Russian Journal of Genetics

, Volume 53, Issue 2, pp 178–186 | Cite as

Coactivator complexes participate in different stages of the Drosophila melanogaster hsp70 gene transcription

  • M. Yu. Mazina
  • P. K. Derevyanko
  • E. V. Kocheryzhkina
  • Yu. V. Nikolenko
  • A. N. Krasnov
  • N. E. VorobyevaEmail author
Molecular Genetics


The objective of this study was to identify transcriptional coactivators participating in transcription elongation of the hsp70 gene induced by heat shock. We found that all investigated coactivator complexes participate in transcription of this gene, as significant level of them were present at the gene promoter in its active state. For most of the coactivators (except for p300/CBP, Set2, and Mediator complex), we also observed a considerable increase of their binding level at the coding region of the gene after activation of its transcription by heat shock. We assume that coactivators CHD1, ISWI, Brm, Kismet-L, INO80, Mi-2, Gcn5, Lid/KDM5, Set1, DART1, DART4, SSRP1, PAF1, and Fs(1)h/Brd4 bind to the promoter of the active hsp70 gene and migrate to its coding region together with elongating RNA polymerase II. It can be suggested that some of these coactivators play an important role in stimulating the transition of the RNA polymerase II complex from transcription initiation to elongation stage.


transcription coactivator complexes chromatin covalent histone modifications RNA polymerase II 


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  1. 1.
    Krasnov, A.N., Mazina, M.Y., Nikolenko, J.V., and Vorobyeva, N.E., On the way of revealing coactivator complexes cross-talk during transcriptional activation, Cell Biosci., 2016, vol. 6, no. 15. doi 10.1186/s13578- 016-0081-yGoogle Scholar
  2. 2.
    van Nuland, R., Schram, A.W., van Schaik, F.M., et al., Multivalent engagement of TFIID to nucleosomes, PLoS One, 2013, vol. 8, no. 9. e73495. doi 10.1371/journal.pone.0073495CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Agalioti, T., Chen, G., and Thanos, D., Deciphering the transcriptional histone acetylation code for a human gene, Cell, 2002, vol. 111, no. 3, pp. 381–392.CrossRefPubMedGoogle Scholar
  4. 4.
    Rybtsova, N., Leimgruber, E., Seguin-Estevez, Q., et al., Transcription-coupled deposition of histone modifications during MHC class II gene activation, Nucleic Acids Res., 2007, vol. 35, no. 10, pp. 3431–3441.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Metivier, R., Penot, G., Hubner, M.R., et al., Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter, Cell, 2003, vol. 115, no. 6, pp. 751–763.PubMedGoogle Scholar
  6. 6.
    Vicent, G.P., Nacht, A.S., Font-Mateu, J., et al., Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation, Genes Dev., 2011, vol. 25, no. 8, pp. 845–862. doi 10.1101/gad.621811CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ding, Y., Ndamukong, I., Xu, Z., et al., ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes, PLoS Genet., 2012, vol. 8, no. 12. e1003111. doi 10.1371/journal.pgen.1003111CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Hampsey, M. and Reinberg, D., Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation, Cell, 2003, vol. 113, no. 4, pp. 429–432.CrossRefPubMedGoogle Scholar
  9. 9.
    Venkatesh, S. and Workman, J.L., Set2 mediated H3 lysine 36 methylation: regulation of transcription elongation and implications in organismal development, Wiley Interdisciplin. Rev. Dev. Biol., 2013, vol. 2, no. 5, pp. 685–700. doi 10.1002/wdev.109CrossRefGoogle Scholar
  10. 10.
    Lloret-Llinares, M., Perez-Lluch, S., Rossell, D., et al., dKDM5/LID regulates H3K4me3 dynamics at the transcription-start site (TSS) of actively transcribed developmental genes, Nucleic Acids Res., 2012, vol. 40, no. 19, pp. 9493–9505. doi 10.1093/nar/gks773CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Reid, G., Gallais, R., and Metivier, R., Marking time: the dynamic role of chromatin and covalent modification in transcription, Int. J. Biochem. Cell Biol., 2009, vol. 41, no. 1, pp. 155–163. doi 10.1016/j.biocel. 2008.08.028CrossRefPubMedGoogle Scholar
  12. 12.
    Mazina, M.Yu. and Vorobyeva, N.E., The role of ATPdependent chromatin remodeling complexes in regulation of genetic processes, Russ. J. Genet., 2016, vol. 52, no. 5, pp. 463–472.CrossRefGoogle Scholar
  13. 13.
    Malik, S. and Roeder, R.G., The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation, Nat. Rev. Genet., 2010, vol. 11, no. 11, pp. 761–772. doi 10.1038/nrg2901CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Vorobyeva, N.E., Soshnikova, N.V., Nikolenko, J.V., et al., Transcription coactivator SAYP combines chromatin remodeler Brahma and transcription initiation factor TFIID into a single supercomplex, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 27, pp. 11049–1154. doi 10.1073/pnas.0901801106CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Lauberth, S.M., Nakayama, T., Wu, X., et al., H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation, Cell, 2013, vol. 152, no. 5, pp. 1021–1036.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Adelman, K. and Lis, J.T., Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans, Nat. Rev. Genet., 2012, vol. 13, no. 10, pp. 720–731. doi 10.1038/nrg3293CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Vorob’eva, N.E., Mechanism of transcription regulation by RNA polymerase II pausing, Tsitologiia, 2013, vol. 55, no. 3, pp. 153–158.PubMedGoogle Scholar
  18. 18.
    Yang, Z., Yik, J.H., Chen, R., et al., Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4, Mol. Cell, 2005, vol. 19, no. 4, pp. 535–545.CrossRefPubMedGoogle Scholar
  19. 19.
    Krogan, N.J., Dover, J., Wood, A., et al., The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation, Mol. Cell, 2003, vol. 11, no. 3, pp. 721–729.CrossRefPubMedGoogle Scholar
  20. 20.
    Shimojima, T., Okada, M., Nakayama, T., et al., Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor, Genes Dev., 2003, vol. 17, no. 13, pp. 1605–1616.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Mazina, M.Yu., Kocheryzhkina, E.V., Derevyanko, P.K., and Vorobyeva, N.E., The composition of SWI/SNF chromatin remodeling complex is stable during gene transcription, Tsitologiia, 2016, vol. 58, no. 4, pp. 285–288.Google Scholar
  22. 22.
    Vorobyeva, N.E., Nikolenko, J.V., Nabirochkina, E.N., et al., SAYP and Brahma are important for “repressive” and “transient” Pol II pausing, Nucleic Acids Res., 2012, vol. 40, no. 15, pp. 7319–7331. doi 10.1093/nar/gks472CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Mathieu, E.L., Finkernagel, F., Murawska, M., et al., Recruitment of the ATP-dependent chromatin remodeler dMi-2 to the transcribed region of active heat shock genes, Nucleic Acids Res., 2012, vol. 40, no. 11, pp. 4879–4891. doi 10.1093/nar/gks178CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Srinivasan, S., Armstrong, J.A., Deuring, R., et al., The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II, Development, 2005, vol. 132, no. 7, pp. 1623–1635.CrossRefPubMedGoogle Scholar
  25. 25.
    Zentner, G.E., Tsukiyama, T., and Henikoff, S., ISWI and CHD chromatin remodelers bind promoters but act in gene bodies, PLoS Genet., 2013, vol. 9, no. 2. e1003317. doi 10.1371/journal.pgenCrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Rougvie, A.E. and Lis, J.T., The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged, Cell, 1988, vol. 54, no. 6, pp. 795–804.CrossRefPubMedGoogle Scholar
  27. 27.
    Vorobyeva, N.E., Nikolenko, J.V., Krasnov, A.N., et al., SAYP interacts with DHR3 nuclear receptor and participates in ecdysone-dependent transcription regulation, Cell Cycle, 2011, vol. 10, no. 11, pp. 1821–1827.CrossRefPubMedGoogle Scholar
  28. 28.
    Mazina, M.Y., Nikolenko, J.V., Fursova, N.A., et al., Early-late genes of the ecdysone cascade as models for transcriptional studies, Cell Cycle, 2015, vol. 14, no. 22, pp. 3593–3601. doi 10.1080/15384101.2015.1100772CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Vorobyeva, N.E., Mazina, M.U., Golovnin, A.K., et al., Insulator protein Su(Hw) recruits SAGA and Brahma complexes and constitutes part of Origin Recognition Complex-binding sites in the Drosophila genome, Nucleic Acids Res., 2013, vol. 41, no. 11, pp. 5717–5730. doi 10.1093/nar/gkt297CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Mazina, M.Yu., Nikolenko, Yu.V., Krasnov, A.N., and Vorobyeva, N.E., SWI/SNF protein complexes participate in the initiation and elongation stages of Drosophila hsp70 gene transcription, Russ. J. Genet., 2016, vol. 52, no. 2, pp. 141–145. doi 10.1134/S1022795416010105CrossRefGoogle Scholar
  31. 31.
    Kopytova, D.V., Orlova, A.V., Krasnov, A.N., et al., Multifunctional factor ENY2 is associated with the THO complex and promotes its recruitment onto nascent mRNA, Genes Dev., 2010, vol. 24, no. 1, pp. 86–96. doi 10.1101/gad.550010CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Lebedeva, L.A., Nabirochkina, E.N., Kurshakova, M.M., et al., Occupancy of the Drosophila hsp70 promoter by a subset of basal transcription factors diminishes upon transcriptional activation, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, no. 50, pp. 18087–18092.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2017

Authors and Affiliations

  • M. Yu. Mazina
    • 1
  • P. K. Derevyanko
    • 1
  • E. V. Kocheryzhkina
    • 1
  • Yu. V. Nikolenko
    • 1
  • A. N. Krasnov
    • 1
  • N. E. Vorobyeva
    • 1
    Email author
  1. 1.Institute of Gene BiologyRussian Academy of SciencesMoscowRussia

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