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. 1987 Jul;61(7):2182–2191. doi: 10.1128/jvi.61.7.2182-2191.1987

Tissue-specific expression of human provirus ERV3 mRNA in human placenta: two of the three ERV3 mRNAs contain human cellular sequences.

N Kato, S Pfeifer-Ohlsson, M Kato, E Larsson, J Rydnert, R Ohlsson, M Cohen
PMCID: PMC254242  PMID: 2884330

Abstract

Three polyadenylated RNAs, 9, 7.3, and 3.5 kilobases long, of a human endogenous retrovirus, ERV3, are abundant in human placental chorion, representing about 0.03 to 0.05% of the total mRNA. We characterized the structure of these mRNAs by Northern blot and S1 nuclease mapping analyses. We found that all three RNAs were spliced mRNAs that lacked 5.9 kilobases of proviral sequence, including the gag gene and most of the pol gene. In contrast to the transcription pattern usual for other retroviruses, the transcription pattern of the ERV3 provirus did not include a genome-length mRNA. All three of the ERV3 mRNAs initiated transcription at the same point in the 5' long terminal repeat (LTR) and contained identical splice junctions in the provirus. The 3.5-kilobase RNA was a typical subgenomic proviral mRNA, with its polyadenylation site in the 3' LTR. The two larger ERV3 mRNAs, however, extended through the polyadenylation site in the 3' LTR and were spliced at a second position approximately 370 nucleotides downstream from the 3' LTR. This finding suggests that when the ERV3 retrovirus integrated at this genomic locus in an ancestor of humans, it integrated within or adjacent to a cellular gene.

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Selected References

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

  1. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernard O., Cory S., Gerondakis S., Webb E., Adams J. M. Sequence of the murine and human cellular myc oncogenes and two modes of myc transcription resulting from chromosome translocation in B lymphoid tumours. EMBO J. 1983;2(12):2375–2383. doi: 10.1002/j.1460-2075.1983.tb01749.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonner T. I., O'Connell C., Cohen M. Cloned endogenous retroviral sequences from human DNA. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4709–4713. doi: 10.1073/pnas.79.15.4709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Callahan R., Drohan W., Tronick S., Schlom J. Detection and cloning of human DNA sequences related to the mouse mammary tumor virus genome. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5503–5507. doi: 10.1073/pnas.79.18.5503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen M., Powers M., O'Connell C., Kato N. The nucleotide sequence of the env gene from the human provirus ERV3 and isolation and characterization of an ERV3-specific cDNA. Virology. 1985 Dec;147(2):449–458. doi: 10.1016/0042-6822(85)90147-3. [DOI] [PubMed] [Google Scholar]
  7. Conklin K. F., Coffin J. M., Robinson H. L., Groudine M., Eisenman R. Role of methylation in the induced and spontaneous expression of the avian endogenous virus ev-1: DNA structure and gene products. Mol Cell Biol. 1982 Jun;2(6):638–652. doi: 10.1128/mcb.2.6.638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deen K. C., Sweet R. W. Murine mammary tumor virus pol-related sequences in human DNA: characterization and sequence comparison with the complete murine mammary tumor virus pol gene. J Virol. 1986 Feb;57(2):422–432. doi: 10.1128/jvi.57.2.422-432.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Gattoni-Celli S., Kirsch K., Kalled S., Isselbacher K. J. Expression of type C-related endogenous retroviral sequences in human colon tumors and colon cancer cell lines. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6127–6131. doi: 10.1073/pnas.83.16.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goodwin R. G., Rottman F. M., Callaghan T., Kung H. J., Maroney P. A., Nilsen T. W. c-erbB activation in avian leukosis virus-induced erythroblastosis: multiple epidermal growth factor receptor mRNAs are generated by alternative RNA processing. Mol Cell Biol. 1986 Sep;6(9):3128–3133. doi: 10.1128/mcb.6.9.3128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  13. Maeda N. Nucleotide sequence of the haptoglobin and haptoglobin-related gene pair. The haptoglobin-related gene contains a retrovirus-like element. J Biol Chem. 1985 Jun 10;260(11):6698–6709. [PubMed] [Google Scholar]
  14. Mager D. L., Henthorn P. S. Identification of a retrovirus-like repetitive element in human DNA. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7510–7514. doi: 10.1073/pnas.81.23.7510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Martin M. A., Bryan T., Rasheed S., Khan A. S. Identification and cloning of endogenous retroviral sequences present in human DNA. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4892–4896. doi: 10.1073/pnas.78.8.4892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. May F. E., Westley B. R. Structure of a human retroviral sequence related to mouse mammary tumor virus. J Virol. 1986 Nov;60(2):743–749. doi: 10.1128/jvi.60.2.743-749.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Nilsen T. W., Maroney P. A., Goodwin R. G., Rottman F. M., Crittenden L. B., Raines M. A., Kung H. J. c-erbB activation in ALV-induced erythroblastosis: novel RNA processing and promoter insertion result in expression of an amino-truncated EGF receptor. Cell. 1985 Jul;41(3):719–726. doi: 10.1016/s0092-8674(85)80052-0. [DOI] [PubMed] [Google Scholar]
  20. O'Connell C. D., Cohen M. The long terminal repeat sequences of a novel human endogenous retrovirus. Science. 1984 Dec 7;226(4679):1204–1206. doi: 10.1126/science.6505687. [DOI] [PubMed] [Google Scholar]
  21. O'Connell C., O'Brien S., Nash W. G., Cohen M. ERV3, a full-length human endogenous provirus: chromosomal localization and evolutionary relationships. Virology. 1984 Oct 30;138(2):225–235. doi: 10.1016/0042-6822(84)90347-7. [DOI] [PubMed] [Google Scholar]
  22. Ono M. Molecular cloning and long terminal repeat sequences of human endogenous retrovirus genes related to types A and B retrovirus genes. J Virol. 1986 Jun;58(3):937–944. doi: 10.1128/jvi.58.3.937-944.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pfeifer-Ohlsson S., Goustin A. S., Rydnert J., Wahlström T., Bjersing L., Stehelin D., Ohlsson R. Spatial and temporal pattern of cellular myc oncogene expression in developing human placenta: implications for embryonic cell proliferation. Cell. 1984 Sep;38(2):585–596. doi: 10.1016/0092-8674(84)90513-0. [DOI] [PubMed] [Google Scholar]
  24. Quintrell N., Hughes S. H., Varmus H. E., Bishop J. M. Structure of viral DNA and RNA in mammalian cells infected with avian sarcoma virus. J Mol Biol. 1980 Nov 15;143(4):363–393. doi: 10.1016/0022-2836(80)90218-1. [DOI] [PubMed] [Google Scholar]
  25. Rabbitts T. H., Hamlyn P. H., Baer R. Altered nucleotide sequences of a translocated c-myc gene in Burkitt lymphoma. Nature. 1983 Dec 22;306(5945):760–765. doi: 10.1038/306760a0. [DOI] [PubMed] [Google Scholar]
  26. Rabson A. B., Hamagishi Y., Steele P. E., Tykocinski M., Martin M. A. Characterization of human endogenous retroviral envelope RNA transcripts. J Virol. 1985 Oct;56(1):176–182. doi: 10.1128/jvi.56.1.176-182.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rabson A. B., Steele P. E., Garon C. F., Martin M. A. mRNA transcripts related to full-length endogenous retroviral DNA in human cells. Nature. 1983 Dec 8;306(5943):604–607. doi: 10.1038/306604a0. [DOI] [PubMed] [Google Scholar]
  28. Seiki M., Hattori S., Hirayama Y., Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3618–3622. doi: 10.1073/pnas.80.12.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shen-Ong G. L., Morse H. C., 3rd, Potter M., Mushinski J. F. Two modes of c-myb activation in virus-induced mouse myeloid tumors. Mol Cell Biol. 1986 Feb;6(2):380–392. doi: 10.1128/mcb.6.2.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Watson D. K., Reddy E. P., Duesberg P. H., Papas T. S. Nucleotide sequence analysis of the chicken c-myc gene reveals homologous and unique coding regions by comparison with the transforming gene of avian myelocytomatosis virus MC29, delta gag-myc. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2146–2150. doi: 10.1073/pnas.80.8.2146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Winberg G., Hammarskjöld M. L. Isolation of DNA from agarose gels using DEAE-paper. Application to restriction site mapping of adenovirus type 16 DNA. Nucleic Acids Res. 1980 Jan 25;8(2):253–264. doi: 10.1093/nar/8.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]

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