Skip to main content
Log in

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

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

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.

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.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DAPI:

4′,6-diamidino-2-phenylindole

FISH:

fluorescence in situ hybridization

HA:

hemagglutinin

piRNA:

Piwi interacting RNA

RIP:

RNA-binding protein immunoprecipitation

RNAi:

RNA interference

RNP:

ribonucleoprotein

TERRA:

telomeric repeat-containing RNA

References

  1. Azzalin, C. M., and Lingner, J. (2015) Telomere functions grounding on TERRA firma, Trends Cell Biol., 25, 2936.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  16. Bah, A., Wischnewski, H., Shchepachev, V., and Azzalin, C. M. (2012) The telomeric transcriptome of Schizosaccharomyces pombe, Nucleic Acids Res., 40, 2995–3005.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. I. Kalmykova.

Additional information

Original Russian Text © I. A. Olovnikov, V. V. Morgunova, A. A. Mironova, M. Y. Kordyukova, E. I. Radion, O. M. Olenkina, N. V. Akulenko, A. I. Kalmykova, 2016, published in Biokhimiya, 2016, Vol. 81, No. 9, pp. 1280-1287.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Olovnikov, I.A., Morgunova, V.V., Mironova, A.A. et al. Interaction of telomeric retroelement HeT-A transcripts and their protein product gag in early embryogenesis of Drosophila . Biochemistry Moscow 81, 1023–1030 (2016). https://doi.org/10.1134/S000629791609011X

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S000629791609011X

Keywords

Navigation