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. 1982 Oct;44(1):311–320. doi: 10.1128/jvi.44.1.311-320.1982

Simple repeat sequence in Epstein-Barr virus DNA is transcribed in latent and productive infections.

M Heller, V van Santen, E Kieff
PMCID: PMC256266  PMID: 6292493

Abstract

The BamHI K region of Epstein-Barr virus DNA is transcribed in latently infected cells from Burkitt tumors and in growth-transformed B-lymphocytes latently infected with Epstein-Barr virus. We determined the nucleotide sequence of a 1,153-base pair HinfI fragment in BamHI fragment K from the B95-8 Epstein-Barr virus isolate. The fragment contains a remarkable 708-base pair simple sequence repeat array, designated IR3, which is composed of only three nucleotide triplet elements: GGG, GCA, and GGA. The triplets are organized into three repeat units: GCAGGA, GCAGGAGGA, and GGGGCAGGA. Immediately 3' of IR3 are tandem nearly perfect direct repeats of two different 24-base pair sequences. IR3 is conserved at a colinear position in the DNAs of other Epstein-Barr virus isolates, and a homologous sequence maps at the same location in the genome of a genetically related baboon herpesvirus, herpesvirus papio. IR3 is transcribed from left to right in latently infected, growth-transformed IB4 cells. It encodes part of a 2.0-kilobase exon of the 3.7-kilobase cytoplasmic polyadenylated RNA previously detected in IB4 cells (van Santen et al., Proc. Natl. Acad. Sci. U.S.A. 78:1930-1934, 1981). IR3 also encodes parts of 2.4- and 1.0-kilobase RNAs in productively infected B95-8 cells.

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Selected References

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

  1. Bell G. I., Selby M. J., Rutter W. J. The highly polymorphic region near the human insulin gene is composed of simple tandemly repeating sequences. Nature. 1982 Jan 7;295(5844):31–35. doi: 10.1038/295031a0. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Lee F., Harrison T., Williams J., Sharp P. A. Pre-early adenovirus 5 gene product regulates synthesis of early viral messenger RNAs. Cell. 1979 Aug;17(4):935–944. doi: 10.1016/0092-8674(79)90333-7. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Cheung A., Kieff E. Epstein-Barr virus DNA. X. Direct repeat within the internal direct repeat of Epstein-Barr virus DNA. J Virol. 1981 Nov;40(2):501–507. doi: 10.1128/jvi.40.2.501-507.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Dambaugh T., Beisel C., Hummel M., King W., Fennewald S., Cheung A., Heller M., Raab-Traub N., Kieff E. Epstein-Barr virus (B95-8) DNA VII: molecular cloning and detailed mapping. Proc Natl Acad Sci U S A. 1980 May;77(5):2999–3003. doi: 10.1073/pnas.77.5.2999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  8. Dolyniuk M., Pritchett R., Kieff E. Proteins of Epstein-Barr virus. I. Analysis of the polypeptides of purified enveloped Epstein-Barr virus. J Virol. 1976 Mar;17(3):935–949. doi: 10.1128/jvi.17.3.935-949.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Emery H. S., Weiner A. M. An irregular satellite sequence is found at the termini of the linear extrachromosomal rDNA in Dictyostelium discoideum. Cell. 1981 Nov;26(3 Pt 1):411–419. doi: 10.1016/0092-8674(81)90210-5. [DOI] [PubMed] [Google Scholar]
  10. Falk L., Deinhardt F., Nonoyama M., Wolfe L. G., Bergholz C. Properties of a baboon lymphotropic herpesvirus related to Epstein-Barr virus. Int J Cancer. 1976 Dec 15;18(6):798–807. doi: 10.1002/ijc.2910180611. [DOI] [PubMed] [Google Scholar]
  11. Gerber P., Kalter S. S., Schidlovsky G., Peterson W. D., Jr, Daniel M. D. Biologic and antigenic characteristics of Epstein-Barr virus-related Herpesviruses of chimpanzees and baboons. Int J Cancer. 1977 Sep 15;20(3):448–459. doi: 10.1002/ijc.2910200318. [DOI] [PubMed] [Google Scholar]
  12. Gerber P., Pritchett R. F., Kieff E. D. Antigens and DNA of a chimpanzee agent related to Epstein-Barr virus. J Virol. 1976 Sep;19(3):1090–1099. doi: 10.1128/jvi.19.3.1090-1099.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hayashi K. A cloning vehicle suitable for strand separation. Gene. 1980 Oct;11(1-2):109–115. doi: 10.1016/0378-1119(80)90091-8. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Heller M., Gerber P., Kieff E. DNA of herpesvirus pan, a third member of the Epstein-Barr virus-Herpesvirus papio group. J Virol. 1982 Mar;41(3):931–939. doi: 10.1128/jvi.41.3.931-939.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heller M., Gerber P., Kieff E. Herpesvirus papio DNA is similar in organization to Epstein-Barr virus DNA. J Virol. 1981 Feb;37(2):698–709. doi: 10.1128/jvi.37.2.698-709.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heller M., Kieff E. Colinearity between the DNAs of Epstein-Barr virus and herpesvirus papio. J Virol. 1981 Feb;37(2):821–826. doi: 10.1128/jvi.37.2.821-826.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hummel M., Kieff E. Epstein-Barr virus RNA. VIII. Viral RNA in permissively infected B95-8 cells. J Virol. 1982 Jul;43(1):262–272. doi: 10.1128/jvi.43.1.262-272.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jelinek W. R., Toomey T. P., Leinwand L., Duncan C. H., Biro P. A., Choudary P. V., Weissman S. M., Rubin C. M., Houck C. M., Deininger P. L. Ubiquitous, interspersed repeated sequences in mammalian genomes. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1398–1402. doi: 10.1073/pnas.77.3.1398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. King W., Thomas-Powell A. L., Raab-Traub N., Hawke M., Kieff E. Epstein-Barr virus RNA. V. Viral RNA in a restringently infected, growth-transformed cell line. J Virol. 1980 Nov;36(2):506–518. doi: 10.1128/jvi.36.2.506-518.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. King W., Van Santen V., Kieff E. Epstein-Barr virus RNA. VI. Viral RNA in restringently and abortively infected Raji cells. J Virol. 1981 May;38(2):649–660. doi: 10.1128/jvi.38.2.649-660.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee Y. S., Nonoyama M., Rabin H. Collinear relationships of herpesvirus papio DNA to Epstein--Barr virus DNA. Virology. 1981 Apr 15;110(1):248–252. doi: 10.1016/0042-6822(81)90031-3. [DOI] [PubMed] [Google Scholar]
  24. Lizardi P. M. Genetic polymorphism of silk fibroin studied by two-dimensional translation pause fingerprints. Cell. 1979 Oct;18(2):581–589. doi: 10.1016/0092-8674(79)90074-6. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. McDonell M. W., Simon M. N., Studier F. W. Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol. 1977 Feb 15;110(1):119–146. doi: 10.1016/s0022-2836(77)80102-2. [DOI] [PubMed] [Google Scholar]
  27. Miesfeld R., Krystal M., Arnheim N. A member of a new repeated sequence family which is conserved throughout eucaryotic evolution is found between the human delta and beta globin genes. Nucleic Acids Res. 1981 Nov 25;9(22):5931–5947. doi: 10.1093/nar/9.22.5931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Miller G., Lipman M. Release of infectious Epstein-Barr virus by transformed marmoset leukocytes. Proc Natl Acad Sci U S A. 1973 Jan;70(1):190–194. doi: 10.1073/pnas.70.1.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mocarski E. S., Roizman B. Site-specific inversion sequence of the herpes simplex virus genome: domain and structural features. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7047–7051. doi: 10.1073/pnas.78.11.7047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nikaido T., Nakai S., Honjo T. Switch region of immunoglobulin Cmu gene is composed of simple tandem repetitive sequences. Nature. 1981 Aug 27;292(5826):845–848. doi: 10.1038/292845a0. [DOI] [PubMed] [Google Scholar]
  31. PULVERTAFT J. V. CYTOLOGY OF BURKITT'S TUMOUR (AFRICAN LYMPHOMA). Lancet. 1964 Feb 1;1(7327):238–240. doi: 10.1016/s0140-6736(64)92345-1. [DOI] [PubMed] [Google Scholar]
  32. Pizzo P. A., Magrath I. T., Chattopadhyay S. K., Biggar R. J., Gerber P. A new tumour-derived transforming strain of Epstein-Barr virus. Nature. 1978 Apr 13;272(5654):629–631. doi: 10.1038/272629a0. [DOI] [PubMed] [Google Scholar]
  33. Powell A. L., King W., Kieff E. Epstein-Barr virus-specific RNA. III. Mapping of DNA encoding viral RNA in restringent infection. J Virol. 1979 Jan;29(1):261–274. doi: 10.1128/jvi.29.1.261-274.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [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. Reedman B. M., Klein G. Cellular localization of an Epstein-Barr virus (EBV)-associated complement-fixing antigen in producer and non-producer lymphoblastoid cell lines. Int J Cancer. 1973 May;11(3):499–520. doi: 10.1002/ijc.2910110302. [DOI] [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. Sharp P. A. Speculations on RNA splicing. Cell. 1981 Mar;23(3):643–646. doi: 10.1016/0092-8674(81)90425-6. [DOI] [PubMed] [Google Scholar]
  39. Slightom J. L., Blechl A. E., Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. doi: 10.1016/0092-8674(80)90426-2. [DOI] [PubMed] [Google Scholar]
  40. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  41. Smith H. O., Birnstiel M. L. A simple method for DNA restriction site mapping. Nucleic Acids Res. 1976 Sep;3(9):2387–2398. doi: 10.1093/nar/3.9.2387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sprague K. U., Roth M. B., Manning R. F., Gage L. P. Alleles of the fibroin gene coding for proteins of different lengths. Cell. 1979 Jun;17(2):407–413. doi: 10.1016/0092-8674(79)90167-3. [DOI] [PubMed] [Google Scholar]
  43. Strnad B. C., Schuster T. C., Hopkins R. F., 3rd, Neubauer R. H., Rabin H. Identification of an Epstein-Barr virus nuclear antigen by fluoroimmunoelectrophoresis and radioimmunoelectrophoresis. J Virol. 1981 Jun;38(3):996–1004. doi: 10.1128/jvi.38.3.996-1004.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sures I., Lowry J., Kedes L. H. The DNA sequence of sea urchin (S. purpuratus) H2A, H2B and H3 histone coding and spacer regions. Cell. 1978 Nov;15(3):1033–1044. doi: 10.1016/0092-8674(78)90287-8. [DOI] [PubMed] [Google Scholar]
  45. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]

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