Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1988 Aug;8(8):2989–2998. doi: 10.1128/mcb.8.8.2989

Complete nucleotide sequence of a mouse VL30 retro-element.

S E Adams 1, P D Rathjen 1, C A Stanway 1, S M Fulton 1, M H Malim 1, W Wilson 1, J Ogden 1, L King 1, S M Kingsman 1, A J Kingsman 1
PMCID: PMC363524  PMID: 2850474

Abstract

The complete nucleotide sequence of a mouse retro-element is presented. The cloned element is composed of 4,834 base pairs (bp) with long terminal repeats of 568 bp separated by an internal region of 3,698 bp. The element did not appear to have any open reading frames that would be capable of encoding the functional proteins that are normally produced by retro-elements. However, some regions of the genome showed some homology to retroviral gag and pol open reading frames. There was no region in VL30 corresponding to a retroviral env gene. This implies that VL30 is related to retrotransposons rather than to retroviruses. The sequence also contained regions that were homologous to known reverse transcriptase priming sites and viral packaging sites. These observations, combined with the known transcriptional capacity of the VL30 promoter, suggest that VL30 relies on protein functions of other retro-elements, such as murine leukemia virus, while maintaining highly conserved cis-active promoter, packaging, and priming sites necessary for its replication and cell-to-cell transmission.

Full text

PDF
2989

Selected References

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

  1. Adams S. E., Kingsman S. M., Kingsman A. J. The yeast Ty element: recent advances in the study of a model retro-element. Bioessays. 1987 Jul;7(1):3–9. doi: 10.1002/bies.950070102. [DOI] [PubMed] [Google Scholar]
  2. Besmer P., Olshevsky U., Baltimore D., Dolberg D., Fan H. Virus-like 30S RNA in mouse cells. J Virol. 1979 Mar;29(3):1168–1176. doi: 10.1128/jvi.29.3.1168-1176.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brûlet P., Kaghad M., Xu Y. S., Croissant O., Jacob F. Early differential tissue expression of transposon-like repetitive DNA sequences of the mouse. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5641–5645. doi: 10.1073/pnas.80.18.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carter A. T., Norton J. D., Avery R. J. A novel approach to cloning transcriptionally active retrovirus-like genetic elements from mouse cells. Nucleic Acids Res. 1983 Sep 24;11(18):6243–6254. doi: 10.1093/nar/11.18.6243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chinault A. C., Carbon J. Overlap hybridization screening: isolation and characterization of overlapping DNA fragments surrounding the leu2 gene on yeast chromosome III. Gene. 1979 Feb;5(2):111–126. doi: 10.1016/0378-1119(79)90097-0. [DOI] [PubMed] [Google Scholar]
  6. Clare J., Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci U S A. 1985 May;82(9):2829–2833. doi: 10.1073/pnas.82.9.2829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clewley J. P., Avery R. J. The virion RNA species of the Kirsten murine sarcoma-leukemia virus complex released from a clonally related series of mouse cells. Arch Virol. 1982;72(1-2):35–46. doi: 10.1007/BF01314448. [DOI] [PubMed] [Google Scholar]
  8. Courtney M. G., Elder P. K., Steffen D. L., Getz M. J. Evidence for an early evolutionary origin and locus polymorphism of mouse VL30 DNA sequences. J Virol. 1982 Aug;43(2):511–518. doi: 10.1128/jvi.43.2.511-518.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devare S. G., Reddy E. P., Law J. D., Robbins K. C., Aaronson S. A. Nucleotide sequence of the simian sarcoma virus genome: demonstration that its acquired cellular sequences encode the transforming gene product p28sis. Proc Natl Acad Sci U S A. 1983 Feb;80(3):731–735. doi: 10.1073/pnas.80.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dragani T. A., Manenti G., Della Porta G., Gattoni-Celli S., Weinstein I. B. Expression of retroviral sequences and oncogenes in murine hepatocellular tumors. Cancer Res. 1986 Apr;46(4 Pt 2):1915–1919. [PubMed] [Google Scholar]
  11. Elder R. T., St John T. P., Stinchcomb D. T., Davis R. W., Scherer S., Davis R. W. Studies on the transposable element Ty1 of yeast. I. RNA homologous to Ty1. II. Recombination and expression of Ty1 and adjacent sequences. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):581–591. doi: 10.1101/sqb.1981.045.01.075. [DOI] [PubMed] [Google Scholar]
  12. Ellis R. W., DeFeo D., Maryak J. M., Young H. A., Shih T. Y., Chang E. H., Lowy D. R., Scolnick E. M. Dual evolutionary origin for the rat genetic sequences of Harvey murine sarcoma virus. J Virol. 1980 Nov;36(2):408–420. doi: 10.1128/jvi.36.2.408-420.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ellis R. W., Defeo D., Shih T. Y., Gonda M. A., Young H. A., Tsuchida N., Lowy D. R., Scolnick E. M. The p21 src genes of Harvey and Kirsten sarcoma viruses originate from divergent members of a family of normal vertebrate genes. Nature. 1981 Aug 6;292(5823):506–511. doi: 10.1038/292506a0. [DOI] [PubMed] [Google Scholar]
  14. Errede B., Cardillo T. S., Sherman F., Dubois E., Deschamps J., Wiame J. M. Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell. 1980 Nov;22(2 Pt 2):427–436. doi: 10.1016/0092-8674(80)90353-0. [DOI] [PubMed] [Google Scholar]
  15. Foster D. N., Schmidt L. J., Hodgson C. P., Moses H. L., Getz M. J. Polyadenylylated RNA complementary to a mouse retrovirus-like multigene family is rapidly and specifically induced by epidermal growth factor stimulation of quiescent cells. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7317–7321. doi: 10.1073/pnas.79.23.7317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fulton A. M., Adams S. E., Mellor J., Kingsman S. M., Kingsman A. J. The organization and expression of the yeast retrotransposon, Ty. Microbiol Sci. 1987 Jun;4(6):180–185. [PubMed] [Google Scholar]
  17. Giri C. P., Hodgson C. P., Elder P. K., Courtney M. G., Getz M. J. Discrete regions of sequence homology between cloned rodent VL30 genetic elements and AKV-related MuLV provirus genomes. Nucleic Acids Res. 1983 Jan 25;11(2):305–319. doi: 10.1093/nar/11.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hauber J., Nelböck-Hochstetter P., Feldmann H. Nucleotide sequence and characteristics of a Ty element from yeast. Nucleic Acids Res. 1985 Apr 25;13(8):2745–2758. doi: 10.1093/nar/13.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hodgson C. P., Elder P. K., Ono T., Foster D. N., Getz M. J. Structure and expression of mouse VL30 genes. Mol Cell Biol. 1983 Dec;3(12):2221–2231. doi: 10.1128/mcb.3.12.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Howk R. S., Troxler D. H., Lowy D., Duesberg P. H., Scolnick E. M. Identification of a 30S RNA with properties of a defective type C virus in murine cells. J Virol. 1978 Jan;25(1):115–123. doi: 10.1128/jvi.25.1.115-123.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Itin A., Keshet E. Diverse long terminal repeats are associated with murine retroviruslike (VL30) elements. Mol Cell Biol. 1986 Apr;6(4):1276–1282. doi: 10.1128/mcb.6.4.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kaghad M., Maillet L., Brûlet P. Retroviral characteristics of the long terminal repeat of murine E.Tn sequences. EMBO J. 1985 Nov;4(11):2911–2915. doi: 10.1002/j.1460-2075.1985.tb04022.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Keshet E., Itin A. Patterns of genomic distribution and sequence heterogeneity of a murine "retrovirus-like" multigene family. J Virol. 1982 Jul;43(1):50–58. doi: 10.1128/jvi.43.1.50-58.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Keshet E., Shaul Y., Kaminchik J., Aviv H. Heterogeneity of "virus-like" genes encoding retrovirus-associated 30S RNA and their organization within the mouse genome. Cell. 1980 Jun;20(2):431–439. doi: 10.1016/0092-8674(80)90629-7. [DOI] [PubMed] [Google Scholar]
  26. Maisel J., Bender W., Hu S., Duesberg P. H., Davidson N. Structure of 50 to 70S RNA from Moloney sarcoma viruses. J Virol. 1978 Jan;25(1):384–394. doi: 10.1128/jvi.25.1.384-394.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mellor J., Kingsman A. J., Kingsman S. M. Ty, an endogenous retrovirus of yeast? Yeast. 1986 Sep;2(3):145–152. doi: 10.1002/yea.320020302. [DOI] [PubMed] [Google Scholar]
  28. Mietz J. A., Grossman Z., Lueders K. K., Kuff E. L. Nucleotide sequence of a complete mouse intracisternal A-particle genome: relationship to known aspects of particle assembly and function. J Virol. 1987 Oct;61(10):3020–3029. doi: 10.1128/jvi.61.10.3020-3029.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mount S. M., Rubin G. M. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol. 1985 Jul;5(7):1630–1638. doi: 10.1128/mcb.5.7.1630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  31. Norton J. D., Connor J., Avery R. J. Unusual long terminal repeat sequence of a retrovirus transmissible mouse (VL 30) genetic element: identification of functional domains. Nucleic Acids Res. 1984 Apr 25;12(8):3445–3460. doi: 10.1093/nar/12.8.3445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ono M., Toh H., Miyata T., Awaya T. Nucleotide sequence of the Syrian hamster intracisternal A-particle gene: close evolutionary relationship of type A particle gene to types B and D oncovirus genes. J Virol. 1985 Aug;55(2):387–394. doi: 10.1128/jvi.55.2.387-394.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Parkhurst S. M., Corces V. G. Developmental expression of Drosophila melanogaster retrovirus-like transposable elements. EMBO J. 1987 Feb;6(2):419–424. doi: 10.1002/j.1460-2075.1987.tb04771.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pikó L., Hammons M. D., Taylor K. D. Amounts, synthesis, and some properties of intracisternal A particle-related RNA in early mouse embryos. Proc Natl Acad Sci U S A. 1984 Jan;81(2):488–492. doi: 10.1073/pnas.81.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rasheed S., Norman G. L., Heidecker G. Nucleotide sequence of the Rasheed rat sarcoma virus oncogene: new mutations. Science. 1983 Jul 8;221(4606):155–157. doi: 10.1126/science.6344220. [DOI] [PubMed] [Google Scholar]
  36. Rodland K. D., Jue S. F., Magun B. E. Regulation of VL30 gene expression by activators of protein kinase C. J Biol Chem. 1986 Apr 15;261(11):5029–5033. [PubMed] [Google Scholar]
  37. Roop D. R., Lowy D. R., Tambourin P. E., Strickland J., Harper J. R., Balaschak M., Spangler E. F., Yuspa S. H. An activated Harvey ras oncogene produces benign tumours on mouse epidermal tissue. 1986 Oct 30-Nov 5Nature. 323(6091):822–824. doi: 10.1038/323822a0. [DOI] [PubMed] [Google Scholar]
  38. Rotman G., Itin A., Keshet E. Promoter and enhancer activities of long terminal repeats associated with cellular retrovirus-like (VL30) elements. Nucleic Acids Res. 1986 Jan 24;14(2):645–658. doi: 10.1093/nar/14.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Scolnick E. M., Vass W. C., Howk R. S., Duesberg P. H. Defective retrovirus-like 30S RNA species of rat and mouse cells are infectious if packaged by type C helper virus. J Virol. 1979 Mar;29(3):964–972. doi: 10.1128/jvi.29.3.964-972.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sherwin S. A., Rapp U. R., Benveniste R. E., Sen A., Todaro G. J. Rescue of endogenous 30S retroviral sequences from mouse cells by baboon type C virus. J Virol. 1978 May;26(2):257–264. doi: 10.1128/jvi.26.2.257-264.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Singh K., Saragosti S., Botchan M. Isolation of cellular genes differentially expressed in mouse NIH 3T3 cells and a simian virus 40-transformed derivative: growth-specific expression of VL30 genes. Mol Cell Biol. 1985 Oct;5(10):2590–2598. doi: 10.1128/mcb.5.10.2590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. 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]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES