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Russian Journal of Genetics

, Volume 55, Issue 2, pp 163–171 | Cite as

The SWI/SNF Chromatin Remodeling Complex Is Involved in Spatial Organization of the ftz-f1 Gene Locus

  • J. V. NikolenkoEmail author
  • A. N. Krasnov
  • N. E. Vorobyeva
MOLECULAR GENETICS

Abstract

The ftz-f1 gene encodes a nuclear receptor that plays an important role in ontogenesis of Drosophila melanogaster. Transcription of this gene at the onset of metamorphosis occurs for a short period of time and is subjected to complex multistep regulation. Recently, in the distal part of the first intron of the ftz-f1 gene, we discovered a regulatory element with enhancer properties. In the present work, we continued the study of the chromatin properties in the ftz-f1 gene locus. Using the chromosome conformation capture method (3C), spatial interaction between promoter and intronic enhancer of the studied locus was detected. At the preparatory stage of gene transcription, knockdown of the SAYP subunit, which recruits the SWI/SNF complex to the ftz-f1 gene, caused considerable attenuation of this interaction. At the stage of active gene transcription, SAYP knockdown led to a considerable decrease in the level of histone H3 acetylation at position 27 on the promoter and enhancer. The data obtained indicate the important role of SWI/SNF in the formation of chromatin structure needed for adequate expression of the ftz-f1 gene and its important role in the intronic enhancer activity.

Keywords:

transcription regulation chromatin remodeling complex enhancer histone modifications ecdysone 

Notes

ACKNOWLEDGMENTS

This study was supported by the Molecular and Cellular Biology Program of the Presidium of the Russian Academy of Sciences and by the Russian Foundation for Basic Research (grant nos. 14-04-01297, 17-04-01713, and 18-04-01019).

COMPLIANCE WITH ETHICAL STANDARDS

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

REFERENCES

  1. 1.
    Marsman, J. and Horsfield, J.A., Long distance relationships: enhancer—promoter communication and dynamic gene transcription, Biochim. Biophys. Acta, 2012, vol. 1819, nos. 11—12, pp. 1217—1227.  https://doi.org/10.1016/j.bbagrm.2012.10.008 CrossRefGoogle Scholar
  2. 2.
    Buecker, C. and Wysocka, J., Enhancers as information integration hubs in development: lessons from genomics, Trends Genet., 2012, vol. 28, no. 6, pp. 276—284.  https://doi.org/10.1016/j.tig.2012.02.008 CrossRefGoogle Scholar
  3. 3.
    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.  https://doi.org/10.1093/nar/gks472 CrossRefGoogle Scholar
  4. 4.
    Huet, F., Ruiz, C., and Richards, G., Sequential gene activation by ecdysone in Drosophila melanogaster: the hierarchical equivalence of early and early late genes, Development, 1995, vol. 121, no. 4, pp. 1195—1204.Google Scholar
  5. 5.
    Koelle, M.R., Segraves, W.A., and Hogness, D.S., DHR3: a Drosophila steroid receptor homolog, Proc. Natl. Acad. Sci. U.S.A., 1992, vol. 89, no. 13, pp. 6167—6171.CrossRefGoogle Scholar
  6. 6.
    Lam, G.T., Jiang, C., and Thummel, C.S., Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis, Development, 1997, vol. 124, no. 9, pp. 1757—1769.Google Scholar
  7. 7.
    Ruaud, A.F., Lam, G., and Thummel, C.S., The Drosophila nuclear receptors DHR3 and betaFTZ-F1 control overlapping developmental responses in late embryos, Development, 2010, vol. 137, no. 1, pp. 123—131.  https://doi.org/10.1242/dev.042036 CrossRefGoogle Scholar
  8. 8.
    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.  https://doi.org/10.1080/15384101.2015.1100772 CrossRefGoogle Scholar
  9. 9.
    Vorob’eva, N.E., Mechanism of transcription regulation by RNA polymerase II pausing, Tsitologiya, 2013, vol. 55, no. 3, pp. 153—158.Google Scholar
  10. 10.
    Nikolenko, J.V., Krasnov, A.N., Mazina, M.Y., et al., Studying a novel ecdysone-dependent enhancer, Dokl. Biochem. Biophys., 2017, vol. 474, no. 1, pp. 236—238.  https://doi.org/10.1134/s160767291703022x CrossRefGoogle Scholar
  11. 11.
    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.  https://doi.org/10.4161/cc.10.11.15727 CrossRefGoogle Scholar
  12. 12.
    Shidlovskii, Y.V., Krasnov, A.N., Nikolenko, J.V., et al., A novel multidomain transcription coactivator SAYP can also repress transcription in heterochromatin, EMBO J., 2005, vol. 24, no. 1, pp. 97—107.  https://doi.org/10.1038/sj.emboj.7600508 CrossRefGoogle Scholar
  13. 13.
    Vorobyeva, N.E., Soshnikova, N.V., Nikolenko, J.V., Kuzmina, J.L., 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—11054.  https://doi.org/10.1073/pnas.0901801106 CrossRefGoogle Scholar
  14. 14.
    Mohrmann, L., Langenberg, K., Krijgsveld, J., et al., Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes, Mol. Cell. Biol., 2004, vol. 24, no. 8, pp. 3077—3088.CrossRefGoogle Scholar
  15. 15.
    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.  https://doi.org/10.1093/nar/gkt297 CrossRefGoogle Scholar
  16. 16.
    Gavrilov, A.A. and Razin, S.V., Study of spatial organization of chicken alpha-globin gene domain by 3C technique, Biochemistry (Moscow), 2008, vol. 73, no. 11, pp. 1192—1199.Google Scholar
  17. 17.
    Liang, J., Lacroix, L., Gamot, A., et al., Chromatin immunoprecipitation indirect peaks highlight long-range interactions of insulator proteins and Pol II pausing, Mol. Cell, 2014, vol. 53, no. 4, pp. 672—681.  https://doi.org/10.1016/j.molcel.2013.12.029 CrossRefGoogle Scholar
  18. 18.
    Heintzman, N.D., Stuart, R.K., Hon, G., et al., Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome, Nat. Genet., 2007, vol. 39, no. 3, pp. 311—318.  https://doi.org/10.1038/ng1966 CrossRefGoogle Scholar
  19. 19.
    Koenecke, N., Johnston, J., Gaertner, B., et al., Genome-wide identification of Drosophila dorso-ventral enhancers by differential histone acetylation analysis, Genome Biol., 2016, vol. 17, no. 1, p. 196.  https://doi.org/10.1186/s13059-016-1057-2 CrossRefGoogle Scholar
  20. 20.
    Cubenas-Potts, C., Rowley, M.J., Lyu, X., et al., Different enhancer classes in Drosophila bind distinct architectural proteins and mediate unique chromatin interactions and 3D architecture, Nucleic Acids Res., 2017, vol. 45, no. 4, pp. 1714—1730.  https://doi.org/10.1093/nar/gkw1114 CrossRefGoogle Scholar
  21. 21.
    Ong, C.T. and Corces, V.G., Enhancer function: new insights into the regulation of tissue-specific gene expression, Nat. Rev. Genet., 2011, vol. 12, no. 4, pp. 283—293.  https://doi.org/10.1038/nrg2957 CrossRefGoogle Scholar
  22. 22.
    Euskirchen, G.M., Auerbach, R.K., Davidov, E., et al., Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches, PLoS Genet., 2011, vol. 7, no. 3. e1002008.  https://doi.org/10.1371/journal.pgen.1002008 CrossRefGoogle Scholar
  23. 23.
    Rubtsov, M.A., Polikanov, Y.S., Bondarenko, V.A., et al., Chromatin structure can strongly facilitate enhancer action over a distance, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 47, pp. 17690—17695.  https://doi.org/10.1073/pnas.0603819103 CrossRefGoogle Scholar
  24. 24.
    Ni, Z., Abou El Hassan, M., Xu, Z., et al., The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers, Nat. Immunol., 2008, vol. 9, no. 7, pp. 785—793.  https://doi.org/10.1038/ni.1619 CrossRefGoogle Scholar
  25. 25.
    Cai, S., Lee, C.C., and Kohwi-Shigematsu, T., SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes, Nat. Genet., 2006, vol. 38, no. 11, pp. 1278—1288.  https://doi.org/10.1038/ng1913 CrossRefGoogle Scholar
  26. 26.
    Kim, S.I., Bresnick, E.H., and Bultman, S.J., BRG1 directly regulates nucleosome structure and chromatin looping of the alpha globin locus to activate transcription, Nucleic Acids Res., 2009, vol. 37, no. 18, pp. 6019—6027.  https://doi.org/10.1093/nar/gkp677 CrossRefGoogle Scholar
  27. 27.
    Kim, S.I., Bultman, S.J., Kiefer, C.M., et al., BRG1 requirement for long-range interaction of a locus control region with a downstream promoter, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 7, pp. 2259—2264.  https://doi.org/10.1073/pnas.0806420106 CrossRefGoogle Scholar
  28. 28.
    Barutcu, A.R., Lajoie, B.R., Fritz, A.J., et al., SMARCA4 regulates gene expression and higher-order chromatin structure in proliferating mammary epithelial cells, Genome Res., 2016, vol. 26, no. 9, pp. 1188—1201.  https://doi.org/10.1101/gr.201624.115 CrossRefGoogle Scholar
  29. 29.
    Li, G., Ruan, X., Auerbach, R.K., et al., Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation, Cell, 2012, vol. 148, nos. 1—2, pp. 84—98.  https://doi.org/10.1016/j.cell.2011.12.014 CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  • J. V. Nikolenko
    • 1
    Email author
  • A. N. Krasnov
    • 1
  • N. E. Vorobyeva
    • 1
  1. 1.Institute of Gene Biology, Russian Academy of SciencesMoscowRussia

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