Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1986 Oct 10;14(19):7751–7765. doi: 10.1093/nar/14.19.7751

Nucleotide sequence of a type II DNA topoisomerase gene. Bacteriophage T4 gene 39.

W M Huang
PMCID: PMC311794  PMID: 3022233

Abstract

T4 DNA topoisomerase is a type II enzyme and is thought to be required for normal T4 DNA replication T4 gene 39 codes for the largest of the three subunits of T4 DNA topoisomerase. I have determined the nucleotide sequence of a region of 2568 nucleotides of T4 DNA which includes gene 39. The location of the gene was established by the identification of the first fifteen amino acids in the large open reading frame in the DNA sequence as those found at the amino-terminus of the purified 39-protein. The coding region of gene 39 has 1560 bases, and it is followed by two in-frame stop codons. The gene is preceded by a typical Shine-Dalgarno sequence as well as possible promoter sequences for E. coli RNA polymerase. T4 39-protein consists of 520 amino acids, and it has a calculated molecular weight of 58,478. By comparing the amino acid sequences, T4 39-protein is found to share homology with the gyrB subunit of DNA gyrase. This suggests that these topoisomerase subunits may be equivalent functionally. Some of the characteristics of the 39-protein and its structural features predicted from the DNA sequence data are discussed.

Full text

PDF
7765

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brutlag D. L., Clayton J., Friedland P., Kedes L. H. SEQ: a nucleotide sequence analysis and recombination system. Nucleic Acids Res. 1982 Jan 11;10(1):279–294. doi: 10.1093/nar/10.1.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  4. Fukada K., Abelson J. DNA sequence of a T4 transfer RNA gene cluster. J Mol Biol. 1980 May 25;139(3):377–391. doi: 10.1016/0022-2836(80)90136-9. [DOI] [PubMed] [Google Scholar]
  5. Fuller F. A family of cloning vectors containing the lacUV5 promoter. Gene. 1982 Jul-Aug;19(1):43–54. doi: 10.1016/0378-1119(82)90187-1. [DOI] [PubMed] [Google Scholar]
  6. Huang W. M., Buchanan J. M. Synergistic interactions of T4 early proteins concerned with their binding to DNA. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2226–2230. doi: 10.1073/pnas.71.6.2226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Huang W. M. Inhibition of initiation of bacteriophage T4 DNA replication by perturbation of Escherichia coli host membrane composition. J Virol. 1979 Dec;32(3):917–924. doi: 10.1128/jvi.32.3.917-924.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Huang W. M. Membrane-associated proteins of T4-infected Escherichia coli. Virology. 1975 Aug;66(2):508–521. doi: 10.1016/0042-6822(75)90223-8. [DOI] [PubMed] [Google Scholar]
  9. Huang W. M. Positive regulation of T-even-phage DNA replication by the DNA-delay protein of gene 39. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):495–499. doi: 10.1101/sqb.1979.043.01.055. [DOI] [PubMed] [Google Scholar]
  10. Huang W. M., Wei L. S., Casjens S. Relationship between bacteriophage T4 and T6 DNA topoisomerases. T6 39-protein subunit is equivalent to the combined T4 39- and 60-protein subunits. J Biol Chem. 1985 Jul 25;260(15):8973–8977. [PubMed] [Google Scholar]
  11. Hübscher U., Lutz H., Kornberg A. Novel histone H2A-like protein of escherichia coli. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5097–5101. doi: 10.1073/pnas.77.9.5097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol. 1981 Feb 15;146(1):1–21. doi: 10.1016/0022-2836(81)90363-6. [DOI] [PubMed] [Google Scholar]
  13. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  14. Liu L. F., Liu C. C., Alberts B. M. T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature. 1979 Oct 11;281(5731):456–461. doi: 10.1038/281456a0. [DOI] [PubMed] [Google Scholar]
  15. Liu L. F., Liu C. C., Alberts B. M. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell. 1980 Mar;19(3):697–707. doi: 10.1016/s0092-8674(80)80046-8. [DOI] [PubMed] [Google Scholar]
  16. Mattson T., Van Houwe G., Bolle A., Selzer G., Epstein R. Genetic identification of cloned fragments of bacteriophage T4 DNA and complementation by some clones containing early T4 genes. Mol Gen Genet. 1977 Sep 9;154(3):319–326. doi: 10.1007/BF00571289. [DOI] [PubMed] [Google Scholar]
  17. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McCarthy D., Minner C., Bernstein H., Bernstein C. DNA elongation rates and growing point distributions of wild-type phage T4 and a DNA-delay amber mutant. J Mol Biol. 1976 Oct 5;106(4):963–981. doi: 10.1016/0022-2836(76)90346-6. [DOI] [PubMed] [Google Scholar]
  19. McClure W. R. Mechanism and control of transcription initiation in prokaryotes. Annu Rev Biochem. 1985;54:171–204. doi: 10.1146/annurev.bi.54.070185.001131. [DOI] [PubMed] [Google Scholar]
  20. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  22. Moriya S., Ogasawara N., Yoshikawa H. Structure and function of the region of the replication origin of the Bacillus subtilis chromosome. III. Nucleotide sequence of some 10,000 base pairs in the origin region. Nucleic Acids Res. 1985 Apr 11;13(7):2251–2265. doi: 10.1093/nar/13.7.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mulligan M. E., Hawley D. K., Entriken R., McClure W. R. Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):789–800. doi: 10.1093/nar/12.1part2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Murray N. E., Bruce S. A., Murray K. Molecular cloning of the DNA ligase gene from bacteriophage T4. II. Amplification and preparation of the gene product. J Mol Biol. 1979 Aug 15;132(3):493–505. doi: 10.1016/0022-2836(79)90271-7. [DOI] [PubMed] [Google Scholar]
  25. Niggemann E., Green I., Meyer H. P., Rüger W. Physical mapping of bacteriophage T4. Mol Gen Genet. 1981;184(2):289–299. doi: 10.1007/BF00272920. [DOI] [PubMed] [Google Scholar]
  26. O'Farrell P. Z., Gold L. M., Huang W. M. The identification of prereplicative bacteriophage T4 proteins. J Biol Chem. 1973 Aug 10;248(15):5499–5501. [PubMed] [Google Scholar]
  27. Ollis D. L., Brick P., Hamlin R., Xuong N. G., Steitz T. A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. 1985 Feb 28-Mar 6Nature. 313(6005):762–766. doi: 10.1038/313762a0. [DOI] [PubMed] [Google Scholar]
  28. Post L. E., Nomura M. DNA sequences from the str operon of Escherichia coli. J Biol Chem. 1980 May 25;255(10):4660–4666. [PubMed] [Google Scholar]
  29. Remaut E., Stanssens P., Fiers W. Plasmid vectors for high-efficiency expression controlled by the PL promoter of coliphage lambda. Gene. 1981 Oct;15(1):81–93. doi: 10.1016/0378-1119(81)90106-2. [DOI] [PubMed] [Google Scholar]
  30. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schiffer M., Edmundson A. B. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys J. 1967 Mar;7(2):121–135. doi: 10.1016/S0006-3495(67)86579-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Selzer G., Bolle A., Krisch B., Epstein R. Construction and properties of recombinant plasmids containing the rII genes of bacteriophage T4. Mol Gen Genet. 1978 Feb 27;159(3):301–309. doi: 10.1007/BF00268267. [DOI] [PubMed] [Google Scholar]
  33. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Snyder L., Gold L., Kutter E. A gene of bacteriophage T4 whose product prevents true late transcription on cytosine-containing T4 DNA. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3098–3102. doi: 10.1073/pnas.73.9.3098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stetler G. L., King G. J., Huang W. M. T4 DNA-delay proteins, required for specific DNA replication, form a complex that has ATP-dependent DNA topoisomerase activity. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3737–3741. doi: 10.1073/pnas.76.8.3737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stüber D., Bujard H. Organization of transcriptional signals in plasmids pBR322 and pACYC184. Proc Natl Acad Sci U S A. 1981 Jan;78(1):167–171. doi: 10.1073/pnas.78.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sutcliffe J. G. Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):77–90. doi: 10.1101/sqb.1979.043.01.013. [DOI] [PubMed] [Google Scholar]
  39. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang J. C. DNA topoisomerases. Annu Rev Biochem. 1985;54:665–697. doi: 10.1146/annurev.bi.54.070185.003313. [DOI] [PubMed] [Google Scholar]
  41. Weiss B., Richardson C. C. Enzymatic breakage and joining of deoxyribonucleic acid, I. Repair of single-strand breaks in DNA by an enzyme system from Escherichia coli infected with T4 bacteriophage. Proc Natl Acad Sci U S A. 1967 Apr;57(4):1021–1028. doi: 10.1073/pnas.57.4.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zubay G. In vitro synthesis of protein in microbial systems. Annu Rev Genet. 1973;7:267–287. doi: 10.1146/annurev.ge.07.120173.001411. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES