Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2004 Mar;166(3):1313–1321. doi: 10.1534/genetics.166.3.1313

Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene.

Emeline Sarot 1, Geneviève Payen-Groschêne 1, Alain Bucheton 1, Alain Pélisson 1
PMCID: PMC1470774  PMID: 15082550

Abstract

In Drosophila melanogaster, the endogenous retrovirus gypsy is repressed by the functional alleles (restrictive) of an as-yet-uncloned heterochromatic gene called flamenco. Using gypsy-lacZ transcriptional fusions, we show here that this repression takes place not only in the follicle cells of restrictive ovaries, as was previously observed, but also in restrictive larval female gonads. Analyses of the role of gypsy cis-regulatory sequences in the control of gypsy expression are also presented. They rule out the hypothesis that gypsy would contain a single binding region for a putative Flamenco repressor. Indeed, the ovarian expression of a chimeric yp3-lacZ construct was shown to become sensitive to the Flamenco regulation when any of three different 5'-UTR gypsy sequences (ranging from 59 to 647 nucleotides) was incorporated into the heterologous yp3-lacZ transcript. The piwi mutation, which is known to affect RNA-mediated homology-dependent transgene silencing, was also shown to impede the repression of gypsy in restrictive female gonads. Finally, a RNA-silencing model is also supported by the finding in ovaries of short RNAs (25-27 nucleotides long) homologous to sequences from within the gypsy 5'-UTR.

Full Text

The Full Text of this article is available as a PDF (351.4 KB).

Selected References

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

  1. Aravin A. A., Naumova N. M., Tulin A. V., Vagin V. V., Rozovsky Y. M., Gvozdev V. A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol. 2001 Jul 10;11(13):1017–1027. doi: 10.1016/s0960-9822(01)00299-8. [DOI] [PubMed] [Google Scholar]
  2. Arkhipova I. R., Ilyin Y. V. Control of transcription of Drosophila retrotransposons. Bioessays. 1992 Mar;14(3):161–168. doi: 10.1002/bies.950140305. [DOI] [PubMed] [Google Scholar]
  3. Carmell Michelle A., Xuan Zhenyu, Zhang Michael Q., Hannon Gregory J. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 2002 Nov 1;16(21):2733–2742. doi: 10.1101/gad.1026102. [DOI] [PubMed] [Google Scholar]
  4. Chaboissier M. C., Bucheton A., Finnegan D. J. Copy number control of a transposable element, the I factor, a LINE-like element in Drosophila. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11781–11785. doi: 10.1073/pnas.95.20.11781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cox D. N., Chao A., Baker J., Chang L., Qiao D., Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998 Dec 1;12(23):3715–3727. doi: 10.1101/gad.12.23.3715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeSousa Dorothy, Mukhopadhyay Mahua, Pelka Peter, Zhao Xiaoli, Dey Bijan K., Robert Valérie, Pélisson Alain, Bucheton Alain, Campos Ana Regina. A novel double-stranded RNA-binding protein, disco interacting protein 1 (DIP1), contributes to cell fate decisions during Drosophila development. J Biol Chem. 2003 Jun 26;278(39):38040–38050. doi: 10.1074/jbc.M303512200. [DOI] [PubMed] [Google Scholar]
  7. Desset Sophie, Meignin Carine, Dastugue Bernard, Vaury Chantal. COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics. 2003 Jun;164(2):501–509. doi: 10.1093/genetics/164.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Godt D., Laski F. A. Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric à brac. Development. 1995 Jan;121(1):173–187. doi: 10.1242/dev.121.1.173. [DOI] [PubMed] [Google Scholar]
  9. Hamilton A. J., Baulcombe D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science. 1999 Oct 29;286(5441):950–952. doi: 10.1126/science.286.5441.950. [DOI] [PubMed] [Google Scholar]
  10. Jensen S., Gassama M. P., Heidmann T. Taming of transposable elements by homology-dependent gene silencing. Nat Genet. 1999 Feb;21(2):209–212. doi: 10.1038/5997. [DOI] [PubMed] [Google Scholar]
  11. Jensen Silke, Gassama Marie-Pierre, Dramard Xavier, Heidmann Thierry. Regulation of I-transposon activity in Drosophila: evidence for cosuppression of nonhomologous transgenes and possible role of ancestral I-related pericentromeric elements. Genetics. 2002 Nov;162(3):1197–1209. doi: 10.1093/genetics/162.3.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kim A. I., Belyaeva E. S., Aslanian M. M. Autonomous transposition of gypsy mobile elements and genetic instability in Drosophila melanogaster. Mol Gen Genet. 1990 Nov;224(2):303–308. doi: 10.1007/BF00271566. [DOI] [PubMed] [Google Scholar]
  13. Kim A. I., Lyubomirskaya N. V., Belyaeva E. S., Shostack N. G., Ilyin Y. V. The introduction of a transpositionally active copy of retrotransposon GYPSY into the Stable Strain of Drosophila melanogaster causes genetic instability. Mol Gen Genet. 1994 Feb;242(4):472–477. doi: 10.1007/BF00281799. [DOI] [PubMed] [Google Scholar]
  14. Kim A., Terzian C., Santamaria P., Pélisson A., Purd'homme N., Bucheton A. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1285–1289. doi: 10.1073/pnas.91.4.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klemenz R., Weber U., Gehring W. J. The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res. 1987 May 26;15(10):3947–3959. doi: 10.1093/nar/15.10.3947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W. Initial sequencing and analysis of the human genome. Nature. 2001 Feb 15;409(6822):860–921. doi: 10.1038/35057062. [DOI] [PubMed] [Google Scholar]
  17. Lécher P., Bucheton A., Pélisson A. Expression of the Drosophila retrovirus gypsy as ultrastructurally detectable particles in the ovaries of flies carrying a permissive flamenco allele. J Gen Virol. 1997 Sep;78(Pt 9):2379–2388. doi: 10.1099/0022-1317-78-9-2379. [DOI] [PubMed] [Google Scholar]
  18. Malinsky S., Bucheton A., Busseau I. New insights on homology-dependent silencing of I factor activity by transgenes containing ORF1 in Drosophila melanogaster. Genetics. 2000 Nov;156(3):1147–1155. doi: 10.1093/genetics/156.3.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Mével-Ninio M., Mariol M. C., Gans M. Mobilization of the gypsy and copia retrotransposons in Drosophila melanogaster induces reversion of the ovo dominant female-sterile mutations: molecular analysis of revertant alleles. EMBO J. 1989 May;8(5):1549–1558. doi: 10.1002/j.1460-2075.1989.tb03539.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okamoto H., Hirochika H. Silencing of transposable elements in plants. Trends Plant Sci. 2001 Nov;6(11):527–534. doi: 10.1016/s1360-1385(01)02105-7. [DOI] [PubMed] [Google Scholar]
  22. Pal-Bhadra Manika, Bhadra Utpal, Birchler James A. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol Cell. 2002 Feb;9(2):315–327. doi: 10.1016/s1097-2765(02)00440-9. [DOI] [PubMed] [Google Scholar]
  23. Pasyukova E., Nuzhdin S., Li W., Flavell A. J. Germ line transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol Gen Genet. 1997 Jun;255(1):115–124. doi: 10.1007/s004380050479. [DOI] [PubMed] [Google Scholar]
  24. Prud'homme N., Gans M., Masson M., Terzian C., Bucheton A. Flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics. 1995 Feb;139(2):697–711. doi: 10.1093/genetics/139.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pélisson A., Song S. U., Prud'homme N., Smith P. A., Bucheton A., Corces V. G. Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 1994 Sep 15;13(18):4401–4411. doi: 10.1002/j.1460-2075.1994.tb06760.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pélisson A., Teysset L., Chalvet F., Kim A., Prud'homme N., Terzian C., Bucheton A. About the origin of retroviruses and the co-evolution of the gypsy retrovirus with the Drosophila flamenco host gene. Genetica. 1997;100(1-3):29–37. [PubMed] [Google Scholar]
  27. Robert V., Prud'homme N., Kim A., Bucheton A., Pélisson A. Characterization of the flamenco region of the Drosophila melanogaster genome. Genetics. 2001 Jun;158(2):701–713. doi: 10.1093/genetics/158.2.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robin Stéphanie, Chambeyron Séverine, Bucheton Alain, Busseau Isabelle. Gene silencing triggered by non-LTR retrotransposons in the female germline of Drosophila melanogaster. Genetics. 2003 Jun;164(2):521–531. doi: 10.1093/genetics/164.2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ronaldson E., Bownes M. Two independent cis-acting elements regulate the sex- and tissue-specific expression of yp3 in Drosophila melanogaster. Genet Res. 1995 Aug;66(1):9–17. doi: 10.1017/s0016672300034340. [DOI] [PubMed] [Google Scholar]
  30. Ronsseray Stéphane, Josse Thibaut, Boivin Antoine, Anxolabéhère Dominique. Telomeric transgenes and trans-silencing in Drosophila. Genetica. 2003 Mar;117(2-3):327–335. doi: 10.1023/a:1022929121828. [DOI] [PubMed] [Google Scholar]
  31. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  32. Song S. U., Gerasimova T., Kurkulos M., Boeke J. D., Corces V. G. An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev. 1994 Sep 1;8(17):2046–2057. doi: 10.1101/gad.8.17.2046. [DOI] [PubMed] [Google Scholar]
  33. Volpe Thomas A., Kidner Catherine, Hall Ira M., Teng Grace, Grewal Shiv I. S., Martienssen Robert A. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 2002 Aug 22;297(5588):1833–1837. doi: 10.1126/science.1074973. [DOI] [PubMed] [Google Scholar]
  34. Waterhouse P. M., Wang M. B., Lough T. Gene silencing as an adaptive defence against viruses. Nature. 2001 Jun 14;411(6839):834–842. doi: 10.1038/35081168. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES