Abstract
Nucleotide sequencing of the vaccinia virus SalI F DNA fragment identified an open reading frame of 552 amino acids encoding a protein of 63.3 kDa. The deduced amino acid sequence shares 30% identity with S. pombe and S. cerevisiae DNA ligases, with homology strongest near the carboxy terminus and around the lysine residue required for ligase-adenylate formation. Prokaryotic DNA ligases are poorly related to the vaccinia sequence. The initiation codon of the ORF forms part of a late transcriptional initiation sequence TAAATG and is preceded by two overlapping early transcriptional termination signals, TTTTTTTAT. Nonetheless, RNA mapping showed that the ligase gene is transcribed early during infection and the 5' end of the mRNA maps to the TAAATG motif. The possible roles of a DNA ligase in vaccinia virus DNA replication and recombination are discussed.
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- Armstrong J., Brown R. S., Tsugita A. Primary structure and genetic organization of phage T4 DNA ligase. Nucleic Acids Res. 1983 Oct 25;11(20):7145–7156. doi: 10.1093/nar/11.20.7145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baldick C. J., Jr, Moss B. Resistance of vaccinia virus to rifampicin conferred by a single nucleotide substitution near the predicted NH2 terminus of a gene encoding an Mr 62,000 polypeptide. Virology. 1987 Jan;156(1):138–145. doi: 10.1016/0042-6822(87)90444-2. [DOI] [PubMed] [Google Scholar]
- Bankier A. T., Weston K. M., Barrell B. G. Random cloning and sequencing by the M13/dideoxynucleotide chain termination method. Methods Enzymol. 1987;155:51–93. doi: 10.1016/0076-6879(87)55009-1. [DOI] [PubMed] [Google Scholar]
- Barker D. G., White J. H., Johnston L. H. Molecular characterisation of the DNA ligase gene, CDC17, from the fission yeast Schizosaccharomyces pombe. Eur J Biochem. 1987 Feb 2;162(3):659–667. doi: 10.1111/j.1432-1033.1987.tb10688.x. [DOI] [PubMed] [Google Scholar]
- Barker D. G., White J. H., Johnston L. H. The nucleotide sequence of the DNA ligase gene (CDC9) from Saccharomyces cerevisiae: a gene which is cell-cycle regulated and induced in response to DNA damage. Nucleic Acids Res. 1985 Dec 9;13(23):8323–8337. doi: 10.1093/nar/13.23.8323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baroudy B. M., Venkatesan S., Moss B. Incompletely base-paired flip-flop terminal loops link the two DNA strands of the vaccinia virus genome into one uninterrupted polynucleotide chain. Cell. 1982 Feb;28(2):315–324. doi: 10.1016/0092-8674(82)90349-x. [DOI] [PubMed] [Google Scholar]
- Baroudy B. M., Venkatesan S., Moss B. Structure and replication of vaccinia virus telomeres. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):723–729. doi: 10.1101/sqb.1983.047.01.083. [DOI] [PubMed] [Google Scholar]
- Barton G. J., Sternberg M. J. A strategy for the rapid multiple alignment of protein sequences. Confidence levels from tertiary structure comparisons. J Mol Biol. 1987 Nov 20;198(2):327–337. doi: 10.1016/0022-2836(87)90316-0. [DOI] [PubMed] [Google Scholar]
- Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
- Bertholet C., Drillien R., Wittek R. One hundred base pairs of 5' flanking sequence of a vaccinia virus late gene are sufficient to temporally regulate late transcription. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2096–2100. doi: 10.1073/pnas.82.7.2096. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bertholet C., Van Meir E., ten Heggeler-Bordier B., Wittek R. Vaccinia virus produces late mRNAs by discontinuous synthesis. Cell. 1987 Jul 17;50(2):153–162. doi: 10.1016/0092-8674(87)90211-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boone R. F., Moss B. Methylated 5'-terminal sequences of vaccinia virus mRNA species made in vivo at early and late times after infection. Virology. 1977 Jun 1;79(1):67–80. doi: 10.1016/0042-6822(77)90335-x. [DOI] [PubMed] [Google Scholar]
- Broyles S. S., Moss B. Homology between RNA polymerases of poxviruses, prokaryotes, and eukaryotes: nucleotide sequence and transcriptional analysis of vaccinia virus genes encoding 147-kDa and 22-kDa subunits. Proc Natl Acad Sci U S A. 1986 May;83(10):3141–3145. doi: 10.1073/pnas.83.10.3141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Challberg M. D., Englund P. T. Purification and properties of the deoxyribonucleic acid polymerase induced by vaccinia virus. J Biol Chem. 1979 Aug 25;254(16):7812–7819. [PubMed] [Google Scholar]
- Chan J. Y., Becker F. F., German J., Ray J. H. Altered DNA ligase I activity in Bloom's syndrome cells. Nature. 1987 Jan 22;325(6102):357–359. doi: 10.1038/325357a0. [DOI] [PubMed] [Google Scholar]
- Dunn J. J., Studier F. W. Nucleotide sequence from the genetic left end of bacteriophage T7 DNA to the beginning of gene 4. J Mol Biol. 1981 Jun 5;148(4):303–330. doi: 10.1016/0022-2836(81)90178-9. [DOI] [PubMed] [Google Scholar]
- Earl P. L., Jones E. V., Moss B. Homology between DNA polymerases of poxviruses, herpesviruses, and adenoviruses: nucleotide sequence of the vaccinia virus DNA polymerase gene. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3659–3663. doi: 10.1073/pnas.83.11.3659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Esteban M., Flores L., Holowczak J. A. Model for vaccinia virus DNA replication. Virology. 1977 Dec;83(2):467–473. doi: 10.1016/0042-6822(77)90197-0. [DOI] [PubMed] [Google Scholar]
- Fuerst T. R., Fernandez M. P., Moss B. Transfer of the inducible lac repressor/operator system from Escherichia coli to a vaccinia virus expression vector. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2549–2553. doi: 10.1073/pnas.86.8.2549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Funahashi S., Sato T., Shida H. Cloning and characterization of the gene encoding the major protein of the A-type inclusion body of cowpox virus. J Gen Virol. 1988 Jan;69(Pt 1):35–47. doi: 10.1099/0022-1317-69-1-35. [DOI] [PubMed] [Google Scholar]
- Hruby D. E., Ball L. A. Mapping and identification of the vaccinia virus thymidine kinase gene. J Virol. 1982 Aug;43(2):403–409. doi: 10.1128/jvi.43.2.403-409.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hänggi M., Bannwarth W., Stunnenberg H. G. Conserved TAAAT motif in vaccinia virus late promoters: overlapping TATA box and site of transcription initiation. EMBO J. 1986 May;5(5):1071–1076. doi: 10.1002/j.1460-2075.1986.tb04324.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishino Y., Shinagawa H., Makino K., Tsunasawa S., Sakiyama F., Nakata A. Nucleotide sequence of the lig gene and primary structure of DNA ligase of Escherichia coli. Mol Gen Genet. 1986 Jul;204(1):1–7. doi: 10.1007/BF00330179. [DOI] [PubMed] [Google Scholar]
- Jones E. V., Moss B. Mapping of the vaccinia virus DNA polymerase gene by marker rescue and cell-free translation of selected RNA. J Virol. 1984 Jan;49(1):72–77. doi: 10.1128/jvi.49.1.72-77.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones E. V., Puckett C., Moss B. DNA-dependent RNA polymerase subunits encoded within the vaccinia virus genome. J Virol. 1987 Jun;61(6):1765–1771. doi: 10.1128/jvi.61.6.1765-1771.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kates J. R., McAuslan B. R. Poxvirus DNA-dependent RNA polymerase. Proc Natl Acad Sci U S A. 1967 Jul;58(1):134–141. doi: 10.1073/pnas.58.1.134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lakritz N., Foglesong P. D., Reddy M., Baum S., Hurwitz J., Bauer W. R. A vaccinia virus DNase preparation which cross-links superhelical DNA. J Virol. 1985 Mar;53(3):935–943. doi: 10.1128/jvi.53.3.935-943.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee-Chen G. J., Bourgeois N., Davidson K., Condit R. C., Niles E. G. Structure of the transcription initiation and termination sequences of seven early genes in the vaccinia virus HindIII D fragment. Virology. 1988 Mar;163(1):64–79. doi: 10.1016/0042-6822(88)90234-6. [DOI] [PubMed] [Google Scholar]
- Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
- Martin S. A., Paoletti E., Moss B. Purification of mRNA guanylyltransferase and mRNA (guanine-7-) methyltransferase from vaccinia virions. J Biol Chem. 1975 Dec 25;250(24):9322–9329. [PubMed] [Google Scholar]
- Morgan J. R., Cohen L. K., Roberts B. E. Identification of the DNA sequences encoding the large subunit of the mRNA-capping enzyme of vaccinia virus. J Virol. 1984 Oct;52(1):206–214. doi: 10.1128/jvi.52.1.206-214.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mosig G. The essential role of recombination in phage T4 growth. Annu Rev Genet. 1987;21:347–371. doi: 10.1146/annurev.ge.21.120187.002023. [DOI] [PubMed] [Google Scholar]
- Moyer R. W., Graves R. L. The mechanism of cytoplasmic orthopoxvirus DNA replication. Cell. 1981 Dec;27(2 Pt 1):391–401. doi: 10.1016/0092-8674(81)90422-0. [DOI] [PubMed] [Google Scholar]
- Munyon W., Paoletti E., Grace J. T., Jr RNA polymerase activity in purified infectious vaccinia virus. Proc Natl Acad Sci U S A. 1967 Dec;58(6):2280–2287. doi: 10.1073/pnas.58.6.2280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niles E. G., Condit R. C., Caro P., Davidson K., Matusick L., Seto J. Nucleotide sequence and genetic map of the 16-kb vaccinia virus HindIII D fragment. Virology. 1986 Aug;153(1):96–112. doi: 10.1016/0042-6822(86)90011-5. [DOI] [PubMed] [Google Scholar]
- Patel D. D., Pickup D. J. Messenger RNAs of a strongly-expressed late gene of cowpox virus contain 5'-terminal poly(A) sequences. EMBO J. 1987 Dec 1;6(12):3787–3794. doi: 10.1002/j.1460-2075.1987.tb02714.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patel D. D., Pickup D. J. The second-largest subunit of the poxvirus RNA polymerase is similar to the corresponding subunits of procaryotic and eucaryotic RNA polymerases. J Virol. 1989 Mar;63(3):1076–1086. doi: 10.1128/jvi.63.3.1076-1086.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pogo B. G., Dales S. Two deoxyribonuclease activities within purified vaccinia virus. Proc Natl Acad Sci U S A. 1969 Jul;63(3):820–827. doi: 10.1073/pnas.63.3.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pogo B. G., O'Shea M. T. The mode of replication of vaccinia virus DNA. Virology. 1978 Jan;84(1):1–8. doi: 10.1016/0042-6822(78)90213-1. [DOI] [PubMed] [Google Scholar]
- Reddy M. K., Bauer W. R. Activation of the vaccinia virus nicking-joining enzyme by trypsinization. J Biol Chem. 1989 Jan 5;264(1):443–449. [PubMed] [Google Scholar]
- Rosel J. L., Earl P. L., Weir J. P., Moss B. Conserved TAAATG sequence at the transcriptional and translational initiation sites of vaccinia virus late genes deduced by structural and functional analysis of the HindIII H genome fragment. J Virol. 1986 Nov;60(2):436–449. doi: 10.1128/jvi.60.2.436-449.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sambrook J., Shatkin A. J. Polynucleotide ligase activity in cells infected with simian virus 40, polyoma virus, or vaccinia virus. J Virol. 1969 Nov;4(5):719–726. doi: 10.1128/jvi.4.5.719-726.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Schmitt J. F., Stunnenberg H. G. Sequence and transcriptional analysis of the vaccinia virus HindIII I fragment. J Virol. 1988 Jun;62(6):1889–1897. doi: 10.1128/jvi.62.6.1889-1897.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwer B., Visca P., Vos J. C., Stunnenberg H. G. Discontinuous transcription or RNA processing of vaccinia virus late messengers results in a 5' poly(A) leader. Cell. 1987 Jul 17;50(2):163–169. doi: 10.1016/0092-8674(87)90212-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaffer R., Traktman P. Vaccinia virus encapsidates a novel topoisomerase with the properties of a eucaryotic type I enzyme. J Biol Chem. 1987 Jul 5;262(19):9309–9315. [PubMed] [Google Scholar]
- Shuman S., Moss B. Identification of a vaccinia virus gene encoding a type I DNA topoisomerase. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7478–7482. doi: 10.1073/pnas.84.21.7478. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slabaugh M., Roseman N., Davis R., Mathews C. Vaccinia virus-encoded ribonucleotide reductase: sequence conservation of the gene for the small subunit and its amplification in hydroxyurea-resistant mutants. J Virol. 1988 Feb;62(2):519–527. doi: 10.1128/jvi.62.2.519-527.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spadari S. Properties of DNA ligase from uninfected and virus-infected HeLa cells. Nucleic Acids Res. 1976 Aug;3(8):2155–2167. doi: 10.1093/nar/3.8.2155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staden R. A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res. 1980 Aug 25;8(16):3673–3694. doi: 10.1093/nar/8.16.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tengelsen L. A., Slabaugh M. B., Bibler J. K., Hruby D. E. Nucleotide sequence and molecular genetic analysis of the large subunit of ribonucleotide reductase encoded by vaccinia virus. Virology. 1988 May;164(1):121–131. doi: 10.1016/0042-6822(88)90627-7. [DOI] [PubMed] [Google Scholar]
- Traktman P., Sridhar P., Condit R. C., Roberts B. E. Transcriptional mapping of the DNA polymerase gene of vaccinia virus. J Virol. 1984 Jan;49(1):125–131. doi: 10.1128/jvi.49.1.125-131.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weir J. P., Bajszár G., Moss B. Mapping of the vaccinia virus thymidine kinase gene by marker rescue and by cell-free translation of selected mRNA. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1210–1214. doi: 10.1073/pnas.79.4.1210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weir J. P., Moss B. Nucleotide sequence of the vaccinia virus thymidine kinase gene and the nature of spontaneous frameshift mutations. J Virol. 1983 May;46(2):530–537. doi: 10.1128/jvi.46.2.530-537.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willis A. E., Lindahl T. DNA ligase I deficiency in Bloom's syndrome. Nature. 1987 Jan 22;325(6102):355–357. doi: 10.1038/325355a0. [DOI] [PubMed] [Google Scholar]
- Yuen L., Moss B. Oligonucleotide sequence signaling transcriptional termination of vaccinia virus early genes. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6417–6421. doi: 10.1073/pnas.84.18.6417. [DOI] [PMC free article] [PubMed] [Google Scholar]