Biochemistry (Moscow)

, Volume 82, Issue 5, pp 565–571 | Cite as

Induction of transposon silencing in the Drosophila germline

  • S. S. Ryazansky
  • A. D. Stolyarenko
  • M. S. Klenov
  • V. A. GvozdevEmail author


In this review we consider the role of the piRNA system in transposable element silencing in the Drosophila melanogaster germline. We focus on new data that demonstrate the mechanisms of initiation of piRNA biogenesis in ovarian germinal cells and the role of Piwi protein in this process, including our own results.


transposon Piwi protein piRNA Drosophila small RNAs 



histone H3 trimethylated at K9


Piwi-interacting RNA


complex of proteins Rhino, Deadlock, and Cutoff


transposable element


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Sarkar, A., Volff, J. N., and Vaury, C. (2016) piRNAs and their diverse roles: a transposable elementdriven tactic for gene regulation? FASEB J., fj.201600637RRfj.201600637RR.Google Scholar
  2. 2.
    Siomi, M. C., Sato, K., Pezic, D., and Aravin, A. A. (2011) PIWI-interacting small RNAs: the vanguard of genome defense, Nat. Rev. Mol. Cell. Biol., 12, 246–258.CrossRefPubMedGoogle Scholar
  3. 3.
    Hirakata, S., and Siomi, M. C. (2016) piRNA biogenesis in the germline: from transcription of piRNA genomic sources to piRNA maturation, Biochim. Biophys. Acta, 1859, 82–92.CrossRefPubMedGoogle Scholar
  4. 4.
    Guzzardo, P. M., Muerdter, F., and Hannon, G. J. (2013) The piRNA pathway in flies: highlights and future directions, Curr. Opin. Genet. Dev., 23, 44–52.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Czech, B., and Hannon, G. J. (2016) One loop to rule them all: the pingpong cycle and piRNA-guided silencing, Trends Biochem. Sci., 41, 324–337.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Cox, D. N., Chao, A., and Lin, H. (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells, Development, 127, 503–514.PubMedGoogle Scholar
  7. 7.
    Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M., and Gvozdev, V. A. (2001) Doublestranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline, Curr. Biol., 11, 1017–1027.CrossRefPubMedGoogle Scholar
  8. 8.
    Aravin, A. A., Klenov, M. S., Vagin, V. V., Bantignies, F., Cavalli, G., and Gvozdev, V. A. (2004) Dissection of a natural RNA silencing process in the Drosophila melanogaster germ line, Mol. Cell. Biol., 24, 6742–6750.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Vagin, V. V., Sigova, A., Li, C., Seitz, H., Gvozdev, V. A., and Zamore, P. D. (2006) A distinct small RNA pathway silences selfish genetic elements in the germline, Science, 313, 320–324.CrossRefPubMedGoogle Scholar
  10. 10.
    Wang, S. H., and Elgin, S. C. (2011) Drosophila Piwi functions downstream of piRNA production mediating a chromatinbased transposon silencing mechanism in female germ line, Proc. Natl. Acad. Sci. USA, 108, 21164–21169.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Shpiz, S., Olovnikov, I., Sergeeva, A., Lavrov, S., Abramov, Y., Savitsky, M., and Kalmykova, A. (2011) Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons, Nucleic Acids Res., 39, 8703–8711.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Klenov, M. S., Sokolova, O. A., Yakushev, E. Y., Stolyarenko, A. D., Mikhaleva, E. A., Lavrov, S. A., and Gvozdev, V. A. (2011) Separation of stem cell maintenance and transposon silencing functions of Piwi protein, Proc. Natl. Acad. Sci. USA, 108, 18760–18765.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Sienski, G., Donertas, D., and Brennecke, J. (2012) Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression, Cell, 151, 964–980.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Rozhkov, N. V., Hammell, M., and Hannon, G. J. (2013) Multiple roles for Piwi in silencing Drosophila transposons, Genes Dev., 27, 400–412.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sienski, G., Batki, J., Senti, K. A., Donertas, D., Tirian, L., Meixner, K., and Brennecke, J. (2015) Silencio/CG9754 connects the Piwi–piRNA complex to the cellular heterochromatin machinery, Genes Dev., 29, 2258–2271.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Yu, Y., Gu, J., Jin, Y., Luo, Y., Preall, J. B., Ma, J., Czech, B., and Hannon, G. J. (2015) Panoramix enforces piRNA-dependent cotranscriptional silencing, Science, 350, 339–342.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Le Thomas, A., Rogers, A. K., Webster, A., Marinov, G. K., Liao, S. E., Perkins, E. M., Hur, J. K., Aravin, A. A., and Toth, K. F. (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state, Genes Dev., 27, 390–399.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Klenov, M. S., Lavrov, S. A., Korbut, A. P., Stolyarenko, A. D., Yakushev, E. Y., Reuter, M., Pillai, R. S., and Gvozdev, V. A. (2014) Impact of nuclear Piwi elimination on chromatin state in Drosophila melanogaster ovaries, Nucleic Acids Res., 42, 6208–6218.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    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
  20. 20.
    Goriaux, C., Theron, E., Brasset, E., and Vaury, C. (2014) History of the discovery of a master locus producing piRNAs: the flamenco/COM locus in Drosophila melanogaster, Front. Genet., 5, 257.PubMedGoogle Scholar
  21. 21.
    Lau, N. C., Robine, N., Martin, R., Chung, W. J., Niki, Y., Berezikov, E., and Lai, E. C. (2009) Abundant primary piRNAs, endosiRNAs, and microRNAs in a Drosophila ovary cell line, Genome Res., 19, 1776–1785.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Malone, C. D., Brennecke, J., Dus, M., Stark, A., McCombie, W. R., Sachidanandam, R., and Hannon, G. J. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary, Cell, 137, 522–535.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Le Thomas, A., Stuwe, E., Li, S., Du, J., Marinov, G., Rozhkov, N., Chen, Y. C., Luo, Y., Sachidanandam, R., Toth, K. F., Patel, D., and Aravin, A. A. (2014) Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing, Genes Dev., 28, 1667–1680.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Mohn, F., Sienski, G., Handler, D., and Brennecke, J. (2014) The rhino–deadlock–cutoff complex licenses noncanonical transcription of dualstrand piRNA clusters in Drosophila, Cell, 157, 1364–1379.CrossRefPubMedGoogle Scholar
  25. 25.
    Zhang, Z., Wang, J., Schultz, N., Zhang, F., Parhad, S. S., Tu, S., Vreven, T., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2014) The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing, Cell, 157, 1353–1363.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Chen, Y.-C. A., Stuwe, E., Luo, Y., Ninova, M., Le Thomas, A., Rozhavskaya, E., Li, S., Vempati, S., Laver, J. D., Patel, D., Smibert, C. A., Lipshitz, H. D., Fejes Toth, K., and Aravin, A. A. (2016) Cutoff suppresses RNA polymerase II termination to ensure expression of piRNA precursors, Mol. Cell, 63, 97–109.CrossRefPubMedGoogle Scholar
  27. 27.
    Zhang, F., Wang, J., Xu, J., Zhang, Z., Koppetsch, B., Schultz, N., Vreven, T., Meignin, C., Davis, I., Zamore, P. D., Weng, Z., and Theurkauf, W. E. (2012) UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery, Cell, 151, 871–884.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Hur, J. K., Luo, Y., Moon, S., Ninova, M., Marinov, G. K., Chung, Y. D., and Aravin, A. A. (2016) Splicingindependent loading of TREX on nascent RNA is required for efficient expression of dualstrand piRNA clusters in Drosophila, Genes Dev., 30, 840–855.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Senti, K. A., Jurczak, D., Sachidanandam, R., and Brennecke, J. (2015) piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire, Genes Dev., 29, 1747–1762.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wang, W., Han, B. W., Tipping, C., Ge, D. T., Zhang, Z., Weng, Z., and Zamore, P. D. (2015) Slicing and binding by Ago3 or Aub trigger Piwibound piRNA production by distinct mechanisms, Mol. Cell, 59, 819–830.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Xiol, J., Spinelli, P., Laussmann, M. A., Homolka, D., Yang, Z., Cora, E., Coute, Y., Conn, S., Kadlec, J., Sachidanandam, R., Kaksonen, M., Cusack, S., Ephrussi, A., and Pillai, R. S. (2014) RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts, Cell, 157, 1698–1711.CrossRefPubMedGoogle Scholar
  32. 32.
    Ishizu, H., Iwasaki, Y. W., Hirakata, S., Ozaki, H., Iwasaki, W., Siomi, H., and Siomi, M. C. (2015) Somatic primary piRNA biogenesis driven by cis-acting RNA elements and trans-acting Yb, Cell Rep., 12, 429–440.CrossRefPubMedGoogle Scholar
  33. 33.
    Homolka, D., Pandey, R. R., Goriaux, C., Brasset, E., Vaury, C., Sachidanandam, R., Fauvarque, M. O., and Pillai, R. S. (2015) PIWI slicing and RNA elements in precursors instruct directional primary piRNA biogenesis, Cell Rep., 12, 418–428.CrossRefPubMedGoogle Scholar
  34. 34.
    Han, B. W., Wang, W., Li, C., Weng, Z., and Zamore, P. D. (2015) Noncoding RNA. piRNA-guided transposon cleavage initiates Zucchinidependent, phased piRNA production, Science, 348, 817–821.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Mohn, F., Handler, D., and Brennecke, J. (2015) Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchinidependent, phased piRNA biogenesis, Science, 348, 812–817.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Klenov, M. S., Lavrov, S. A., Stolyarenko, A. D., Ryazansky, S. S., Aravin, A. A., Tuschl, T., and Gvozdev, V. A. (2007) Repeatassociated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline, Nucleic Acids Res., 35, 5430–5438.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Andress, A., Bei, Y., Fonslow, B. R., Giri, R., Wu, Y., Yates, J. R., and Carthew, R. W. (2016) Spindle-E cycling between nuage and cytoplasm is controlled by Qin and PIWI proteins, J. Cell Biol., 213, 201–211.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Brennecke, J., Malone, C. D., Aravin, A. A., Sachidanandam, R., Stark, A., and Hannon, G. J. (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing, Science, 322, 1387–1392.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Grentzinger, T., Armenise, C., Brun, C., Mugat, B., Serrano, V., Pelisson, A., and Chambeyron, S. (2012) piRNA-mediated transgenerational inheritance of an acquired trait, Genome Res., 22, 1877–1888.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    De Vanssay, A., Bouge, A. L., Boivin, A., Hermant, C., Teysset, L., Delmarre, V., Antoniewski, C., and Ronsseray, S. (2012) Paramutation in Drosophila linked to emergence of a piRNA-producing locus, Nature, 490, 112–115.CrossRefPubMedGoogle Scholar
  41. 41.
    Le Thomas, A., Marinov, G. K., and Aravin, A. A. (2014) A transgenerational process defines piRNA biogenesis in Drosophila virilis, Cell Rep., 8, 1617–1623.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Megosh, H. B., Cox, D. N., Campbell, C., and Lin, H. (2006) The role of PIWI and the miRNA machinery in Drosophila germline determination, Curr. Biol., 16, 1884–1894.CrossRefPubMedGoogle Scholar
  43. 43.
    Harris, A. N., and Macdonald, P. M. (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C, Development, 128, 2823–2832.PubMedGoogle Scholar
  44. 44.
    Vourekas, A., Alexiou, P., Vrettos, N., Maragkakis, M., and Mourelatos, Z. (2016) Sequencedependent but not sequencespecific piRNA adhesion traps mRNAs to the germ plasm, Nature, 531, 390–394.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Fagegaltier, D., Falciatori, I., Czech, B., Castel, S., Perrimon, N., Simcox, A., and Hannon, G. J. (2016) Oncogenic transformation of Drosophila somatic cells induces a functional piRNA pathway, Genes Dev., 30, 1623–1635.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • S. S. Ryazansky
    • 1
  • A. D. Stolyarenko
    • 1
  • M. S. Klenov
    • 1
  • V. A. Gvozdev
    • 1
    Email author
  1. 1.Institute of Molecular GeneticsRussian Academy of SciencesMoscowRussia

Personalised recommendations