1887

Abstract

The endogenous retrovirus is controlled by the gene (). New insertions of occur in any individual if its mother is homozygous for the permissive allele and contains functional proviruses. The ovaries of females also contain high amounts of RNAs. Unexpectedly however, derepression does not occur in the female germline proper but in the somatic follicular epithelium of the ovary. Since extracts from these females are able to efficiently infect the germ-line of a strain devoid of active proviruses, we assume that a similar kind of germ-line infection, which would occur inside the females themselves, could be required for insertions to occur in their progeny. This hypothesis was confirmed by electron microscopy observations showing that non-enve-loped intracytoplasmic particles containing RNAs accumulate in the apical region of the follicle cells, close to specific membrane domains to which the envelope proteins are targeted, whereas both are absent in the controls. Low amounts of similar virus-like particles were also observed in oocytes, but it is not yet known whether they entered passively or as a result of membrane fusion. This is the first report of the beginning of a retrovirus cycle in invertebrates and these observations should be taken into account when explaining the maternal effect of the gene on the multiplication of proviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-9-2379
1997-09-01
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/9/9292028.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-9-2379&mimeType=html&fmt=ahah

References

  1. Arkhipova I. R., Lyubomirskaya N. V., Ilyin Y. V. 1995 Drosophila retrotransposons Austin, Tex: R. G. Landes;
    [Google Scholar]
  2. Bautch V. L. 1986; Genetic background affects integration frequency of ecotropic proviral sequences into the mouse germ-line. Journal of Virology 60:693–701
    [Google Scholar]
  3. Bernhard W. 1960; The detection and study of tumor viruses with the electron microscope. Cancer Research 20:712–727
    [Google Scholar]
  4. Bucheton A. 1995; The relationship between the flamenco gene and gypsy in Drosophila: how to tame a retrovirus. Trends in Genetics 11:349–353
    [Google Scholar]
  5. Coffin J. M. 1990; Retroviridae and their replication. In Virology, 2nd edn. pp. 1437–1500 Fields B. N., Knipe D. M. Edited by New York: Raven Press;
    [Google Scholar]
  6. Escaig-Haye F., Grigoriev V., Sharova I., Rudneva V., Buckrinskaya A., Fournier J. G. 1992; Ultrastructural localization of HIV-1 RNA and core proteins. Simultaneous visualization using double immunogold labelling after in situ hybridization and immunocytochemistry. Journal of Submicroscopic Cytology and Pathology 24:437–443
    [Google Scholar]
  7. Fine D., Schochetman G. 1978; Type D primate retroviruses: a review. Cancer Research 38:3123–3139
    [Google Scholar]
  8. Gans M., Audit C., Masson M. 1975; Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics 81:683–704
    [Google Scholar]
  9. Kim A., Terzian C., Santamaria P., Pélisson A., Prud’homme N., Bucheton A. 1994; Retroviruses in invertebrates : gypsy is an infectious retrovirus of Drosophila. Proceedings of the National Academy of Sciences, USA 91:1285–1289
    [Google Scholar]
  10. King R. C. 1970 Ovarian Development in Drosophila melanogaster New York: Academic Press;
    [Google Scholar]
  11. Lasko P. F. 1994 Molecular Genetics of Drosophila Oogenesis Austin, Tex: R. G. Landes;
    [Google Scholar]
  12. Lécher P., Petit N., Berziat F., Alziari S. 1996; Localization by ultrastructural in situ hybridization of mitochondrial transcripts in epithelial cells of a Drosophila subobscura deletion mutant. European Journal of Cell Biology 71:423–427
    [Google Scholar]
  13. Lower R., Lower J., Kurth R. 1996; The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proceedings of the National Academy of Sciences, USA 93:5177–5184
    [Google Scholar]
  14. Mahowald A. P., Kambysellis M. P. 1980; Oogenesis. In The Genetics and Biology of Drosophila 2d pp. 141–224 Ashburner M., Wright T. R. F. Edited by London: Academic Press;
    [Google Scholar]
  15. Marlor R. L., Parkhurst S. M., Corces V. G. 1986; The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Molecular and Cell Biology 6:1129–1134
    [Google Scholar]
  16. Pélisson A., Song S. U., Prud’homme N., Smith P. A., Bucheton A., Corces V. G. 1994; Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO Journal 13:4401–4411
    [Google Scholar]
  17. Prud’homme N., Gans M., Masson M., Terzian C., Bucheton A. 1995; flamenco, a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139:697–711
    [Google Scholar]
  18. Puvion-Dutilleul F. 1995; Procedures of in situ nucleic acid hybridization to detect viral DNA and RNA in cells by electron microscopy. In Hybridization Techniques for Electron Microscopy pp. 270–297 Morel G. Edited by Boca Raton, Fla: CRC Press;
    [Google Scholar]
  19. Rhee S. S., Hunter E. 1987; Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. Journal of Virology 61:1045–1053
    [Google Scholar]
  20. Rhee S. S., Hunter E. 1990; A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell 63:77–86
    [Google Scholar]
  21. Song S. U., Gerasimova T., Kurkulos M., Boeke J. D., Corces V. G. 1994; An Env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes & Development 8:2046–2057
    [Google Scholar]
  22. Spence S. E., Gilbert D. J., Swing D. A., Copeland N. G., Jenkins N. A. 1989; Spontaneous germ-line virus infection and retroviral insertional mutagenesis in eighteen transgenic Srev lines of mice. Molecular and Cell Biology 9:177–184
    [Google Scholar]
  23. Spradling A. C. 1993; Developmental genetics of oogenesis. In The Development of Drosophila melanogaster pp. 1–70 Bates M., Martinez-Arias A. Edited by Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  24. Syomin B. V., Ilyin Y. V. 1994; Extracellular virus-like particles of the retrotransposon gypsy (Mdg4) as an infectivity factor. Doklady Biological Sciences 339:642–645
    [Google Scholar]
  25. Syomin B. V., Kandror K. V., Semakin A. B., Tsuprun V. L., Stepanov A. S. 1993; Presence ofthe gypsy (Mdg4) retrotransposon in extracellular virus-like particles. FEBS Letters 323:285–288
    [Google Scholar]
  26. Teninges D., Ohanessian A., Richard-Molard C., Contamine D. 1979; Contamination and persistent infection of Drosophila cell lines by reovirus type particles. In Vitro 15:425–428
    [Google Scholar]
  27. Tucker S. P., Compans R. W. 1993; Virus infection of polarized epithelial cells. Advances in Virus Research 42:187–247
    [Google Scholar]
  28. Varmus H., Brown P. 1989; Retroviruses. In Mobile DNA pp. 53–108 Berg D. E., Howe M. M. Edited by Washington, DC: American Society for Microbiology;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-78-9-2379
Loading
/content/journal/jgv/10.1099/0022-1317-78-9-2379
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error