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. 1986 Oct;60(1):114–123. doi: 10.1128/jvi.60.1.114-123.1986

Organization of the thymidylate synthase gene of herpesvirus saimiri.

W Bodemer, H H Niller, N Nitsche, B Scholz, B Fleckenstein
PMCID: PMC253908  PMID: 3018278

Abstract

Herpesvirus saimiri codes, unlike most other herpesviruses, for a thymidylate synthase (TS). The TS gene of herpesvirus saimiri is unusual in structure and regulation of expression. It is transcribed into a nonspliced mRNA of 2,190 nucleotides. The single open reading frame of the viral TS gene, instructing a polypeptide of 33.5 kilodaltons, has extensive sequence homology with the corresponding TS coding sequences of human cells and of various procaryotes; the putative polypeptide derived from the nucleotide sequence of the herpesvirus saimiri TS gene is 70% identical with the human enzyme. The untranslated regions of the herpesvirus saimiri TS gene do not share homology with the other characterized eucaryotic or bacterial TS genes. The 5' untranslated sequence has 22 ATG triplets shortly followed by stop codons. The herpesvirus saimiri TS gene, which may be weakly transcribed during immediate early and early times of virus replication, is maximally expressed at the late phase. Various parameters suggest that the TS gene has been acquired in virus evolution by an ancestral herpesvirus from the cellular genome.

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Selected References

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

  1. Akrigg A., Wilkinson G. W., Oram J. D. The structure of the major immediate early gene of human cytomegalovirus strain AD169. Virus Res. 1985 Mar;2(2):107–121. doi: 10.1016/0168-1702(85)90242-4. [DOI] [PubMed] [Google Scholar]
  2. Ayusawa D., Shimizu K., Koyama H., Takeishi K., Seno T. Accumulation of DNA strand breaks during thymineless death in thymidylate synthase-negative mutants of mouse FM3A cells. J Biol Chem. 1983 Oct 25;258(20):12448–12454. [PubMed] [Google Scholar]
  3. Baer R., Bankier A. T., Biggin M. D., Deininger P. L., Farrell P. J., Gibson T. J., Hatfull G., Hudson G. S., Satchwell S. C., Séguin C. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature. 1984 Jul 19;310(5974):207–211. doi: 10.1038/310207a0. [DOI] [PubMed] [Google Scholar]
  4. Belfort M., Maley G., Pedersen-Lane J., Maley F. Primary structure of the Escherichia coli thyA gene and its thymidylate synthase product. Proc Natl Acad Sci U S A. 1983 Aug;80(16):4914–4918. doi: 10.1073/pnas.80.16.4914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  6. Bodemer W., Knust E., Angermüller S., Fleckenstein B. Immediate-early transcription of Herpesvirus saimiri. J Virol. 1984 Aug;51(2):452–457. doi: 10.1128/jvi.51.2.452-457.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chu F. K., Maley G. F., Maley F., Belfort M. Intervening sequence in the thymidylate synthase gene of bacteriophage T4. Proc Natl Acad Sci U S A. 1984 May;81(10):3049–3053. doi: 10.1073/pnas.81.10.3049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Collins T., Ginsburg D., Boss J. M., Orkin S. H., Pober J. S. Cultured human endothelial cells express platelet-derived growth factor B chain: cDNA cloning and structural analysis. Nature. 1985 Aug 22;316(6030):748–750. doi: 10.1038/316748a0. [DOI] [PubMed] [Google Scholar]
  9. Darveau A., Pelletier J., Sonenberg N. Differential efficiencies of in vitro translation of mouse c-myc transcripts differing in the 5' untranslated region. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2315–2319. doi: 10.1073/pnas.82.8.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Desrosiers R. C. Herpesvirus saimiri DNA in tumor cells--deleted sequences and sequence rearrangements. J Virol. 1981 Aug;39(2):497–509. doi: 10.1128/jvi.39.2.497-509.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dull T. J., Gray A., Hayflick J. S., Ullrich A. Insulin-like growth factor II precursor gene organization in relation to insulin gene family. 1984 Aug 30-Sep 5Nature. 310(5980):777–781. doi: 10.1038/310777a0. [DOI] [PubMed] [Google Scholar]
  13. Ebeling A., Keil G., Nowak B., Fleckenstein B., Berthelot N., Sheldrick P. Genome structure and virion polypeptides of the primate herpesviruses Herpesvirus aotus types 1 and 3: comparison with human cytomegalovirus. J Virol. 1983 Feb;45(2):715–726. doi: 10.1128/jvi.45.2.715-726.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Favaloro J., Treisman R., Kamen R. Transcription maps of polyoma virus-specific RNA: analysis by two-dimensional nuclease S1 gel mapping. Methods Enzymol. 1980;65(1):718–749. doi: 10.1016/s0076-6879(80)65070-8. [DOI] [PubMed] [Google Scholar]
  15. Fleckenstein B. Oncogenic herpesviruses of non-human primates. Biochim Biophys Acta. 1979 Nov 30;560(3):301–342. doi: 10.1016/0304-419x(79)90007-6. [DOI] [PubMed] [Google Scholar]
  16. Gil A., Proudfoot N. J. A sequence downstream of AAUAAA is required for rabbit beta-globin mRNA 3'-end formation. 1984 Nov 29-Dec 5Nature. 312(5993):473–474. doi: 10.1038/312473a0. [DOI] [PubMed] [Google Scholar]
  17. Glisin V., Crkvenjakov R., Byus C. Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry. 1974 Jun 4;13(12):2633–2637. doi: 10.1021/bi00709a025. [DOI] [PubMed] [Google Scholar]
  18. Hinnebusch A. G. A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Sep;5(9):2349–2360. doi: 10.1128/mcb.5.9.2349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  20. Honess R. W., Bodemer W., Cameron K. R., Niller H. H., Fleckenstein B., Randall R. E. The A+T-rich genome of Herpesvirus saimiri contains a highly conserved gene for thymidylate synthase. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3604–3608. doi: 10.1073/pnas.83.11.3604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Iltis J. P., Oakes J. E., Hyman R. W., Rapp F. Comparison of the DNAs of varicella-zoster viruses isolated from clinical cases of varicella and herpes zoster. Virology. 1977 Oct 15;82(2):345–352. doi: 10.1016/0042-6822(77)90009-5. [DOI] [PubMed] [Google Scholar]
  22. Jahn G., Knust E., Schmolla H., Sarre T., Nelson J. A., McDougall J. K., Fleckenstein B. Predominant immediate-early transcripts of human cytomegalovirus AD 169. J Virol. 1984 Feb;49(2):363–370. doi: 10.1128/jvi.49.2.363-370.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kaschka-Dierich C., Werner F. J., Bauer I., Fleckenstein B. Structure of nonintegrated, circular Herpesvirus saimiri and Herpesvirus ateles genomes in tumor cell lines and in vitro-transformed cells. J Virol. 1982 Oct;44(1):295–310. doi: 10.1128/jvi.44.1.295-310.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Keil G. M., Ebeling-Keil A., Koszinowski U. H. Temporal regulation of murine cytomegalovirus transcription and mapping of viral RNA synthesized at immediate early times after infection. J Virol. 1984 Jun;50(3):784–795. doi: 10.1128/jvi.50.3.784-795.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Knust E., Dietrich W., Fleckenstein B., Bodemer W. Virus-specific transcription in a Herpesvirus saimiri-transformed lymphoid tumor cell line. J Virol. 1983 Nov;48(2):377–383. doi: 10.1128/jvi.48.2.377-383.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lee D. C., Roeder R. G. Transcription of adenovirus type 2 genes in a cell-free system: apparent heterogeneity of initiation at some promoters. Mol Cell Biol. 1981 Jul;1(7):635–651. doi: 10.1128/mcb.1.7.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Maley G. F., Bellisario R. L., Guarino D. U., Maley F. The primary structure of Lactobacillus casei thymidylate synthetase. III. The use of 2-(2-nitrophenylsulfenyl)-3-methyl-3-bromoindolenine and limited tryptic peptides to establish the complete amino acid sequence of the enzyme. J Biol Chem. 1979 Feb 25;254(4):1301–1304. [PubMed] [Google Scholar]
  28. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  29. McDevitt M. A., Imperiale M. J., Ali H., Nevins J. R. Requirement of a downstream sequence for generation of a poly(A) addition site. Cell. 1984 Jul;37(3):993–999. doi: 10.1016/0092-8674(84)90433-1. [DOI] [PubMed] [Google Scholar]
  30. Roizman B. The structure and isomerization of herpes simplex virus genomes. Cell. 1979 Mar;16(3):481–494. doi: 10.1016/0092-8674(79)90023-0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Schirm S., Müller I., Desrosiers R. C., Fleckenstein B. Herpesvirus saimiri DNA in a lymphoid cell line established by in vitro transformation. J Virol. 1984 Mar;49(3):938–946. doi: 10.1128/jvi.49.3.938-946.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schirm S., Weber F., Schaffner W., Fleckenstein B. A transcription enhancer in the Herpesvirus saimiri genome. EMBO J. 1985 Oct;4(10):2669–2674. doi: 10.1002/j.1460-2075.1985.tb03986.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Seeburg P. H., Adelman J. P. Characterization of cDNA for precursor of human luteinizing hormone releasing hormone. Nature. 1984 Oct 18;311(5987):666–668. doi: 10.1038/311666a0. [DOI] [PubMed] [Google Scholar]
  35. Takeishi K., Kaneda S., Ayusawa D., Shimizu K., Gotoh O., Seno T. Nucleotide sequence of a functional cDNA for human thymidylate synthase. Nucleic Acids Res. 1985 Mar 25;13(6):2035–2043. doi: 10.1093/nar/13.6.2035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thireos G., Penn M. D., Greer H. 5' untranslated sequences are required for the translational control of a yeast regulatory gene. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5096–5100. doi: 10.1073/pnas.81.16.5096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watson R. J., Weis J. H., Salstrom J. S., Enquist L. W. Herpes simplex virus type-1 glycoprotein D gene: nucleotide sequence and expression in Escherichia coli. Science. 1982 Oct 22;218(4570):381–384. doi: 10.1126/science.6289440. [DOI] [PubMed] [Google Scholar]
  38. Werner F. J., Bornkamm G. W., Fleckenstein B. Episomal viral DNA in a Herpesvirus saimiri-transformed lymphoid cell line. J Virol. 1977 Jun;22(3):794–803. doi: 10.1128/jvi.22.3.794-803.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]

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