Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1984 Apr;3(4):813–821. doi: 10.1002/j.1460-2075.1984.tb01890.x

The EB virus genome in Daudi Burkitt's lymphoma cells has a deletion similar to that observed in a non-transforming strain (P3HR-1) of the virus.

M D Jones, L Foster, T Sheedy, B E Griffin
PMCID: PMC557432  PMID: 6327290

Abstract

Epstein-Barr virus (EBV) DNA isolated from the frequently studied and unusual Burkitt's lymphoma cell line, Daudi, contains a 7.4-kb deletion, similar to (but larger than) that found in a non-transforming isolate of the virus, P3HR-1. A comparison of EBV sequence in Daudi cells with that from a comparable region in a wild-type, transforming strain of the virus (B95-8) indicates that at least two of the previously identified RNAs, a highly repetitive sequence, and other interesting coding or structural features should be absent in Daudi EBV DNA as a consequence of the deletion. The information removed by the deletion, as well as that which might be generated by juxtaposition of two regions of the genome that are not adjacent in most strains of the virus are discussed.

Full text

PDF
813

Images in this article

Selected References

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

  1. Adams A., Strander H., Cantell K. Sensitivity of the Epstein-Barr virus transformed human lymphoid cell lines to interferon. J Gen Virol. 1975 Aug;28(2):207–217. doi: 10.1099/0022-1317-28-2-207. [DOI] [PubMed] [Google Scholar]
  2. Arrand J. R., Rymo L., Walsh J. E., Björck E., Lindahl T., Griffin B. E. Molecular cloning of the complete Epstein-Barr virus genome as a set of overlapping restriction endonuclease fragments. Nucleic Acids Res. 1981 Jul 10;9(13):2999–3014. doi: 10.1093/nar/9.13.2999. [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. Bornkamm G. W., Delius H., Zimber U., Hudewentz J., Epstein M. A. Comparison of Epstein-Barr virus strains of different origin by analysis of the viral DNAs. J Virol. 1980 Sep;35(3):603–618. doi: 10.1128/jvi.35.3.603-618.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bornkamm G. W., Hudewentz J., Freese U. K., Zimber U. Deletion of the nontransforming Epstein-Barr virus strain P3HR-1 causes fusion of the large internal repeat to the DSL region. J Virol. 1982 Sep;43(3):952–968. doi: 10.1128/jvi.43.3.952-968.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cheung A., Kieff E. Long internal direct repeat in Epstein-Barr virus DNA. J Virol. 1982 Oct;44(1):286–294. doi: 10.1128/jvi.44.1.286-294.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Erikson J., Finan J., Nowell P. C., Croce C. M. Translocation of immunoglobulin VH genes in Burkitt lymphoma. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5611–5615. doi: 10.1073/pnas.79.18.5611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fischer D. K., Miller G., Gradoville L., Heston L., Westrate M. W., Maris W., Wright J., Brandsma J., Summers W. C. Genome of a mononucleosis Epstein-Barr virus contains DNA fragments previously regarded to be unique to Burkitt's lymphoma isolates. Cell. 1981 May;24(2):543–553. doi: 10.1016/0092-8674(81)90345-7. [DOI] [PubMed] [Google Scholar]
  9. Fresen K. O., Merkt B., Bornkamm G. W., Hausen H. Heterogeneity of Epstein-Barr virus originating from P3HR-1 cells. I. Studies on EBNA induction. Int J Cancer. 1977 Mar 15;19(3):317–323. doi: 10.1002/ijc.2910190306. [DOI] [PubMed] [Google Scholar]
  10. Gerber P., Ablashi D., Magrath I., Armstrong G., Andersen P., Trach L. Persistence of transforming and nontransforming Epstein-Barr virus in high passages of P3HR-1 cell lines. J Natl Cancer Inst. 1982 Sep;69(3):585–590. [PubMed] [Google Scholar]
  11. Gewert D. R., Shah S., Clemens M. J. Inhibition of cell division by interferons: Changes in the transport and intracellular metabolism of thymidine in human lymphoblastoid (Daudi) cells. Eur J Biochem. 1981 Jun 1;116(3):487–492. doi: 10.1111/j.1432-1033.1981.tb05362.x. [DOI] [PubMed] [Google Scholar]
  12. Given D., Kieff E. DNA of Epstein-Barr virus. IV. Linkage map of restriction enzyme fragments of the B95-8 and W91 strains of Epstein-Barr Virus. J Virol. 1978 Nov;28(2):524–542. doi: 10.1128/jvi.28.2.524-542.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Glaser R., Boyd A., Stoerker J., Holliday J. Functional mapping of the Epstein-Barr virus genome: identification of sites coding for the restricted early antigen, the diffuse early antigen, and the nuclear antigen. Virology. 1983 Aug;129(1):188–198. doi: 10.1016/0042-6822(83)90405-1. [DOI] [PubMed] [Google Scholar]
  14. Godson G. N., Ellis J., Svec P., Schlesinger D. H., Nussenzweig V. Identification and chemical synthesis of a tandemly repeated immunogenic region of Plasmodium knowlesi circumsporozoite protein. Nature. 1983 Sep 1;305(5929):29–33. doi: 10.1038/305029a0. [DOI] [PubMed] [Google Scholar]
  15. Griffin B. E., Björck E., Bjursell G., Lindahl T. Sequence complexity of circular Epstein-Bar virus DNA in transformed cells. J Virol. 1981 Oct;40(1):11–19. doi: 10.1128/jvi.40.1.11-19.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayward S. D., Lazarowitz S. G., Hayward G. S. Organization of the Epstein-Barr virus DNA molecule. II. Fine mapping of the boundaries of the internal repeat cluster of B95-8 and identification of additional small tandem repeats adjacent to the HR-1 deletion. J Virol. 1982 Jul;43(1):201–212. doi: 10.1128/jvi.43.1.201-212.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heller M., Dambaugh T., Kieff E. Epstein-Barr virus DNA. IX. Variation among viral DNAs from producer and nonproducer infected cells. J Virol. 1981 May;38(2):632–648. doi: 10.1128/jvi.38.2.632-648.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Henry B. E., 2nd, Raab-Traub N. J., Pagano J. S. Detection of autonomous replicating sequences (ars) in the genome of Epstein-Barr virus. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1096–1100. doi: 10.1073/pnas.80.4.1096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Heston L., Rabson M., Brown N., Miller G. New Epstein-Barr virus variants from cellular subclones of P3J-HR-1 Burkitt lymphoma. Nature. 1982 Jan 14;295(5845):160–163. doi: 10.1038/295160a0. [DOI] [PubMed] [Google Scholar]
  20. Hinuma Y., Konn M., Yamaguchi J., Wudarski D. J., Blakeslee J. R., Jr, Grace J. T., Jr Immunofluorescence and herpes-type virus particles in the P3HR-1 Burkitt lymphoma cell line. J Virol. 1967 Oct;1(5):1045–1051. doi: 10.1128/jvi.1.5.1045-1051.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hudewentz J., Delius H., Freese U. K., Zimber U., Bornkamm G. W. Two distant regions of the Epstein-Barr virus genome with sequence homologies have the same orientation and involve small tandem repeats. EMBO J. 1982;1(1):21–26. doi: 10.1002/j.1460-2075.1982.tb01118.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hummel M., Kieff E. Mapping of polypeptides encoded by the Epstein-Barr virus genome in productive infection. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5698–5702. doi: 10.1073/pnas.79.18.5698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jeang K. T., Hayward S. D. Organization of the Epstein-Barr virus DNA molecule. III. Location of the P3HR-1 deletion junction and characterization of the NotI repeat units that form part of the template for an abundant 12-O-tetradecanoylphorbol-13-acetate-induced mRNA transcript. J Virol. 1983 Oct;48(1):135–148. doi: 10.1128/jvi.48.1.135-148.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jones M. D., Griffin B. E. Clustered repeat sequences in the genome of Epstein Barr virus. Nucleic Acids Res. 1983 Jun 25;11(12):3919–3937. doi: 10.1093/nar/11.12.3919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. King W., Dambaugh T., Heller M., Dowling J., Kieff E. Epstein-Barr virus DNA XII. A variable region of the Epstein-Barr virus genome is included in the P3HR-1 deletion. J Virol. 1982 Sep;43(3):979–986. doi: 10.1128/jvi.43.3.979-986.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Klein E., Klein G., Nadkarni J. S., Nadkarni J. J., Wigzell H., Clifford P. Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res. 1968 Jul;28(7):1300–1310. [PubMed] [Google Scholar]
  27. Kozak M. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res. 1981 Oct 24;9(20):5233–5252. doi: 10.1093/nar/9.20.5233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lenoir G. M., Preud'homme J. L., Bernheim A., Berger R. Correlation between immunoglobulin light chain expression and variant translocation in Burkitt's lymphoma. Nature. 1982 Jul 29;298(5873):474–476. doi: 10.1038/298474a0. [DOI] [PubMed] [Google Scholar]
  29. Luka J., Kallin B., Klein G. Induction of the Epstein-Barr virus (EBV) cycle in latently infected cells by n-butyrate. Virology. 1979 Apr 15;94(1):228–231. doi: 10.1016/0042-6822(79)90455-0. [DOI] [PubMed] [Google Scholar]
  30. Manolov G., Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature. 1972 May 5;237(5349):33–34. doi: 10.1038/237033a0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Miller G., Robinson J., Heston L., Lipman M. Differences between laboratory strains of Epstein-Barr virus based on immortalization, abortive infection, and interference. Proc Natl Acad Sci U S A. 1974 Oct;71(10):4006–4010. doi: 10.1073/pnas.71.10.4006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pritchett R., Pendersen M., Kieff E. Complexity of EBV homologous DNA in continous lymphoblastoid cell lines. Virology. 1976 Oct 1;74(1):227–231. [PubMed] [Google Scholar]
  35. Raab-Traub N., Dambaugh T., Kieff E. DNA of Epstein-Barr virus VIII: B95-8, the previous prototype, is an unusual deletion derivative. Cell. 1980 Nov;22(1 Pt 1):257–267. doi: 10.1016/0092-8674(80)90173-7. [DOI] [PubMed] [Google Scholar]
  36. Rabson M., Gradoville L., Heston L., Miller G. Non-immortalizing P3J-HR-1 Epstein-Barr virus: a deletion mutant of its transforming parent, Jijoye. J Virol. 1982 Dec;44(3):834–844. doi: 10.1128/jvi.44.3.834-844.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  38. Rymo L., Forsblom S. Cleavage of Epstein-Barr virus DNA by restriction endonucleases EcoRI, HindIII and BamI. Nucleic Acids Res. 1978 Apr;5(4):1387–1402. doi: 10.1093/nar/5.4.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rymo L., Lindahl T., Adams A. Sites of sequence variability in Epstein-Barr virus DNA from different sources. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2794–2798. doi: 10.1073/pnas.76.6.2794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rymo L., Lindahl T., Povey S., Klein G. Analysis of restriction endonuclease fragments of intracellular Epstein-Barr virus DNA and isoenzymes indicate a common origin of the Raji, NC-37, and F-265 human lymphoid cell lines. Virology. 1981 Nov;115(1):115–124. doi: 10.1016/0042-6822(81)90093-3. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Silverman R. H., Watling D., Balkwill F. R., Trowsdale J., Kerr I. M. The ppp(A2'p)nA and protein kinase systems in wild-type and interferon-resistant Daudi cells. Eur J Biochem. 1982 Aug;126(2):333–341. doi: 10.1111/j.1432-1033.1982.tb06783.x. [DOI] [PubMed] [Google Scholar]
  43. Skare J., Strominger J. L. Cloning and mapping of BamHi endonuclease fragments of DNA from the transforming B95-8 strain of Epstein-Barr virus. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3860–3864. doi: 10.1073/pnas.77.7.3860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  45. Stoerker J., Holliday J. E., Glaser R. Identification of a region of the Epstein-Barr virus (B95-8) genome required for transformation. Virology. 1983 Aug;129(1):199–206. doi: 10.1016/0042-6822(83)90406-3. [DOI] [PubMed] [Google Scholar]
  46. Tovey M. G., Dron M., Gresser I. Interferon enhances the expression of epstein-Barr virus early antigen in Daudi cells. J Gen Virol. 1982 May;60(Pt 1):31–38. doi: 10.1099/0022-1317-60-1-31. [DOI] [PubMed] [Google Scholar]
  47. Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
  48. Weigel R., Miller G. Major EB virus-specific cytoplasmic transcripts in a cellular clone of the HR-1 Burkitt lymphoma line during latency and after induction of viral replicative cycle by phorbol esters. Virology. 1983 Mar;125(2):287–298. doi: 10.1016/0042-6822(83)90202-7. [DOI] [PubMed] [Google Scholar]
  49. Zech L., Haglund U., Nilsson K., Klein G. Characteristic chromosomal abnormalities in biopsies and lymphoid-cell lines from patients with Burkitt and non-Burkitt lymphomas. Int J Cancer. 1976 Jan 15;17(1):47–56. doi: 10.1002/ijc.2910170108. [DOI] [PubMed] [Google Scholar]
  50. van Santen V., Cheung A., Kieff E. Epstein-Barr virus RNA VII: size and direction of transcription of virus-specified cytoplasmic RNAs in a transformed cell line. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1930–1934. doi: 10.1073/pnas.78.3.1930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. zur Hausen H., Bornkamm G. W., Schmidt R., Hecker E. Tumor initiators and promoters in the induction of Epstein-Barr virus. Proc Natl Acad Sci U S A. 1979 Feb;76(2):782–785. doi: 10.1073/pnas.76.2.782. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES