Biochemistry (Moscow)

, Volume 81, Issue 9, pp 1023–1030 | Cite as

Interaction of telomeric retroelement HeT-A transcripts and their protein product gag in early embryogenesis of Drosophila

  • I. A. Olovnikov
  • V. V. Morgunova
  • A. A. Mironova
  • M. Y. Kordyukova
  • E. I. Radion
  • O. M. Olenkina
  • N. V. Akulenko
  • A. I. KalmykovaEmail author


The telomere is a nucleoprotein complex at the ends of linear chromosomes that protects them from fusion and degradation. The telomere consists of telomeric DNA, a protective protein complex and telomeric RNA. Biogenesis of telomeric transcripts in development is still far from being understood. Drosophila telomeres are elongated by a transposition of specialized telomeric retrotransposons that encode proteins. Using transgenic constructs encoding tagged telomeric protein, we found that transcripts of Drosophila telomeric element HeT-A bind Gag-HeT-A protein encoded by these transcripts. Maternal HeT-A transcripts and Gag-HeT-A form ribonucleoprotein granules around centrosomes, centers of microtubule organization, during blastoderm formation, upon disruption of telomere silencing during oogenesis. The specific localization of HeT-A RNA is dependent on microtubules since disruption of microtubules caused delocalization of HeT-A transcripts. This transgenic system is a valuable model for the study of telomeric RNA biogenesis.


telomere development retrotransposon HeT-A Drosophila telomeric RNA 





fluorescence in situ hybridization




Piwi interacting RNA


RNA-binding protein immunoprecipitation


RNA interference




telomeric repeat-containing RNA


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  1. 1.
    Azzalin, C. M., and Lingner, J. (2015) Telomere functions grounding on TERRA firma, Trends Cell Biol., 25, 2936.CrossRefGoogle Scholar
  2. 2.
    Reig-Viader, R., Brieno-Enriquez, M. A., Khouriauli, L., Toran, N., Cabero, L., Giulotto, E., Garcia-Caldes, M., and Ruiz-Herrera, A. (2013) Telomeric repeat-containing RNA and telomerase in human fetal oocytes, Hum. Reprod., 28, 414–422.CrossRefPubMedGoogle Scholar
  3. 3.
    Pardue, M. L., and DeBaryshe, P. G. (2003) Retrotransposons provide an evolutionarily robust nontelomerase mechanism to maintain telomeres, Annu. Rev. Genet., 37, 485–511.CrossRefPubMedGoogle Scholar
  4. 4.
    Raffa, G. D., Cenci, G., Ciapponi, L., and Gatti, M. (2013) Organization and evolution of Drosophila terminin: similarities and differences between Drosophila and human telomeres, Front. Oncol., 3, 112.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Savitsky, M., Kwon, D., Georgiev, P., Kalmykova, A., and Gvozdev, V. (2006) Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline, Genes Dev., 20, 345–354.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Shpiz, S., Kwon, D., Rozovsky, Y., and Kalmykova, A. (2009) rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus, Nucleic Acids Res., 37, 268–278.CrossRefPubMedGoogle Scholar
  7. 7.
    Zhang, L., Beaucher, M., Cheng, Y., and Rong, Y. S. (2014) Coordination of transposon expression with DNA replication in the targeting of telomeric retrotransposons in Drosophila, EMBO J., 33, 1148–1158.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Rashkova, S., Karam, S. E., Kellum, R., and Pardue, M. L. (2002) Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends, J. Cell Biol., 159, 397–402.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Silva-Sousa, R., Lopez-Panades, E., Pineyro, D., and Casacuberta, E. (2012) The chromosomal proteins JIL-1 and Z4/Putzig regulate the telomeric chromatin in Drosophila melanogaster, PLoS Genet., 8, e1003153.CrossRefGoogle Scholar
  10. 10.
    Belfort, M., Curcio, M. J., and Lue, N. F. (2011) Telomerase and retrotransposons: reverse transcriptases that shaped genome, Proc. Natl. Acad. Sci. USA, 108, 20304–20310.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Kopera, H. C., Moldovan, J. B., Morrish, T. A., GarciaPerez, J. L., and Moran, J. V. (2011) Similarities between long interspersed element-1 (LINE-1) reverse transcriptase and telomerase, Proc. Natl. Acad. Sci. USA, 108, 2034520350.CrossRefGoogle Scholar
  12. 12.
    Morrish, T. A., Garcia-Perez, J. L., Stamato, T. D., Taccioli, G. E., Sekiguchi, J., and Moran, J. V. (2007) Endonuclease-independent LINE-1 retrotransposition at mammalian telomeres, Nature, 446, 208–212.CrossRefPubMedGoogle Scholar
  13. 13.
    Aschacher, T., Wolf, B., Enzmann, F., Kienzl, P., Messner, B., Sampl, S., Svoboda, M., Mechtcheriakova, D., Holzmann, K., and Bergmann, M. (2016) LINE-1 induces hTERT and ensures telomere maintenance in tumour cell lines, Oncogene, 35, 94–104.CrossRefPubMedGoogle Scholar
  14. 14.
    Fujiwara, H., Osanai, M., Matsumoto, T., and Kojima, K. K. (2005) Telomere-specific non-LTR retrotransposons and telomere maintenance in the silkworm, Bombyx mori, Chromosome Res., 13, 455–467.PubMedGoogle Scholar
  15. 15.
    Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends, Science, 318, 798–801.CrossRefPubMedGoogle Scholar
  16. 16.
    Bah, A., Wischnewski, H., Shchepachev, V., and Azzalin, C. M. (2012) The telomeric transcriptome of Schizosaccharomyces pombe, Nucleic Acids Res., 40, 2995–3005.CrossRefPubMedGoogle Scholar
  17. 17.
    Cao, F., Li, X., Hiew, S., Brady, H., Liu, Y., and Dou, Y. (2009) Dicer independent small RNAs associate with telomeric heterochromatin, RNA, 15, 1274–1281.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Vrbsky, J., Akimcheva, S., Watson, J. M., Turner, T. L., Daxinger, L., Vyskot, B., Aufsatz, W., and Riha, K. (2010) siRNA-mediated methylation of Arabidopsis telomeres, PLoS Genet., 6, e1000986.CrossRefGoogle Scholar
  19. 19.
    Morgunova, V., Akulenko, N., Radion, E., Olovnikov, I., Abramov, Y., Olenina, L. V., Shpiz, S., Kopytova, D. V., Georgieva, S. G., and Kalmykova, A. (2015) Telomeric repeat silencing in germ cells is essential for early development in Drosophila, Nucleic Acids Res., 43, 8762–8773.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Nakamura, M., Zhou, X. Z., Kishi, S., Kosugi, I., Tsutsui, Y., and Lu, K. P. (2001) A specific interaction between the telomeric protein Pin2/TRF1 and the mitotic spindle, Curr. Biol., 11, 1512–1516.CrossRefPubMedGoogle Scholar
  21. 21.
    Smith, S., Giriat, I., Schmitt, A., and De Lange, T. (1998) Tankyrase, a poly(ADP-ribose) polymerase at human telomeres, Science, 282, 1484–1487.PubMedGoogle Scholar
  22. 22.
    Jain, R., Devine, T., George, A. D., Chittur, S. V., Baroni, T. E., Penalva, L. O., and Tenenbaum, S. A. (2011) RIPChip analysis: RNA-binding protein immunoprecipitation-microarray (Chip) profiling, Methods Mol. Biol., 703, 247–263.CrossRefPubMedGoogle Scholar
  23. 23.
    Brennecke, J., Aravin, A. A., Stark, A., Dus, M., Kellis, M., Sachidanandam, R., and Hannon, G. J. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila, Cell, 128, 1089–1103.CrossRefPubMedGoogle Scholar
  24. 24.
    Lopez-Panades, E., Gavis, E. R., and Casacuberta, E. (2015) Specific localization of the drosophila telomere transposon proteins and RNAs, give insight in their behavior, control and telomere biology in this organism, PLoS One, 10, e0128573.Google Scholar
  25. 25.
    Vagin, V. V., Klenov, M. S., Kalmykova, A. I., Stolyarenko, A. D., Kotelnikov, R. N., and Gvozdev, V. A. (2004) The RNA interference proteins and vasa locus are involved in the silencing of retrotransposons in the female germline of Drosophila melanogaster, RNA Biol., 1, 54–58.CrossRefPubMedGoogle Scholar
  26. 26.
    Wei, W., Gilbert, N., Ooi, S. L., Lawler, J. F., Ostertag, E. M., Kazazian, H. H., Boeke, J. D., and Moran, J. V. (2001) Human L1 retrotransposition: cis preference versus transcomplementation, Mol. Cell. Biol., 21, 1429–1439.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kulpa, D. A., and Moran, J. V. (2006) Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles, Nat. Struct. Mol. Biol., 13, 655–660.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • I. A. Olovnikov
    • 1
  • V. V. Morgunova
    • 1
  • A. A. Mironova
    • 1
  • M. Y. Kordyukova
    • 1
  • E. I. Radion
    • 1
  • O. M. Olenkina
    • 1
  • N. V. Akulenko
    • 1
  • A. I. Kalmykova
    • 1
    Email author
  1. 1.Institute of Molecular GeneticsRussian Academy of SciencesMoscowRussia

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