Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1988 Mar;62(3):757–767. doi: 10.1128/jvi.62.3.757-767.1988

Conservation of gene organization in the lymphotropic herpesviruses herpesvirus Saimiri and Epstein-Barr virus.

U A Gompels 1, M A Craxton 1, R W Honess 1
PMCID: PMC253629  PMID: 2828671

Abstract

By analyses of short DNA sequences, we have deduced the overall arrangement of genes in the (A + T)-rich coding sequences of herpesvirus saimiri (HVS) relative to the arrangements of homologous genes in the (G + C)-rich coding sequences of the Epstein-Barr virus (EBV) genome and the (A + T)-rich sequences of the varicella-zoster virus (VZV) genome. Fragments of HVS DNA from 13 separate sites within the 111 kilobase pairs of the light DNA coding sequences of the genome were subcloned into M13 vectors, and sequences of up to 350 bases were determined from each of these sites. Amino acid sequences predicted for fragments of open reading frames defined by these sequences were compared with a library of the protein sequences of major open reading frames predicted from the complete DNA sequences of VZV and EBV. Of the 13 short amino acid sequences obtained from HVS, only 3 were recognizably homologous to proteins encoded by VZV, but all 13 HVS sequences were unambiguously homologous to gene products encoded by EBV. The HVS reading frames identified by this method included homologs of the major capsid polypeptides, glycoprotein H, the major nonstructural DNA-binding protein, thymidine kinase, and the homolog of the regulatory gene product of the BMLF1 reading frame of EBV. Locally as well as globally, the order and relative orientation of these genes resembled that of their homologs on the EBV genome. Despite the major differences in their nucleotide compositions and in the nature and arrangements of reiterated DNA sequences, the genomes of the lymphotropic herpesviruses HVS and EBV encode closely related proteins, and they share a common organization of these coding sequences which differs from that of the neurotropic herpesviruses, VZV and herpes simplex virus.

Full text

PDF
757

Selected References

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

  1. 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]
  2. Bankier A. T., Dietrich W., Baer R., Barrell B. G., Colbère-Garapin F., Fleckenstein B., Bodemer W. Terminal repetitive sequences in herpesvirus saimiri virion DNA. J Virol. 1985 Jul;55(1):133–139. doi: 10.1128/jvi.55.1.133-139.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Bird A. P. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res. 1980 Apr 11;8(7):1499–1504. doi: 10.1093/nar/8.7.1499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blair E. D., Honess R. W. DNA-binding proteins specified by herpesvirus saimiri. J Gen Virol. 1983 Dec;64(Pt 12):2697–2715. doi: 10.1099/0022-1317-64-12-2697. [DOI] [PubMed] [Google Scholar]
  7. Bodemer W., Niller H. H., Nitsche N., Scholz B., Fleckenstein B. Organization of the thymidylate synthase gene of herpesvirus saimiri. J Virol. 1986 Oct;60(1):114–123. doi: 10.1128/jvi.60.1.114-123.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cameron K. R., Stamminger T., Craxton M., Bodemer W., Honess R. W., Fleckenstein B. The 160,000-Mr virion protein encoded at the right end of the herpesvirus saimiri genome is homologous to the 140,000-Mr membrane antigen encoded at the left end of the Epstein-Barr virus genome. J Virol. 1987 Jul;61(7):2063–2070. doi: 10.1128/jvi.61.7.2063-2070.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen C. W., Thomas C. A., Jr Recovery of DNA segments from agarose gels. Anal Biochem. 1980 Jan 15;101(2):339–341. doi: 10.1016/0003-2697(80)90197-9. [DOI] [PubMed] [Google Scholar]
  10. Chevallier-Greco A., Manet E., Chavrier P., Mosnier C., Daillie J., Sergeant A. Both Epstein-Barr virus (EBV)-encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J. 1986 Dec 1;5(12):3243–3249. doi: 10.1002/j.1460-2075.1986.tb04635.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Costa R. H., Draper K. G., Kelly T. J., Wagner E. K. An unusual spliced herpes simplex virus type 1 transcript with sequence homology to Epstein-Barr virus DNA. J Virol. 1985 May;54(2):317–328. doi: 10.1128/jvi.54.2.317-328.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davison A. J., McGeoch D. J. Evolutionary comparisons of the S segments in the genomes of herpes simplex virus type 1 and varicella-zoster virus. J Gen Virol. 1986 Apr;67(Pt 4):597–611. doi: 10.1099/0022-1317-67-4-597. [DOI] [PubMed] [Google Scholar]
  13. Davison A. J., Scott J. E. DNA sequence of the major capsid protein gene of herpes simplex virus type 1. J Gen Virol. 1986 Oct;67(Pt 10):2279–2286. doi: 10.1099/0022-1317-67-10-2279. [DOI] [PubMed] [Google Scholar]
  14. Davison A. J., Scott J. E. The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986 Sep;67(Pt 9):1759–1816. doi: 10.1099/0022-1317-67-9-1759. [DOI] [PubMed] [Google Scholar]
  15. Davison A. J., Taylor P. Genetic relations between varicella-zoster virus and Epstein-Barr virus. J Gen Virol. 1987 Apr;68(Pt 4):1067–1079. doi: 10.1099/0022-1317-68-4-1067. [DOI] [PubMed] [Google Scholar]
  16. Davison A. J., Wilkie N. M. Location and orientation of homologous sequences in the genomes of five herpesviruses. J Gen Virol. 1983 Sep;64(Pt 9):1927–1942. doi: 10.1099/0022-1317-64-9-1927. [DOI] [PubMed] [Google Scholar]
  17. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  18. Desrosiers R. C., Bakker A., Kamine J., Falk L. A., Hunt R. D., King N. W. A region of the Herpesvirus saimiri genome required for oncogenicity. Science. 1985 Apr 12;228(4696):184–187. doi: 10.1126/science.2983431. [DOI] [PubMed] [Google Scholar]
  19. Desrosiers R. C., Mulder C., Fleckenstein B. Methylation of Herpesvirus saimiri DNA in lymphoid tumor cell lines. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3839–3843. doi: 10.1073/pnas.76.8.3839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Desrosiers R. C., Silva D. P., Waldron L. M., Letvin N. L. Nononcogenic deletion mutants of herpesvirus saimiri are defective for in vitro immortalization. J Virol. 1986 Feb;57(2):701–705. doi: 10.1128/jvi.57.2.701-705.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Falk L. A., Wolfe L. G., Deinhardt F. Isolation of Herpesvirus saimiri from blood of squirrel monkeys (Saimiri sciureus). J Natl Cancer Inst. 1972 May;48(5):1499–1505. [PubMed] [Google Scholar]
  22. Feng D. F., Johnson M. S., Doolittle R. F. Aligning amino acid sequences: comparison of commonly used methods. J Mol Evol. 1984;21(2):112–125. doi: 10.1007/BF02100085. [DOI] [PubMed] [Google Scholar]
  23. Gibson T., Stockwell P., Ginsburg M., Barrell B. Homology between two EBV early genes and HSV ribonucleotide reductase and 38K genes. Nucleic Acids Res. 1984 Jun 25;12(12):5087–5099. doi: 10.1093/nar/12.12.5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Goad W. B. Computational analysis of genetic sequences. Annu Rev Biophys Biophys Chem. 1986;15:79–95. doi: 10.1146/annurev.bb.15.060186.000455. [DOI] [PubMed] [Google Scholar]
  25. Godowski P. J., Knipe D. M. Identification of a herpes simplex virus function that represses late gene expression from parental viral genomes. J Virol. 1985 Aug;55(2):357–365. doi: 10.1128/jvi.55.2.357-365.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gompels U., Minson A. The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology. 1986 Sep;153(2):230–247. doi: 10.1016/0042-6822(86)90026-7. [DOI] [PubMed] [Google Scholar]
  27. Hell W., Modrow S., Wolf H. Mapping of herpesvirus saimiri proteins on the viral genome: proteins dependent and not dependent on viral DNA synthesis. J Virol. 1985 Nov;56(2):414–418. doi: 10.1128/jvi.56.2.414-418.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Honess R. W. Herpes simplex and 'the herpes complex': diverse observations and a unifying hypothesis. The eighth Fleming lecture. J Gen Virol. 1984 Dec;65(Pt 12):2077–2107. doi: 10.1099/0022-1317-65-12-2077. [DOI] [PubMed] [Google Scholar]
  30. Honess R. W., Watson D. H. Unity and diversity in the herpesviruses. J Gen Virol. 1977 Oct;37(1):15–37. doi: 10.1099/0022-1317-37-1-15. [DOI] [PubMed] [Google Scholar]
  31. Knust E., Schirm S., Dietrich W., Bodemer W., Kolb E., Fleckenstein B. Cloning of Herpesvirus saimiri DNA fragments representing the entire L-region of the genome. Gene. 1983 Nov;25(2-3):281–289. doi: 10.1016/0378-1119(83)90232-9. [DOI] [PubMed] [Google Scholar]
  32. Kouzarides T., Bankier A. T., Satchwell S. C., Weston K., Tomlinson P., Barrell B. G. Large-scale rearrangement of homologous regions in the genomes of HCMV and EBV. Virology. 1987 Apr;157(2):397–413. doi: 10.1016/0042-6822(87)90282-0. [DOI] [PubMed] [Google Scholar]
  33. Lieberman P. M., O'Hare P., Hayward G. S., Hayward S. D. Promiscuous trans activation of gene expression by an Epstein-Barr virus-encoded early nuclear protein. J Virol. 1986 Oct;60(1):140–148. doi: 10.1128/jvi.60.1.140-148.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Littler E., Zeuthen J., McBride A. A., Trøst Sørensen E., Powell K. L., Walsh-Arrand J. E., Arrand J. R. Identification of an Epstein-Barr virus-coded thymidine kinase. EMBO J. 1986 Aug;5(8):1959–1966. doi: 10.1002/j.1460-2075.1986.tb04450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Maruyama T., Gojobori T., Aota S., Ikemura T. Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res. 1986;14 (Suppl):r151–r197. doi: 10.1093/nar/14.suppl.r151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McGeoch D. J., Davison A. J. DNA sequence of the herpes simplex virus type 1 gene encoding glycoprotein gH, and identification of homologues in the genomes of varicella-zoster virus and Epstein-Barr virus. Nucleic Acids Res. 1986 May 27;14(10):4281–4292. doi: 10.1093/nar/14.10.4281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McGeoch D. J., Dolan A., Frame M. C. DNA sequence of the region in the genome of herpes simplex virus type 1 containing the exonuclease gene and neighbouring genes. Nucleic Acids Res. 1986 Apr 25;14(8):3435–3448. doi: 10.1093/nar/14.8.3435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McLachlan A. D. Tests for comparing related amino-acid sequences. Cytochrome c and cytochrome c 551 . J Mol Biol. 1971 Oct 28;61(2):409–424. doi: 10.1016/0022-2836(71)90390-1. [DOI] [PubMed] [Google Scholar]
  39. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  40. Morgan D. G. Observations on the antigenic relationships between Epstein-Barr virus and herpesvirus saimiri. J Gen Virol. 1977 Aug;36(2):281–287. doi: 10.1099/0022-1317-36-2-281. [DOI] [PubMed] [Google Scholar]
  41. Pellett P. E., Biggin M. D., Barrell B., Roizman B. Epstein-Barr virus genome may encode a protein showing significant amino acid and predicted secondary structure homology with glycoprotein B of herpes simplex virus 1. J Virol. 1985 Dec;56(3):807–813. doi: 10.1128/jvi.56.3.807-813.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pellett P. E., Jenkins F. J., Ackermann M., Sarmiento M., Roizman B. Transcription initiation sites and nucleotide sequence of a herpes simplex virus 1 gene conserved in the Epstein-Barr virus genome and reported to affect the transport of viral glycoproteins. J Virol. 1986 Dec;60(3):1134–1140. doi: 10.1128/jvi.60.3.1134-1140.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Quinn J. P., McGeoch D. J. DNA sequence of the region in the genome of herpes simplex virus type 1 containing the genes for DNA polymerase and the major DNA binding protein. Nucleic Acids Res. 1985 Nov 25;13(22):8143–8163. doi: 10.1093/nar/13.22.8143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Randall R. E., Honess R. W., O'Hare P. Proteins specified by herpesvirus saimiri: identification and properties of virus-specific polypeptides in productively infected cells. J Gen Virol. 1983 Jan;64(Pt 1):19–35. doi: 10.1099/0022-1317-64-1-19. [DOI] [PubMed] [Google Scholar]
  45. Randall R. E., Newman C., Honess R. W. A single major immediate-early virus gene product is synthesized in cells productively infected with herpesvirus saimiri. J Gen Virol. 1984 Jul;65(Pt 7):1215–1219. doi: 10.1099/0022-1317-65-7-1215. [DOI] [PubMed] [Google Scholar]
  46. Randall R. E., Newman C., Honess R. W. Asynchronous expression of the immediate-early protein of herpesvirus saimiri in populations of productively infected cells. J Gen Virol. 1985 Oct;66(Pt 10):2199–2213. doi: 10.1099/0022-1317-66-10-2199. [DOI] [PubMed] [Google Scholar]
  47. Randall R. E., Newman C., Honess R. W. Isolation and characterization of monoclonal antibodies to structural and nonstructural herpesvirus saimiri proteins. J Virol. 1984 Dec;52(3):872–883. doi: 10.1128/jvi.52.3.872-883.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Sawada I., Schmid C. W. Primate evolution of the alpha-globin gene cluster and its Alu-like repeats. J Mol Biol. 1986 Dec 20;192(4):693–709. doi: 10.1016/0022-2836(86)90022-7. [DOI] [PubMed] [Google Scholar]
  51. Staden R. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res. 1982 May 11;10(9):2951–2961. doi: 10.1093/nar/10.9.2951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. 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]
  53. Staden R. Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):521–538. doi: 10.1093/nar/12.1part2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Staden R., McLachlan A. D. Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res. 1982 Jan 11;10(1):141–156. doi: 10.1093/nar/10.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Staden R. Measurements of the effects that coding for a protein has on a DNA sequence and their use for finding genes. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):551–567. doi: 10.1093/nar/12.1part2.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Staden R. The current status and portability of our sequence handling software. Nucleic Acids Res. 1986 Jan 10;14(1):217–231. doi: 10.1093/nar/14.1.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Stamminger T., Honess R. W., Young D. F., Bodemer W., Blair E. D., Fleckenstein B. Organization of terminal reiterations in the virion DNA of herpesvirus saimiri. J Gen Virol. 1987 Apr;68(Pt 4):1049–1066. doi: 10.1099/0022-1317-68-4-1049. [DOI] [PubMed] [Google Scholar]
  58. Thompson R., Honess R. W., Taylor L., Morran J., Davison A. J. Varicella-zoster virus specifies a thymidylate synthetase. J Gen Virol. 1987 May;68(Pt 5):1449–1455. doi: 10.1099/0022-1317-68-5-1449. [DOI] [PubMed] [Google Scholar]
  59. Vogelstein B., Gillespie D. Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci U S A. 1979 Feb;76(2):615–619. doi: 10.1073/pnas.76.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Weston K., Barrell B. G. Sequence of the short unique region, short repeats, and part of the long repeats of human cytomegalovirus. J Mol Biol. 1986 Nov 20;192(2):177–208. doi: 10.1016/0022-2836(86)90359-1. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. 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]
  63. de Klein A., van Agthoven T., Groffen C., Heisterkamp N., Groffen J., Grosveld G. Molecular analysis of both translocation products of a Philadelphia-positive CML patient. Nucleic Acids Res. 1986 Sep 11;14(17):7071–7082. doi: 10.1093/nar/14.17.7071. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES