Skip to main content
Log in

Two retrotransposons maintain telomeres in Drosophila

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Telomeres across the genus Drosophila are maintained, not by telomerase, but by two non-LTR retrotransposons, HeT-A and TART, that transpose specifically to chromosome ends. Successive transpositions result in long head-to-tail arrays of these elements. Thus Drosophila telomeres, like those produced by telomerase, consist of repeated sequences reverse transcribed from RNA templates. The Drosophila repeats, complete and 5′-truncated copies of HeT-A and TART, are more complex than telomerase repeats; nevertheless, these evolutionary variants have functional similarities to the more common telomeres. Like other telomeres, the Drosophila arrays are dynamic, fluctuating around an average length that can be changed by changes in the genetic background. Several proteins that interact with telomeres in other species have been found to have homologues that interact with Drosophila telomeres. Although they have hallmarks of non-LTR retrotransposons, HeT-A and TART appear to have a special relationship to Drosophila. Their Gag proteins are efficiently transported into diploid nuclei where HeT-A Gag recruits TART Gag to chromosome ends. Gags of other non-LTR elements remain predominantly in the cytoplasm. These studies provide intriguing evolutionary links between telomeres and retrotransposable elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abad JP, De Pablos B, Osoegawa K, De Jong PJ, Martin-Gallardo A, Villasante A (2004a) Genomic analysis of Drosophila melanogaster telomeres: full-length copies of HeT-A and TART elements at telomeres. Mol Biol Evol 21: 1613–1619.

    Article  PubMed  Google Scholar 

  • Abad JP, De Pablos B, Osoegawa K, De Jong PJ, Martin-Gallardo A, Villasante A (2004b) TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol Biol Evol 21: 1620–1624.

    Article  PubMed  Google Scholar 

  • Askree SH, Yehuda T, Smolikov S et al. (2004) A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci USA 101: 8658–8663.

    Article  PubMed  Google Scholar 

  • Beverley SM, Wilson AC (1984) Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. JMol Evol 21: 1–13.

    PubMed  Google Scholar 

  • Blackburn EH (1992) Telomerases. Annu Rev Biochem 61: 113–129.

    Article  PubMed  Google Scholar 

  • Blackburn EH (2001) Switching and signaling at the telomere. Cell 106: 661–673.

    Article  PubMed  Google Scholar 

  • Blasco MA (2002) Telomerase beyond telomeres. Nat Rev, Cancer 2: 627–633.

    Google Scholar 

  • Casacuberta E, Pardue M-L (2003a) Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc Natl Acad Sci USA 100: 3363–3368.

    Article  PubMed  Google Scholar 

  • Casacuberta E, Pardue M-L (2003b) HeT-A elements in D. virilis: retrotransposon telomeres are conserved across the Drosophila genus. Proc Natl Acac Sci USA 100: 14091–14096.

    Article  Google Scholar 

  • Casacuberta E, Pardue M-L (2005) HeT-A and TART, two Drosophila retrotransposons with a bona fide role in chromosome structure for more than 60 million years. Cytogenet Genome Res (special issue “Retransposable elements and genome evolution”) (in press).

  • Cenci G, Siriaco G, Raffa GD, Kellum R, Gatti MM (2003) The Drosophila HOAP protein is required for telomere capping. Nat Cell Biol 5: 82–84.

    Article  PubMed  Google Scholar 

  • Collins K (2000) Mammalian telomeres and telomerase. Curr Opin Cell Biol 12: 378–383.

    Article  PubMed  Google Scholar 

  • Fanti L, Giovinazzo G, Berloco M, Pimpinelli S (1998) The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 2: 527–538.

    Article  PubMed  Google Scholar 

  • George JA, Pardue M-L (2003) The promoter of the heterochromatic Drosophila telomeric retrotransposon, HeT-A, is active when moved into euchromatic locations. Genetics 163: 625–635.

    PubMed  Google Scholar 

  • Greider CW (1996) Telomere length regulation. Annu Rev Biochem 65: 337–365.

    Article  PubMed  Google Scholar 

  • Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51: 887–898.

    Article  PubMed  Google Scholar 

  • Griffith JD, Comeau L, Rosenfield S et al. (1999) Mammalian telomeres end in a large duplex loop. Cell 97: 503–514.

    Article  PubMed  Google Scholar 

  • Henson JD, Neumann AA, Yeager TR, Reddel RR (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene 21: 598–610.

    Article  PubMed  Google Scholar 

  • Jacks T (1990) Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Microbiol Immunol 157: 93–124.

    PubMed  Google Scholar 

  • Kahn T, Savitsky M, Georgiev P (2000) Attachment of HeT-A sequences to chromosomal termini in Drosophila melanogaster may occur by different mechanisms. Mol Cell Biol 20: 7634–7642.

    Article  PubMed  Google Scholar 

  • Karlseder J, Smogorzewska A, de Lange T (2002) Senescence induced by altered telomere state, not telomere loss. Science 295: 2446–2449.

    Article  PubMed  Google Scholar 

  • Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595–605.

    Article  PubMed  Google Scholar 

  • Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est1 senescence. Cell 73: 347–360.

    Article  PubMed  Google Scholar 

  • McClintock B (1978) Mechanisms that rapidly reorganize the genome. Stadler Genet Symp 10: 25–47.

    Google Scholar 

  • Melnikova L, Georgiev P (2002) Enhancer of terminal gene conversion,a new mutation in D. melanogaster that induces telomere elongation by gene conversion. Genetics 162: 1301–1312.

    PubMed  Google Scholar 

  • Melnikova L, Biessmann H, Georgiev P (2005) The ku protein complex is involved in length regulation of Drosophila telomeres. Genetics 169: 034538.

    Google Scholar 

  • Mikhailovsky S, Belenkaya T, Georgiev P (1999) Broken chromosome ends can be elongated by conversion in Drosophila melanogaster. Chromosoma 108: 114–120.

    Article  PubMed  Google Scholar 

  • Okazaki S, Tsuchida K, Maekawa H, Ishikawa H, Fijiwara H (1993) Identification of a pentanucleotide telomeric sequence (TTAGGG)n in the silkworm, Bombyx mori, and other insects. Mol Cell Biol 13: 1424–1432.

    PubMed  Google Scholar 

  • Pardue M-L, DeBaryshe PG (2003) Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu Rev Genet 37: 485–511.

    Article  PubMed  Google Scholar 

  • Pardue M-L, Danilevskaya ON, Lowenhaupt K, Slot F, Traverse KL (1996) Drosophila telomeres: new views on chromosome evolution. Trends Genet 12: 48–52.

    Article  PubMed  Google Scholar 

  • Purdy A, Su TT (2004) Telomeres: not all breaks are equal. Curr Biol 14: R613–614.

    Article  PubMed  Google Scholar 

  • Rashkova S, Karam SE, Pardue M-L (2002a) Element-specific localization of Drosophila retrotransposon Gag proteins occurs in both nucleus and cytoplasm. Proc Natl Acad Sci USA 99: 3621–3626.

    Article  PubMed  Google Scholar 

  • Rashkova S, Karam SE, Pardue M-L (2002b) Element-specific localization of Drosophila retrotransposon Gag proteins occurs in both nucleus and cytoplasm. Proc Natl Acad Sci USA 99: 3621–3626.

    Article  PubMed  Google Scholar 

  • Rashkova S, Athanasiadis A, Pardue M-L (2003) Intracellular targeting of Gag proteins of the Drosophila telomeric retrotransposons. J Virol 77: 6376–6384.

    Google Scholar 

  • Sahara K, Marec F, Traut W (1999) TTAAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7: 449–460.

    Article  PubMed  Google Scholar 

  • Savitsky M, Kravchuk O, Melnikova L, Georgiev P (2002) Heterochromatin protein 1 is involved in control of telomere elongation in Drosophila melanogaster. Mol Cell Biol 22: 3204–3218.

    Article  PubMed  Google Scholar 

  • Siriaco GM, Cenci G, Haoudi A et al. (2002) Telomere elongation (Tel), a new mutation in Drosophilla melanogaster that produces long telomeres. Genetics 160: 235–245.

    PubMed  Google Scholar 

  • Walter MF, Biessmann H (2004) Expression of the telomeric retrotransposon HeT-A in D. melanogaster is correlated with cell proliferation. Dev Genes Evol 214: 211–219.

    Article  PubMed  Google Scholar 

  • Wills JW, Craven RC (1992) Form, function, and use of retroviral Gag proteins. Aids 5: 639–654.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M.-L. Pardue.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pardue, ML., Rashkova, S., Casacuberta, E. et al. Two retrotransposons maintain telomeres in Drosophila. Chromosome Res 13, 443–453 (2005). https://doi.org/10.1007/s10577-005-0993-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-005-0993-6

Key words

Navigation