Abstract
Gypsy is an infectious endogenous retrovirus of Drosophila melanogaster. The gypsy proviruses replicate very efficiently in the genome of the progeny of females homozygous for permissive alleles of the flamenco gene. This replicative transposition is correlated with derepression of gypsy expression, specifically in the somatic cells of the ovaries of the permissive mothers. The determinism of this amplification was studied further by making chimeric mothers containing different permissive/restrictive and somatic/germinal lineages. We show here that the derepression of active proviruses in the permissive soma is necessary and sufficient to induce proviral insertions in the progeny, even if the F1 flies derive from restrictive germ cells devoid of active proviruses. Therefore, gypsy endogenous multiplication results from the transfer of some gypsy-encoded genetic material from the soma towards the germen of the mother and its subsequent insertion into the chromosomes of the progeny. This transfer, however, is not likely to result from retroviral infection of the germline. Indeed, we also show here that the insertion of a tagged gypsy element, mutant for the env gene, occurs at high frequency, independently of the production of gypsy Env proteins by any transcomplementing helper. The possible role of the env gene for horizontal transfer to new hosts is discussed.
Full Text
The Full Text of this article is available as a PDF (275.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alberola T. M., Bori L., de Frutos R. Structural analysis of Drosophila subobscura gypsy elements (gypsyDs). Genetica. 1997;100(1-3):39–48. [PubMed] [Google Scholar]
- Bayev A. A., Jr, Lyubomirskaya N. V., Dzhumagaliev E. B., Ananiev E. V., Amiantova I. G., Ilyin Y. V. Structural organization of transposable element mdg4 from Drosophila melanogaster and a nucleotide sequence of its long terminal repeats. Nucleic Acids Res. 1984 Apr 25;12(8):3707–3723. doi: 10.1093/nar/12.8.3707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brookman J. J., Toosy A. T., Shashidhara L. S., White R. A. The 412 retrotransposon and the development of gonadal mesoderm in Drosophila. Development. 1992 Dec;116(4):1185–1192. doi: 10.1242/dev.116.4.1185. [DOI] [PubMed] [Google Scholar]
- Bucheton A. The relationship between the flamenco gene and gypsy in Drosophila: how to tame a retrovirus. Trends Genet. 1995 Sep;11(9):349–353. doi: 10.1016/s0168-9525(00)89105-2. [DOI] [PubMed] [Google Scholar]
- Busson D., Gans M., Komitopoulou K., Masson M. Genetic Analysis of Three Dominant Female-Sterile Mutations Located on the X Chromosome of DROSOPHILA MELANOGASTER. Genetics. 1983 Oct;105(2):309–325. doi: 10.1093/genetics/105.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chalvet F., Debec A., Marcaillou C., Rougeau C., Bucheton A. Morphological and molecular characterization of new Drosophila cell lines established from a strain permissive for gypsy transposition. In Vitro Cell Dev Biol Anim. 1998 Nov-Dec;34(10):799–804. doi: 10.1007/s11626-998-0034-9. [DOI] [PubMed] [Google Scholar]
- Domínguez A., Albornoz J. Rates of movement of transposable elements in Drosophila melanogaster. Mol Gen Genet. 1996 May 23;251(2):130–138. doi: 10.1007/BF02172910. [DOI] [PubMed] [Google Scholar]
- Gans M., Audit C., Masson M. Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics. 1975 Dec;81(4):683–704. doi: 10.1093/genetics/81.4.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gardner M. B., Kozak C. A., O'Brien S. J. The Lake Casitas wild mouse: evolving genetic resistance to retroviral disease. Trends Genet. 1991 Jan;7(1):22–27. doi: 10.1016/0168-9525(91)90017-k. [DOI] [PubMed] [Google Scholar]
- Giorgi F., Jacob J. Recent findings on oogenesis of Drosophila melanogaster. I. Ultrastructural observations on the developing ooplasm. J Embryol Exp Morphol. 1977 Apr;38:115–124. [PubMed] [Google Scholar]
- Godwin A. K., Miller P. D., Getts L. A., Jackson K., Sonoda G., Schray K. J., Testa J. R., Hamilton T. C. Retroviral-like sequences specifically expressed in the rat ovary detect genetic differences between normal and transformed rat ovarian surface epithelial cells. Endocrinology. 1995 Oct;136(10):4640–4649. doi: 10.1210/endo.136.10.7664684. [DOI] [PubMed] [Google Scholar]
- Harris J. R. Placental endogenous retrovirus (ERV): structural, functional, and evolutionary significance. Bioessays. 1998 Apr;20(4):307–316. doi: 10.1002/(SICI)1521-1878(199804)20:4<307::AID-BIES7>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]
- Heidmann O., Heidmann T. Retrotransposition of a mouse IAP sequence tagged with an indicator gene. Cell. 1991 Jan 11;64(1):159–170. doi: 10.1016/0092-8674(91)90217-m. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Laverty T. R., Lim J. K. Site-specific instability in Drosophila melanogaster: evidence for transposition of destabilizing element. Genetics. 1982 Jul-Aug;101(3-4):461–476. doi: 10.1093/genetics/101.3-4.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leblanc P., Desset S., Dastugue B., Vaury C. Invertebrate retroviruses: ZAM a new candidate in D.melanogaster. EMBO J. 1997 Dec 15;16(24):7521–7531. doi: 10.1093/emboj/16.24.7521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lock L. F., Keshet E., Gilbert D. J., Jenkins N. A., Copeland N. G. Studies of the mechanism of spontaneous germline ecotropic provirus acquisition in mice. EMBO J. 1988 Dec 20;7(13):4169–4177. doi: 10.1002/j.1460-2075.1988.tb03313.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyubomirskaya N. V., Arkhipova I. R., Ilyin Y. V., Kim A. I. Molecular analysis of the gypsy (mdg4) retrotransposon in two Drosophila melanogaster strains differing by genetic instability. Mol Gen Genet. 1990 Sep;223(2):305–309. doi: 10.1007/BF00265067. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Mizrokhi L. J., Mazo A. M. Cloning and analysis of the mobile element gypsy from D. virilis. Nucleic Acids Res. 1991 Feb 25;19(4):913–916. doi: 10.1093/nar/19.4.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Nuzhdin S. V., Mackay T. F. The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol. 1995 Jan;12(1):180–181. doi: 10.1093/oxfordjournals.molbev.a040188. [DOI] [PubMed] [Google Scholar]
- Perrimon N., Gans M. Clonal analysis of the tissue specificity of recessive female-sterile mutations of Drosophila melanogaster using a dominant female-sterile mutation Fs(1)K1237. Dev Biol. 1983 Dec;100(2):365–373. doi: 10.1016/0012-1606(83)90231-2. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Quint W., van der Putten H., Janssen F., Berns A. Mobility of endogenous ecotropic murine leukemia viral genomes within mouse chromosomal DNA and integration of a mink cell focus-forming virus-type recombinant provirus in the germ line. J Virol. 1982 Mar;41(3):901–908. doi: 10.1128/jvi.41.3.901-908.1982. [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]
- 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]
- Song S. U., Kurkulos M., Boeke J. D., Corces V. G. Infection of the germ line by retroviral particles produced in the follicle cells: a possible mechanism for the mobilization of the gypsy retroelement of Drosophila. Development. 1997 Jul;124(14):2789–2798. doi: 10.1242/dev.124.14.2789. [DOI] [PubMed] [Google Scholar]
- Sánchez L., Santamaria P. Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics. 1997 Sep;147(1):231–242. doi: 10.1093/genetics/147.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tanda S., Mullor J. L., Corces V. G. The Drosophila tom retrotransposon encodes an envelope protein. Mol Cell Biol. 1994 Aug;14(8):5392–5401. doi: 10.1128/mcb.14.8.5392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tchenio T., Heidmann T. Defective retroviruses can disperse in the human genome by intracellular transposition. J Virol. 1991 Apr;65(4):2113–2118. doi: 10.1128/jvi.65.4.2113-2118.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Temin H. M. Origin of retroviruses from cellular moveable genetic elements. Cell. 1980 Oct;21(3):599–600. doi: 10.1016/0092-8674(80)90420-1. [DOI] [PubMed] [Google Scholar]
- Teysset L., Burns J. C., Shike H., Sullivan B. L., Bucheton A., Terzian C. A Moloney murine leukemia virus-based retroviral vector pseudotyped by the insect retroviral gypsy envelope can infect Drosophila cells. J Virol. 1998 Jan;72(1):853–856. doi: 10.1128/jvi.72.1.853-856.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thummel C. S., Boulet A. M., Lipshitz H. D. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 1988 Dec 30;74(2):445–456. doi: 10.1016/0378-1119(88)90177-1. [DOI] [PubMed] [Google Scholar]
- Venables P. J., Brookes S. M., Griffiths D., Weiss R. A., Boyd M. T. Abundance of an endogenous retroviral envelope protein in placental trophoblasts suggests a biological function. Virology. 1995 Aug 20;211(2):589–592. doi: 10.1006/viro.1995.1442. [DOI] [PubMed] [Google Scholar]
- Villarreal L. P., Villareal L. P. On viruses, sex, and motherhood. J Virol. 1997 Feb;71(2):859–865. doi: 10.1128/jvi.71.2.859-865.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wieschaus E., Audit C., Masson M. A clonal analysis of the roles of somatic cells and germ line during oogenesis in Drosophila. Dev Biol. 1981 Nov;88(1):92–103. doi: 10.1016/0012-1606(81)90221-9. [DOI] [PubMed] [Google Scholar]
- de Parseval N., Heidmann T. Physiological knockout of the envelope gene of the single-copy ERV-3 human endogenous retrovirus in a fraction of the Caucasian population. J Virol. 1998 Apr;72(4):3442–3445. doi: 10.1128/jvi.72.4.3442-3445.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
