DNA Topoisomerase Mutations in Bacteria

  • K. Drlica
  • G. J. Pruss
  • S. H. Manes
  • S. G. Chevalier
Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)

Abstract

The chromosome of Escherichia coli is a DNA molecule having a length more than a thousand times that of the cell in which it resides (Cairns 1963). How this DNA is compacted and packaged is poorly understood. It appears that the DNA is arranged into about 50 large (100 kbp), topologically independent domains (Worcel and Burgi 1972; Sinden and Pettijohn 1981), and each of these domains, or loops, is probably under negative superhelical tension (Worcel and Burgi 1972; Sinden et al. 1980). While it is becoming increasingly clear that the superhelical tension is a result of topoisomerase action, how the loops are established and maintained is still a mystery. Another level of compaction appears to be the packaging of DNA into nucleosomelike structures (Griffith 1976; Varshavsky et al. 1977). Unfortunately, bacterial chromatin, unlike its eukaryotic counterpact, has been difficult to isolate and study.

Keywords

Recombination Titration Sedimentation Electrophoresis Fractionation 

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References

  1. Busby S, Kolb A, Buc Henri (1979) Isolation of plasmid-protein complexes horn Escherichia coli. Eur J Biochem 99:105–111PubMedCrossRefGoogle Scholar
  2. Cairns J (1963) The chromosome of Escherichia coli. Cold Spring Harbor Symp Quant Biol 28: 43–46Google Scholar
  3. Cozzarelli N (1980) DNA gyrase and the supercoiling of DNA. Science 207:953–960PubMedCrossRefGoogle Scholar
  4. Dean F, Krasnow M, Otter R, Matzuk M, Spangler S, Cozzarelli N (1983) Escherichia coli type I topoisomerases: identification, mechanism, and role in recombination. Cold Spring Harbor Symp Quant Biol 41:169–171Google Scholar
  5. DiNardo S, Voelkel K, Sternglanz R, Reynolds A, Wright A (1982) Escherichia coli DNA topo-isomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31:43–51PubMedCrossRefGoogle Scholar
  6. Dixon N, Kornberg A (1984) Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc Natl Acad Sci USA 81:424–428PubMedCrossRefGoogle Scholar
  7. Drlica K (1984) Biology of bacterial DNA topoisomerases. Microbiol Rev 48:273–289PubMedGoogle Scholar
  8. Drlica K, Snyder M (1978) Superhelical Escherichia coli DNA: relaxation by coumermycin. J Mol Biol 120:145–154PubMedCrossRefGoogle Scholar
  9. Fairweather N, Orr E, Holland I (1980) Inhibition of deoxyribonucleic acid gyrase: effects on nucleic acid synthesis and cell division in Escherichia coli K-12. J Bacteriol 142:153161Google Scholar
  10. Filutowicz M, Jonczyk P (1981) Essential role of gyrB gene product in the transcriptional event coupled to dnaA-dependent initiation of Escherichia coli chromosome replication. Mol Gen Genet 183:134–138PubMedCrossRefGoogle Scholar
  11. Filutowicz M, Jonczyk P (1983) The gyrB gene product functions in both initiation and chain polymerization of Escherichia coli chromosome replication: suppression of the initiation deficiency in gyrB-ts mutants by a class of the rpoB mutations. Mol Gen Genet 191:282–287PubMedCrossRefGoogle Scholar
  12. Fisher L, Mizuuchi K, O’Dea M, Ohmori H, Geliert M (1981) Site-specific interaction of DNA gyrase with DNA. Proc Natl Acad Sci USA 78:4165–4169PubMedCrossRefGoogle Scholar
  13. Friedman D, Olson E, Carver D, Geliert M (1984a) Synergistic effect of himA and gyrB mutations: evidence that Him functions control expression of ilv and xyl genes. J Bacteriol 157:484–489PubMedGoogle Scholar
  14. Friedman D, Pantefaber L, Olson E, Carver D, O’Dea M, Geliert M (1984b) Mutations in the DNA gyrB gene that are temperature sensitive for lambda site-specific recombination, Mu growth, and plasmid maintenance. J Bacteriol 157:490–497PubMedGoogle Scholar
  15. Geliert M (1981) DNA topoisomerases. Annu Rev Biochem 50:879-910CrossRefGoogle Scholar
  16. Geliert M, Mizuuchi K, O’Dea M, Nash H (1976a) DNA gyrase: an enzyme that introduces super-helical turns into DNA. Proc Natl Acad Sci USA 73:3872–3876CrossRefGoogle Scholar
  17. Geliert M, O’Dea M, Itoh T, Tomizawa J (1976b) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 73:4474–4478CrossRefGoogle Scholar
  18. Geliert M, Mizuuchi K, O’Dea M, Itoh T, Tomizawa J (1977) Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc Natl Acad Sci USA 74:4772–4776CrossRefGoogle Scholar
  19. Geliert M, Fisher L, O’Dea M (1979) DNA gyrase: purification and catalytic properties of a fragment of gyrase B protein. Proc Natl Acad Sci USA 76:6289–6293CrossRefGoogle Scholar
  20. Gellert M, Menzel R, Mizuuchi K, O’Dea M, Friedman D (1983) Regulation of DNA supercoiling inE. coli. Cold Spring Harbor Symp Quant Biol 47:763–767PubMedGoogle Scholar
  21. Germond J, Hirt B, Oudet P, Gross-Bellard M, Chambon P (1975) Folding of the DNA double helix in chromatin-like structures from simian virus 40. Proc Natl Acad Sci USA 72:1843–1847PubMedCrossRefGoogle Scholar
  22. Glikin G, Ruberti I, Worcel A (1984) Chromatin assembly in Xenopus oocytes: in vitro studies. Cell 37:33–41PubMedCrossRefGoogle Scholar
  23. Goldstein E, Drlica K (1984) Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci USA 81:4046–4050PubMedCrossRefGoogle Scholar
  24. Griffith J (1976) Visualization of prokaryotic DNA in a regularly condensed chromatin-like fiber. Proc Natl Acad Sci USA 73:563–567PubMedCrossRefGoogle Scholar
  25. Hill W, Fangman W (1972) Single-strand breaks in deoxyribonucleic acid and viability loss during deoxyribonucleic acid synthesis inhibition in Escherichia coli. J Bacteriol 116:1329–1335Google Scholar
  26. Kreuzer K, Cozzarelli N (1979) Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase sub unit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J Bacteriol 140:424–435PubMedGoogle Scholar
  27. Manes S, Pruss G, Drlica K (1983) Inhibition of RNA synthesis by oxolinic acid is unrelated to average DNA supercoiling. J Bacteriol 155:420–423PubMedGoogle Scholar
  28. McGhee J, Felsenfeld G (1980) Nucleosome structure. Annu Rev Biochem 49:1115–1156PubMedCrossRefGoogle Scholar
  29. Menzel R, Geliert M (1983) Regulation of the genes for E. coli gyrase: homeostatic control of DNA supercoiling. Cell 34:105–113PubMedCrossRefGoogle Scholar
  30. Morrison A, Cozzarelli N (1979) Site-specific cleavage of DNA by E. coli DNA gyrase. Cell 17: 175–184PubMedCrossRefGoogle Scholar
  31. Mukai F, Margolin P (1963) Analysis of unlinked suppressors of an 0° mutation in Salmonella. Proc Natl Acad Sci USA 50:140–148PubMedCrossRefGoogle Scholar
  32. Orr E, Fairweather N, Holland I, Pritchard R (1979) Isolation and characterization of a strain carrying a conditional lethal mutation in the cou gene of Escherichia coli K-12. Mol Gen Genet 177:103–112PubMedCrossRefGoogle Scholar
  33. Overbye K, Margolin P (1981) Role of the supX gene in ultraviolet light induced mutagenesis in Salmonella typhimurium. J Bacteriol 146:170–178PubMedGoogle Scholar
  34. Overbye K, Basu S, Margolin P (1983) Loss of DNA topoisomerase I activity alters many cellular functions in Salmonella typhimurium. Cold Spring Harbor Symp Quant Biol 47:785–791PubMedGoogle Scholar
  35. Peebles C, Higgins N, Kreuzer K, Morrison A, Brown P, Sugino A, Cozzarelli N (1979) Structure and activities of Escherichia coli DNA gyrase. Cold Spring Harbor Symp Quant Biol 43:41–52PubMedGoogle Scholar
  36. Pettijohn D, Pfenninger O (1980) Supercoils in prokaryotic DNA restrained in vivo. Proc Natl Acad Sci USA 77:1331–1335PubMedCrossRefGoogle Scholar
  37. Pisetsky D, Berkower I, Wickner P, Hurwitz J (1972) Role of ATP in DNA synthesis in Escherichia coll. J Mol Biol 71:557–571PubMedCrossRefGoogle Scholar
  38. Pruss G (1985) DNA topoisomerase I mutants: increased heterogeneity in linking number and other replicon-dependent changes in DNA supercoiling. J Mol Biol 185:51–63PubMedCrossRefGoogle Scholar
  39. Pruss G, Manes S, Drlica K (1982) Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31:35–42PubMedCrossRefGoogle Scholar
  40. Richardson SM, Higgins L, Lilley D (1984) The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J 3:1745–1752PubMedGoogle Scholar
  41. Rouviere-Yaniv J, Gros F (1975) Characterization of a novel, low molecular-weight DNA-binding protein from Escherichia coll. Proc Natl Acad Sci USA 72:3428–3432PubMedCrossRefGoogle Scholar
  42. Ryoji M, Worcel A (1984) Chromatin assembly in Xenopus oocytes: in vivo studies. Cell 37:21–32PubMedCrossRefGoogle Scholar
  43. Sinden R, Pettijohn D (1981) Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc Natl Acad Sci USA 78:224–228PubMedCrossRefGoogle Scholar
  44. Sinden R, Carlson J, Pettijohn D (1980) Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells. Cell 21:773–783PubMedCrossRefGoogle Scholar
  45. Snyder M, Drlica K (1979) DNA gyrase on the bacterial chromosome: DNA cleavage induced by oxolinic acid. J Mol Biol 131:287–302PubMedCrossRefGoogle Scholar
  46. Steck T, Drlica K (1984) Bacterial chromosome segregation: evidence for DNA gyrase involvement in decatenation. Cell 36:1081–1088PubMedCrossRefGoogle Scholar
  47. Steck T, Pruss G, Manes S, Burg L, Drlica K (1984) DNA supercoiling in gyrase mutants. J Bacteriol 158:397–403PubMedGoogle Scholar
  48. Sternglanz R, DiNardo S, Voelkel K, Nishimura Y, Hirota Y, Becherer K, Zumstein L, Wang J (1981) Mutations in the gene coding for Escherichia coli DNA topoisomerase I affecting transcription and transposition. Proc Natl Acad Sci USA 78:2747–2751PubMedCrossRefGoogle Scholar
  49. Sugino A, Peebles C, Kreuzer K, Cozzarelli N (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 74:4767–4771PubMedCrossRefGoogle Scholar
  50. Trucksis M, Golub E, Zabel D, DePew R (1981) Escherichia coli and Salmonella typhimurium supX genes specify deoxyribonucleic acid topoisomerase I. J Bacteriol 147:679–681PubMedGoogle Scholar
  51. Varshavsy A, Nedospasov V, Bakeayev V, Bakeayev T, Georgiev G (1977) Histone-like proteins in the purified Escherichia coli deoxyribonucleoprotein. Nucleic Acids Res 4:2725–2745CrossRefGoogle Scholar
  52. Villeponteau B, Lundell M, Martinson H (1984) Torsional stress promotes the DNase I sensitivity of active genes. Cell 39:469–478PubMedCrossRefGoogle Scholar
  53. Wang J (1971) Interaction between DNA and an Escherichia coli protein. J Mol biol 55:523–533PubMedCrossRefGoogle Scholar
  54. Worcel A, Burgi E (1972) On the structure of the folded chromosome of Escherichia coll. J Mol Biol 71:127–147PubMedCrossRefGoogle Scholar
  55. Wu F, Kolb A, Buc H (1982) A transcriptionally active plasmid-protein complex isolated from Escherichia coli. Biochim Biophys Acta 696:231–238PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1986

Authors and Affiliations

  • K. Drlica
    • 1
  • G. J. Pruss
    • 1
  • S. H. Manes
    • 1
  • S. G. Chevalier
    • 1
  1. 1.Department of BiologyUniversity of RochesterRochesterUSA

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