Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2001 Jun;158(2):701–713. doi: 10.1093/genetics/158.2.701

Characterization of the flamenco region of the Drosophila melanogaster genome.

V Robert 1, N Prud'homme 1, A Kim 1, A Bucheton 1, A Pélisson 1
PMCID: PMC1461675  PMID: 11404334

Abstract

The flamenco gene, located at 20A1-3 in the beta-heterochromatin of the Drosophila X chromosome, is a major regulator of the gypsy/mdg4 endogenous retrovirus. As a first step to characterize this gene, approximately 100 kb of genomic DNA flanking a P-element-induced mutation of flamenco was isolated. This DNA is located in a sequencing gap of the Celera Genomics project, i.e., one of those parts of the genome in which the "shotgun" sequence could not be assembled, probably because it contains long stretches of repetitive DNA, especially on the proximal side of the P insertion point. Deficiency mapping indicated that sequences required for the normal flamenco function are located >130 kb proximal to the insertion site. The distal part of the cloned DNA does, nevertheless, contain several unique sequences, including at least four different transcription units. Dip1, the closest one to the P-element insertion point, might be a good candidate for a gypsy regulator, since it putatively encodes a nuclear protein containing two double-stranded RNA-binding domains. However, transgenes containing dip1 genomic DNA were not able to rescue flamenco mutant flies. The possible nature of the missing flamenco sequences is discussed.

Full Text

The Full Text of this article is available as a PDF (493.9 KB).

Selected References

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

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Andrews J., Smith M., Merakovsky J., Coulson M., Hannan F., Kelly L. E. The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides. Genetics. 1996 Aug;143(4):1699–1711. doi: 10.1093/genetics/143.4.1699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benkirane M., Neuveut C., Chun R. F., Smith S. M., Samuel C. E., Gatignol A., Jeang K. T. Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR. EMBO J. 1997 Feb 3;16(3):611–624. doi: 10.1093/emboj/16.3.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Best S., Le Tissier P., Towers G., Stoye J. P. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature. 1996 Aug 29;382(6594):826–829. doi: 10.1038/382826a0. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Chalvet F., Teysset L., Terzian C., Prud'homme N., Santamaria P., Bucheton A., Pélisson A. Proviral amplification of the Gypsy endogenous retrovirus of Drosophila melanogaster involves env-independent invasion of the female germline. EMBO J. 1999 May 4;18(9):2659–2669. doi: 10.1093/emboj/18.9.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chong K. L., Feng L., Schappert K., Meurs E., Donahue T. F., Friesen J. D., Hovanessian A. G., Williams B. R. Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J. 1992 Apr;11(4):1553–1562. doi: 10.1002/j.1460-2075.1992.tb05200.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Desset S., Conte C., Dimitri P., Calco V., Dastugue B., Vaury C. Mobilization of two retroelements, ZAM and Idefix, in a novel unstable line of Drosophila melanogaster. Mol Biol Evol. 1999 Jan;16(1):54–66. doi: 10.1093/oxfordjournals.molbev.a026038. [DOI] [PubMed] [Google Scholar]
  10. Donzeau M., Winnacker E. L., Meisterernst M. Specific repression of Tax trans-activation by TAR RNA-binding protein TRBP. J Virol. 1997 Apr;71(4):2628–2635. doi: 10.1128/jvi.71.4.2628-2635.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dubois M. F., Galabru J., Lebon P., Safer B., Hovanessian A. G. Reduced activity of the interferon-induced double-stranded RNA-dependent protein kinase during a heat shock stress. J Biol Chem. 1989 Jul 25;264(21):12165–12171. [PubMed] [Google Scholar]
  12. Gatignol A., Buckler-White A., Berkhout B., Jeang K. T. Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR. Science. 1991 Mar 29;251(5001):1597–1600. doi: 10.1126/science.2011739. [DOI] [PubMed] [Google Scholar]
  13. Gibson T. J., Thompson J. D. Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases. Nucleic Acids Res. 1994 Jul 11;22(13):2552–2556. doi: 10.1093/nar/22.13.2552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hovanessian A. G. The double stranded RNA-activated protein kinase induced by interferon: dsRNA-PK. J Interferon Res. 1989 Dec;9(6):641–647. doi: 10.1089/jir.1989.9.641. [DOI] [PubMed] [Google Scholar]
  15. Kai K., Sato H., Odaka T. Relationship between the cellular resistance to Friend murine leukemia virus infection and the expression of murine leukemia virus-gp70-related glycoprotein on cell surface of BALB/c-Fv-4wr mice. Virology. 1986 Apr 30;150(2):509–512. doi: 10.1016/0042-6822(86)90315-6. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Lee K. J., Mukhopadhyay M., Pelka P., Campos A. R., Steller H. Autoregulation of the Drosophila disconnected gene in the developing visual system. Dev Biol. 1999 Oct 15;214(2):385–398. doi: 10.1006/dbio.1999.9420. [DOI] [PubMed] [Google Scholar]
  18. Marra M. A., Kucaba T. A., Dietrich N. L., Green E. D., Brownstein B., Wilson R. K., McDonald K. M., Hillier L. W., McPherson J. D., Waterston R. H. High throughput fingerprint analysis of large-insert clones. Genome Res. 1997 Nov;7(11):1072–1084. doi: 10.1101/gr.7.11.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miklos G. L., Yamamoto M. T., Davies J., Pirrotta V. Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the beta-heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2051–2055. doi: 10.1073/pnas.85.7.2051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mitchelson A., Simonelig M., Williams C., O'Hare K. Homology with Saccharomyces cerevisiae RNA14 suggests that phenotypic suppression in Drosophila melanogaster by suppressor of forked occurs at the level of RNA stability. Genes Dev. 1993 Feb;7(2):241–249. doi: 10.1101/gad.7.2.241. [DOI] [PubMed] [Google Scholar]
  21. Myers E. W., Sutton G. G., Delcher A. L., Dew I. M., Fasulo D. P., Flanigan M. J., Kravitz S. A., Mobarry C. M., Reinert K. H., Remington K. A. A whole-genome assembly of Drosophila. Science. 2000 Mar 24;287(5461):2196–2204. doi: 10.1126/science.287.5461.2196. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Pimpinelli S., Berloco M., Fanti L., Dimitri P., Bonaccorsi S., Marchetti E., Caizzi R., Caggese C., Gatti M. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3804–3808. doi: 10.1073/pnas.92.9.3804. [DOI] [PMC free article] [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. Rackwitz H. R., Zehetner G., Frischauf A. M., Lehrach H. Rapid restriction mapping of DNA cloned in lambda phage vectors. Gene. 1984 Oct;30(1-3):195–200. doi: 10.1016/0378-1119(84)90120-3. [DOI] [PubMed] [Google Scholar]
  28. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. St Johnston D., Brown N. H., Gall J. G., Jantsch M. A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10979–10983. doi: 10.1073/pnas.89.22.10979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Vaury C., Bucheton A., Pelisson A. The beta heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma. 1989 Sep;98(3):215–224. doi: 10.1007/BF00329686. [DOI] [PubMed] [Google Scholar]
  33. Wakimoto B. T., Hearn M. G. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics. 1990 May;125(1):141–154. doi: 10.1093/genetics/125.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wassarman D. A., Solomon N. M., Rubin G. M. The Drosophila melanogaster ribosomal S6 kinase II-encoding sequence. Gene. 1994 Jul 8;144(2):309–310. doi: 10.1016/0378-1119(94)90396-4. [DOI] [PubMed] [Google Scholar]
  35. Yamamoto M. T., Mitchelson A., Tudor M., O'Hare K., Davies J. A., Miklos G. L. Molecular and cytogenetic analysis of the heterochromatin-euchromatin junction region of the Drosophila melanogaster X chromosome using cloned DNA sequences. Genetics. 1990 Aug;125(4):821–832. doi: 10.1093/genetics/125.4.821. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES