Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1990 Jun;10(6):3067–3077. doi: 10.1128/mcb.10.6.3067

Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome.

P D Friesen 1, M S Nissen 1
PMCID: PMC360671  PMID: 1692964

Abstract

A single copy of the retrotransposon TED, from the moth Trichoplusia ni (a lepidopteran noctuid), was identified within the DNA genome of the baculovirus Autographa californica nuclear polyhedrosis virus. Determination of the complete nucleotide sequence (7,510 base pairs) of the integrated copy indicated that TED belongs to the family of retrotransposons that includes Drosophila melanogaster elements 17.6 and gypsy and thus represents the first nondipteran member of this invertebrate group to be identified. The internal portion of TED, flanked by long terminal repeats (LTRs), is composed of three long open reading frames comparable in size and location to the gag, pol, and env genes of the vertebrate retroviruses. Sequence similarity with the dipteran elements was the highest within individual domains of TED open reading frame 2 (pol region) that are also conserved among the retroviruses and encode protease, reverse transcriptase, and integrase functions, respectively. Mapping the 5' and 3' termini of TED RNAs indicated that the LTRs have a retroviral U3-R-U5 structural organization that is capable of directing the synthesis of transcripts that represent potential substrates for reverse transcription and intermediates in transposition. Abundant RNAs were also initiated from a site within the 5' LTR that matches the consensus motif for the promoter of late, hyperexpressed baculovirus genes. The presence of this viruslike promoter within TED and its subsequent activation only after integration within the viral genome suggest a possible symbiotic relationship with the baculovirus that could extend transposon host range.

Full text

PDF
3067

Images in this article

3072Image
on p.3072
3072Image
on p.3072
3073Image
on p.3073
3073Image
on p.3073
3074Image
on p.3074

Selected References

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

  1. Adams S. E., Mellor J., Gull K., Sim R. B., Tuite M. F., Kingsman S. M., Kingsman A. J. The functions and relationships of Ty-VLP proteins in yeast reflect those of mammalian retroviral proteins. Cell. 1987 Apr 10;49(1):111–119. doi: 10.1016/0092-8674(87)90761-6. [DOI] [PubMed] [Google Scholar]
  2. Arkhipova I. R., Mazo A. M., Cherkasova V. A., Gorelova T. V., Schuppe N. G., Llyin Y. V. The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell. 1986 Feb 28;44(4):555–563. doi: 10.1016/0092-8674(86)90265-5. [DOI] [PubMed] [Google Scholar]
  3. Beames B., Summers M. D. Comparisons of host cell DNA insertions and altered transcription at the site of insertions in few polyhedra bacilovirus mutants. Virology. 1988 Jan;162(1):206–220. doi: 10.1016/0042-6822(88)90410-2. [DOI] [PubMed] [Google Scholar]
  4. Boeke J. D., Corces V. G. Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol. 1989;43:403–434. doi: 10.1146/annurev.mi.43.100189.002155. [DOI] [PubMed] [Google Scholar]
  5. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  6. Carstens E. B. Identification and nucleotide sequence of the regions of Autographa californica nuclear polyhedrosis virus genome carrying insertion elements derived from Spodoptera frugiperda. Virology. 1987 Nov;161(1):8–17. doi: 10.1016/0042-6822(87)90165-6. [DOI] [PubMed] [Google Scholar]
  7. Cary L. C., Goebel M., Corsaro B. G., Wang H. G., Rosen E., Fraser M. J. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology. 1989 Sep;172(1):156–169. doi: 10.1016/0042-6822(89)90117-7. [DOI] [PubMed] [Google Scholar]
  8. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Copeland T. D., Oroszlan S., Kalyanaraman V. S., Sarngadharan M. G., Gallo R. C. Complete amino acid sequence of human T-cell leukemia virus structural protein p15. FEBS Lett. 1983 Oct 17;162(2):390–395. doi: 10.1016/0014-5793(83)80793-5. [DOI] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Donehower L. A., Varmus H. E. A mutant murine leukemia virus with a single missense codon in pol is defective in a function affecting integration. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6461–6465. doi: 10.1073/pnas.81.20.6461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Emori Y., Shiba T., Kanaya S., Inouye S., Yuki S., Saigo K. The nucleotide sequences of copia and copia-related RNA in Drosophila virus-like particles. 1985 Jun 27-Jul 3Nature. 315(6022):773–776. doi: 10.1038/315773a0. [DOI] [PubMed] [Google Scholar]
  14. Faulkner P., Carstens E. B. An overview of the structure and replication of baculoviruses. Curr Top Microbiol Immunol. 1986;131:1–19. doi: 10.1007/978-3-642-71589-1_1. [DOI] [PubMed] [Google Scholar]
  15. Friesen P. D., Miller L. K. Divergent transcription of early 35- and 94-kilodalton protein genes encoded by the HindIII K genome fragment of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol. 1987 Jul;61(7):2264–2272. doi: 10.1128/jvi.61.7.2264-2272.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Friesen P. D., Rice W. C., Miller D. W., Miller L. K. Bidirectional transcription from a solo long terminal repeat of the retrotransposon TED: symmetrical RNA start sites. Mol Cell Biol. 1986 May;6(5):1599–1607. doi: 10.1128/mcb.6.5.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hansen L. J., Chalker D. L., Sandmeyer S. B. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol. 1988 Dec;8(12):5245–5256. doi: 10.1128/mcb.8.12.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  19. Hink W. F. Established insect cell line from the cabbage looper, Trichoplusia ni. Nature. 1970 May 2;226(5244):466–467. doi: 10.1038/226466b0. [DOI] [PubMed] [Google Scholar]
  20. Hruby D. E., Roberts W. K. Encephalomyocarditis virus RNA: variations in polyadenylic acid content and biological activity. J Virol. 1976 Aug;19(2):325–330. doi: 10.1128/jvi.19.2.325-330.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Inouye S., Yuki S., Saigo K. Complete nucleotide sequence and genome organization of a Drosophila transposable genetic element, 297. Eur J Biochem. 1986 Jan 15;154(2):417–425. doi: 10.1111/j.1432-1033.1986.tb09414.x. [DOI] [PubMed] [Google Scholar]
  22. Johnson M. S., McClure M. A., Feng D. F., Gray J., Doolittle R. F. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7648–7652. doi: 10.1073/pnas.83.20.7648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Katoh I., Yasunaga T., Ikawa Y., Yoshinaka Y. Inhibition of retroviral protease activity by an aspartyl proteinase inhibitor. Nature. 1987 Oct 15;329(6140):654–656. doi: 10.1038/329654a0. [DOI] [PubMed] [Google Scholar]
  24. Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McClure M. A., Johnson M. S., Feng D. F., Doolittle R. F. Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2469–2473. doi: 10.1073/pnas.85.8.2469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miller D. W., Miller L. K. A virus mutant with an insertion of a copia-like transposable element. Nature. 1982 Oct 7;299(5883):562–564. doi: 10.1038/299562a0. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Nissen M. S., Friesen P. D. Molecular analysis of the transcriptional regulatory region of an early baculovirus gene. J Virol. 1989 Feb;63(2):493–503. doi: 10.1128/jvi.63.2.493-503.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Panganiban A. T., Temin H. M. The retrovirus pol gene encodes a product required for DNA integration: identification of a retrovirus int locus. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7885–7889. doi: 10.1073/pnas.81.24.7885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Parkhurst S. M., Corces V. G. Forked, gypsys, and suppressors in Drosophila. Cell. 1985 Jun;41(2):429–437. doi: 10.1016/s0092-8674(85)80016-7. [DOI] [PubMed] [Google Scholar]
  32. Possee R. D., Howard S. C. Analysis of the polyhedrin gene promoter of the Autographa californica nuclear polyhedrosis virus. Nucleic Acids Res. 1987 Dec 23;15(24):10233–10248. doi: 10.1093/nar/15.24.10233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rankin C., Ooi B. G., Miller L. K. Eight base pairs encompassing the transcriptional start point are the major determinant for baculovirus polyhedrin gene expression. Gene. 1988 Oct 15;70(1):39–49. doi: 10.1016/0378-1119(88)90102-3. [DOI] [PubMed] [Google Scholar]
  34. Rohrmann G. F. Polyhedrin structure. J Gen Virol. 1986 Aug;67(Pt 8):1499–1513. doi: 10.1099/0022-1317-67-8-1499. [DOI] [PubMed] [Google Scholar]
  35. Saigo K., Kugimiya W., Matsuo Y., Inouye S., Yoshioka K., Yuki S. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature. 1984 Dec 13;312(5995):659–661. doi: 10.1038/312659a0. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Toh H., Kikuno R., Hayashida H., Miyata T., Kugimiya W., Inouye S., Yuki S., Saigo K. Close structural resemblance between putative polymerase of a Drosophila transposable genetic element 17.6 and pol gene product of Moloney murine leukaemia virus. EMBO J. 1985 May;4(5):1267–1272. doi: 10.1002/j.1460-2075.1985.tb03771.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vaughn J. L., Goodwin R. H., Tompkins G. J., McCawley P. The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). In Vitro. 1977 Apr;13(4):213–217. doi: 10.1007/BF02615077. [DOI] [PubMed] [Google Scholar]
  42. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Youngren S. D., Boeke J. D., Sanders N. J., Garfinkel D. J. Functional organization of the retrotransposon Ty from Saccharomyces cerevisiae: Ty protease is required for transposition. Mol Cell Biol. 1988 Apr;8(4):1421–1431. doi: 10.1128/mcb.8.4.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES