzer KN, Cozzarelli NR (1977) Mechanism of action of nalidixic acid: purification ofEscherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc Natl Acad Sci USA 74:4767–4771

    Google Scholar 

  • Tanji K, Mizushima T, Natori S, Sekimizu K (1992) Induction by psychotropic drugs and local anesthetics of DnaK and GroEL proteins inEscherichia coli. Biochim Biophys Acta 1129:172–176

    Google Scholar 

  • Taylor WE, Straus DB, Grossman AD, Burton ZF, Gross CA, Burgess R (1984) Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit ofE. coli RNA polymerase. Cell 38:371–381

    Google Scholar 

  • Yamamori T, Yura T (1980) Temperature-induced synthesis of specific proteins inEscherichia coli: evidence for transcriptional control. J Bacteriol 142:843–851

    Google Scholar 

  • Yamamori T, Yura T (1982) Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance inEscherichia coli K-12. Proc Natl Acad Sci USA 79:860–864

    Google Scholar 

  • Wang JC (1969) Variation of the average rotation angle, of the DNA helix and the superhelical turns of covalently closed cyclic λ DNA. J Mol Biol 43:25–39

    Google Scholar 

  • Wang JC (1985) DNA topoisomerases. Annu Rev Biochem 54:665–697

    Google Scholar 

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Communicated by K. Isono

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Ogata, Y., Mizushima, T., Kataoka, K. et al. Identification of DNA topoisomerases involved in immediate and transient DNA relaxation induced by heat shock inEscherichia coli . Molec. Gen. Genet. 244, 451–455 (1994). https://doi.org/10.1007/BF00583895

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  • DOI: https://doi.org/10.1007/BF00583895

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