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PMID: 2548439 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cloning and characterization of a DNA gyrase A gene from Escherichia coli that confers clinical resistance to 4-quinolones.

Antimicrobial agents and chemotherapy ·Vol. 33 ·No. 6 ·1989-06-00 ·Pages 886-94

Cullen ME, Wyke AW, Kuroda R, Fisher LM

Abstract

Nalidixic acid, enoxacin, and other antibacterial 4-quinolones inhibit DNA gyrase activity by interrupting DNA breakage and reunion by A subunits of the A2B2 gyrase complex. Despite their clinical importance, the mode of quinolone action and mechanisms of resistance are poorly understood at the molecular level. Using a DNA fragment enrichment procedure, we isolated the gyrA gene from a uropathogenic Escherichia coli strain that encodes a gyrase A protein cross-resistant to a variety of quinolones. When complemented with gyrase B subunit, the purified A protein reconstituted DNA supercoiling activity approximately 100-fold more resistant to inhibition by enoxacin than the susceptible enzyme and failed to mediate quinolone-dependent DNA cleavage. Nucleotide sequence analysis revealed that the gene differed at 58 nucleotide positions compared with the K-12 gyrA sequence. The 875-amino-acid residue-resistant gyrase A protein differed at three positions from its wild-type E. coli K-12 counterpart: tryptophan, glutamate, and serine replaced serine, aspartate, and alanine residues at positions 83, 678, and 828, respectively. By genetic analysis of chimeric gyrA genes in a gyrA(Ts) background, we showed that the Ser-83----Trp mutation in the gyrase A protein was solely responsible for high-level bacterial resistance to nalidixic acid and fluoroquinolones.

MeSH Terms
4-Quinolones Anti-Infective Agents/pharmacology Base Sequence Blotting, Southern Cloning, Molecular DNA Topoisomerases, Type II/genetics DNA, Bacterial/biosynthesis Drug Resistance, Microbial Escherichia coli/enzymology,genetics Genes, Bacterial Molecular Sequence Data
Chemicals
4-Quinolones Anti-Infective Agents DNA, Bacterial DNA Topoisomerases, Type II
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Cullen M E
Department of Biochemistry, St. George's Hospital Medical School, University of London, United Kingdom.
Wyke A W
Kuroda R
Fisher L M
References (37)
37 references, click to expand
  1. Escherichia coli K-12 mutants resistant to nalidixic acid: genetic mapping and dominance studies.
    J Bacteriol. 1969 Jul;99(1):238-41 PMID: 4895844
  2. MECHANISM OF ACTION OF NALIDIXIC ACID ON ESCHERICHIA COLI.II. INHIBITION OF DEOXYRIBONUCLEIC ACID SYNTHESIS.
    J Bacteriol. 1965 Apr;89:1068-74 PMID: 14276097
  3. DNA gyrase: an enzyme that introduces superhelical turns into DNA.
    Proc Natl Acad Sci U S A. 1976 Nov;73(11):3872-6 PMID: 186775
  4. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4474-8 PMID: 794878
  5. 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 U S A. 1977 Nov;74(11):4767-71 PMID: 200930
  6. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):4772-6 PMID: 337300
  7. Purification of subunits of Escherichia coli DNA gyrase and reconstitution of enzymatic activity.
    Proc Natl Acad Sci U S A. 1978 Apr;75(4):1773-7 PMID: 347446
  8. DNA gyrase: subunit structure and ATPase activity of the purified enzyme.
    Proc Natl Acad Sci U S A. 1978 Dec;75(12):5960-3 PMID: 153529
  9. Energy coupling in DNA gyrase and the mechanism of action of novobiocin.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):4838-42 PMID: 368801
  10. Site-specific cleavage of DNA by E. coli DNA gyrase.
    Cell. 1979 May;17(1):175-84 PMID: 378403
  11. DNA gyrase on the bacterial chromosome: DNA cleavage induced by oxolinic acid.
    J Mol Biol. 1979 Jun 25;131(2):287-302 PMID: 226717
  12. A sign inversion mechanism for enzymatic supercoiling of DNA.
    Science. 1979 Nov 30;206(4422):1081-3 PMID: 227059
  13. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  14. DNA gyrase action involves the introduction of transient double-strand breaks into DNA.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):1847-51 PMID: 6246508
  15. Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA.
    J Biol Chem. 1980 Jun 25;255(12):5560-5 PMID: 6155377
  16. Formation and resolution of DNA catenanes by DNA gyrase.
    Cell. 1980 May;20(1):245-54 PMID: 6248235
  17. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I.
    Nature. 1980 Aug 28;286(5776):854-60 PMID: 6774262
  18. DNA topoisomerases.
    Annu Rev Biochem. 1981;50:879-910 PMID: 6267993
  19. DNA gyrase: affinity chromatography on novobiocin-Sepharose and catalytic properties.
    Nucleic Acids Res. 1981 Aug 11;9(15):3589-603 PMID: 6269086
  20. Site-specific interaction of DNA gyrase with DNA.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4165-9 PMID: 6270661
  21. Biology of bacterial deoxyribonucleic acid topoisomerases.
    Microbiol Rev. 1984 Dec;48(4):273-89 PMID: 6097803
  22. Mechanism of inhibition of DNA gyrase by analogues of nalidixic acid: the target of the drugs is DNA.
    Proc Natl Acad Sci U S A. 1985 Jan;82(2):307-11 PMID: 2982149
  23. DNA topoisomerases.
    Annu Rev Biochem. 1985;54:665-97 PMID: 2992360
  24. Direct cloning of specific genomic DNA sequences in plasmid libraries following fragment enrichment.
    Nucleic Acids Res. 1985 Nov 11;13(21):7569-78 PMID: 2999697
  25. The fluoroquinolones: structures, mechanisms of action and resistance, and spectra of activity in vitro.
    Antimicrob Agents Chemother. 1985 Oct;28(4):581-6 PMID: 3000292
  26. DNA gyrase complex with DNA: determinants for site-specific DNA breakage.
    EMBO J. 1986 Jun;5(6):1411-8 PMID: 3015604
  27. Nalidixic acid-resistant mutations of the gyrB gene of Escherichia coli.
    Mol Gen Genet. 1986 Sep;204(3):367-73 PMID: 3020376
  28. Purification and properties of DNA gyrase from a fluoroquinolone-resistant strain of Escherichia coli.
    Antimicrob Agents Chemother. 1986 Nov;30(5):777-80 PMID: 3026239
  29. Mapping the active site tyrosine of Escherichia coli DNA gyrase.
    J Biol Chem. 1987 Apr 15;262(11):5339-44 PMID: 3031051
  30. Cloning and simplified purification of Escherichia coli DNA gyrase A and B proteins.
    J Biol Chem. 1984 Jul 25;259(14):9199-201 PMID: 6086626
  31. Cloning and sequencing of the Escherichia coli gyrA gene coding for the A subunit of DNA gyrase.
    J Mol Biol. 1987 Oct 20;197(4):729-36 PMID: 2828631
  32. Quinolone-resistant mutations of the gyrA gene of Escherichia coli.
    Mol Gen Genet. 1988 Jan;211(1):1-7 PMID: 2830458
  33. Purification of Citrobacter freundii DNA gyrase and inhibition by quinolones.
    Antimicrob Agents Chemother. 1988 Jan;32(1):104-9 PMID: 2831810
  34. Studies on the interaction of 4-quinolones with DNA by DNA unwinding experiments.
    Biochim Biophys Acta. 1988 Mar 31;949(3):279-87 PMID: 2831987
  35. Do quinolones bind to DNA?
    Biochem Pharmacol. 1988 May 1;37(9):1887-8 PMID: 3163928
  36. Inhibitors of DNA topoisomerases.
    Biochemistry. 1988 Apr 5;27(7):2253-9 PMID: 2838070
  37. Studies on the mechanism of action of nalidixic acid.
    Antimicrob Agents Chemother. 1973 Oct;4(4):479-86 PMID: 4208771
Article Info
Journal
Antimicrobial agents and chemotherapy
Abbr.
Antimicrob Agents Chemother
ISSN
0066-4804
Published
1989-06-00
Pages
886-94
Language
English
Region
United States
NLM ID
0315061
PMCID
PMC284251
Subset
IM
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