Topoisomerase I Mutants: the Gene on PBR322 That Encodes Resistance to Tetracycline Affects Plasmid DNA Supercoiling

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1986 Dec 1

PMID 3024156

Citations 67

Authors

G J Pruss

K Drlica

Affiliations

Soon will be listed here.

Abstract

Plasmid pBR322 DNA isolated from topoisomerase I mutants of Escherichia coli and Salmonella typhimurium exhibits a distinctive supercoiling distribution characterized by an extremely heterogeneous distribution of linking numbers that contains highly negatively supercoiled topoisomers. Analysis of the supercoiling distributions of deletion and insertion derivatives of pBR322 shows that the presence of the gene on pBR322 encoding resistance to tetracycline is responsible for the unusual supercoiling distribution. Both an intact promoter and a portion of the remainder of the gene, but not the gene product, are required. However, no particular section of the gene outside the promoter appears to be necessary; only the size of the section remaining appears to be important. These observations suggest that transcription of this gene may be responsible for its effect on DNA supercoiling.

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References

Sternglanz R, DiNardo S, Voelkel K, Nishimura Y, Hirota Y, Becherer K . Mutations in the gene coding for Escherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci U S A. 1981; 78(5):2747-51. PMC: 319434. DOI: 10.1073/pnas.78.5.2747. View

Orr E, Fairweather N, Holland I, Pritchard R . Isolation and characterisation of a strain carrying a conditional lethal mutation in the cou gene of Escherichia coli K12. Mol Gen Genet. 1979; 177(1):103-12. DOI: 10.1007/BF00267259. View

Brosius J, Cate R, Perlmutter A . Precise location of two promoters for the beta-lactamase gene of pBR322. S1 mapping of ribonucleic acid isolated from Escherichia coli or synthesized in vitro. J Biol Chem. 1982; 257(15):9205-10. View

Gamper H, Hearst J . A topological model for transcription based on unwinding angle analysis of E. coli RNA polymerase binary, initiation and ternary complexes. Cell. 1982; 29(1):81-90. DOI: 10.1016/0092-8674(82)90092-7. View

Isberg R, Syvanen M . DNA gyrase is a host factor required for transposition of Tn5. Cell. 1982; 30(1):9-18. DOI: 10.1016/0092-8674(82)90006-x. View

Vieira J, Messing J . The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982; 19(3):259-68. DOI: 10.1016/0378-1119(82)90015-4. View

Pruss G, Manes S, Drlica K . Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell. 1982; 31(1):35-42. DOI: 10.1016/0092-8674(82)90402-0. View

DiNardo S, Voelkel K, Sternglanz R, Reynolds A, Wright A . Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell. 1982; 31(1):43-51. DOI: 10.1016/0092-8674(82)90403-2. View

Som T, Tomizawa J . Regulatory regions of ColE1 that are involved in determination of plasmid copy number. Proc Natl Acad Sci U S A. 1983; 80(11):3232-6. PMC: 394014. DOI: 10.1073/pnas.80.11.3232. View

10.

Wang J, Peck L, Becherer K . DNA supercoiling and its effects on DNA structure and function. Cold Spring Harb Symp Quant Biol. 1983; 47 Pt 1:85-91. DOI: 10.1101/sqb.1983.047.01.011. View

11.

Gellert M, Menzel R, Mizuuchi K, ODea M, Friedman D . Regulation of DNA supercoiling in Escherichia coli. Cold Spring Harb Symp Quant Biol. 1983; 47 Pt 2:763-7. DOI: 10.1101/sqb.1983.047.01.087. View

12.

Dean F, Krasnow M, Otter R, Matzuk M, Spengler S, Cozzarelli N . Escherichia coli type-1 topoisomerases: identification, mechanism, and role in recombination. Cold Spring Harb Symp Quant Biol. 1983; 47 Pt 2:769-77. DOI: 10.1101/sqb.1983.047.01.088. View

13.

Peden K . Revised sequence of the tetracycline-resistance gene of pBR322. Gene. 1983; 22(2-3):277-80. DOI: 10.1016/0378-1119(83)90112-9. View

14.

Menzel R, Gellert M . Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell. 1983; 34(1):105-13. DOI: 10.1016/0092-8674(83)90140-x. View

15.

Richardson S, Higgins C, Lilley D . The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J. 1984; 3(8):1745-52. PMC: 557591. DOI: 10.1002/j.1460-2075.1984.tb02041.x. View

16.

Drlica K . Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev. 1984; 48(4):273-89. PMC: 373219. DOI: 10.1128/mr.48.4.273-289.1984. View

17.

Unger B, Becker J, Hillen W . Nucleotide sequence of the gene, protein purification and characterization of the pSC101-encoded tetracycline resistance-gene-repressor. Gene. 1984; 31(1-3):103-8. DOI: 10.1016/0378-1119(84)90199-9. View

18.

Lockshon D, Morris D . Sites of reaction of Escherichia coli DNA gyrase on pBR322 in vivo as revealed by oxolinic acid-induced plasmid linearization. J Mol Biol. 1985; 181(1):63-74. DOI: 10.1016/0022-2836(85)90324-9. View

19.

Vosberg H . DNA topoisomerases: enzymes that control DNA conformation. Curr Top Microbiol Immunol. 1985; 114:19-102. DOI: 10.1007/978-3-642-70227-3_2. View

20.

Raji A, Zabel D, Laufer C, Depew R . Genetic analysis of mutations that compensate for loss of Escherichia coli DNA topoisomerase I. J Bacteriol. 1985; 162(3):1173-9. PMC: 215900. DOI: 10.1128/jb.162.3.1173-1179.1985. View