Abstract
All retroviruses and retrotransposons studied to date regulate the relative levels of gag and pol/int gene products post-transcriptionally from a single mRNA. In these genetic elements the production of protein encoded by the pol and int genes is attenuated by a translational stop or frameshift in the reading frame preceding their coding regions in the mRNA. We show here that the Drosophila retrotransposon copia also produces lower amounts of gene products from its int/pol region than gag region but this is achieved by a mechanism which is novel for this class of genetic element. We show by the use of gene fusion constructs that the subgenomic 2 kilobase copia RNA, encoding gag products, is expressed as protein in cultured cells at least ten-fold more efficiently than the full genome length RNA, which additionally contains the pol and int open reading frames.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aebi M., Hornig H., Padgett R. A., Reiser J., Weissmann C. Sequence requirements for splicing of higher eukaryotic nuclear pre-mRNA. Cell. 1986 Nov 21;47(4):555–565. doi: 10.1016/0092-8674(86)90620-3. [DOI] [PubMed] [Google Scholar]
- Carlson M., Brutlag D. A gene adjacent to satellite DNA in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5898–5902. doi: 10.1073/pnas.75.12.5898. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clare J. J., Belcourt M., Farabaugh P. J. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6816–6820. doi: 10.1073/pnas.85.18.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cullen B. R., Greene W. C. Regulatory pathways governing HIV-1 replication. Cell. 1989 Aug 11;58(3):423–426. doi: 10.1016/0092-8674(89)90420-0. [DOI] [PubMed] [Google Scholar]
- Dayton A. I., Sodroski J. G., Rosen C. A., Goh W. C., Haseltine W. A. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell. 1986 Mar 28;44(6):941–947. doi: 10.1016/0092-8674(86)90017-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Finnegan D. J. Transposable elements in eukaryotes. Int Rev Cytol. 1985;93:281–326. doi: 10.1016/s0074-7696(08)61376-5. [DOI] [PubMed] [Google Scholar]
- Flavell A. J., Levis R., Simon M. A., Rubin G. M. The 5' termini of RNAs encoded by the transposable element copia. Nucleic Acids Res. 1981 Dec 11;9(23):6279–6291. doi: 10.1093/nar/9.23.6279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flavell A. J., Ruby S. W., Toole J. J., Roberts B. E., Rubin G. M. Translation and developmental regulation of RNA encoded by the eukaryotic transposable element copia. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7107–7111. doi: 10.1073/pnas.77.12.7107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grandbastien M. A., Spielmann A., Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989 Jan 26;337(6205):376–380. doi: 10.1038/337376a0. [DOI] [PubMed] [Google Scholar]
- Jacks T., Power M. D., Masiarz F. R., Luciw P. A., Barr P. J., Varmus H. E. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature. 1988 Jan 21;331(6153):280–283. doi: 10.1038/331280a0. [DOI] [PubMed] [Google Scholar]
- Jacks T., Varmus H. E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985 Dec 13;230(4731):1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
- 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]
- Mellor J., Fulton S. M., Dobson M. J., Wilson W., Kingsman S. M., Kingsman A. J. A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature. 1985 Jan 17;313(5999):243–246. doi: 10.1038/313243a0. [DOI] [PubMed] [Google Scholar]
- Miller K., Rosenbaum J., Zbrzezna V., Pogo A. O. The nucleotide sequence of Drosophila melanogaster copia-specific 2.1-kb mRNA. Nucleic Acids Res. 1989 Mar 11;17(5):2134–2134. doi: 10.1093/nar/17.5.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Schwartz H. E., Lockett T. J., Young M. W. Analysis of transcripts from two families of nomadic DNA. J Mol Biol. 1982 May 5;157(1):49–68. doi: 10.1016/0022-2836(82)90512-5. [DOI] [PubMed] [Google Scholar]
- Sneddon A., Flavell A. J. The transcriptional control regions of the copia retrotransposon. Nucleic Acids Res. 1989 Jun 12;17(11):4025–4035. doi: 10.1093/nar/17.11.4025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sondermeijer P. J., Derksen J. W., Lubsen N. H. New cell line: established cell lines of Drosophila hydei. In Vitro. 1980 Nov;16(11):913–914. doi: 10.1007/BF02619327. [DOI] [PubMed] [Google Scholar]
- Strebel K., Daugherty D., Clouse K., Cohen D., Folks T., Martin M. A. The HIV 'A' (sor) gene product is essential for virus infectivity. Nature. 1987 Aug 20;328(6132):728–730. doi: 10.1038/328728a0. [DOI] [PubMed] [Google Scholar]
- Terwilliger E., Burghoff R., Sia R., Sodroski J., Haseltine W., Rosen C. The art gene product of human immunodeficiency virus is required for replication. J Virol. 1988 Feb;62(2):655–658. doi: 10.1128/jvi.62.2.655-658.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Voytas D. F., Ausubel F. M. A copia-like transposable element family in Arabidopsis thaliana. Nature. 1988 Nov 17;336(6196):242–244. doi: 10.1038/336242a0. [DOI] [PubMed] [Google Scholar]
- Wieringa B., Hofer E., Weissmann C. A minimal intron length but no specific internal sequence is required for splicing the large rabbit beta-globin intron. Cell. 1984 Jul;37(3):915–925. doi: 10.1016/0092-8674(84)90426-4. [DOI] [PubMed] [Google Scholar]
- Wilson W., Malim M. H., Mellor J., Kingsman A. J., Kingsman S. M. Expression strategies of the yeast retrotransposon Ty: a short sequence directs ribosomal frameshifting. Nucleic Acids Res. 1986 Sep 11;14(17):7001–7016. doi: 10.1093/nar/14.17.7001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshinaka Y., Katoh I., Copeland T. D., Oroszlan S. Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1618–1622. doi: 10.1073/pnas.82.6.1618. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshinaka Y., Katoh I., Copeland T. D., Oroszlan S. Translational readthrough of an amber termination codon during synthesis of feline leukemia virus protease. J Virol. 1985 Sep;55(3):870–873. doi: 10.1128/jvi.55.3.870-873.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshioka K., Honma H., Zushi M., Kondo S., Togashi S., Miyake T., Shiba T. Virus-like particle formation of Drosophila copia through autocatalytic processing. EMBO J. 1990 Feb;9(2):535–541. doi: 10.1002/j.1460-2075.1990.tb08140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]