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Impact of Interactions between Su(Hw)-Dependent Insulators on the Transvection Effect in Drosophila melanogaster

  • BIOCHEMISTRY, BIOPHYSICS, AND MOLECULAR BIOLOGY
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Abstract

Transvection is a phenomenon of interallelic communication in which enhancers can activate a specific promoter located on a homologous chromosome. Insulators play a significant role in ensuring functional interactions between enhancers and promoters. In the presented work, we created a model where two or three copies of the insulator are located next to enhancers and promoters localized on homologous chromosomes. Using the Su(Hw) insulator as a model, we showed that the functional interaction between a pair of insulators promotes enhancer–promoter trans-interactions. The interaction between the three insulators, on the contrary, can lead to the formation of chromatin loops that sterically hinder the full enhancer–promoter interaction. The results of the work suggest the participation of insulators in the regulation of homologous chromosome pairing and in communication between distant genomic loci.

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REFERENCES

  1. Hafner, A. and Boettiger, A., The spatial organization of transcriptional control, Nat. Rev. Genet., 2023, vol. 24, no. 1, pp. 53–68. https://doi.org/10.1038/s41576-022-00526-0

    Article  CAS  PubMed  Google Scholar 

  2. Kyrchanova, O., Sokolov, V., and Georgiev, P., Mechanisms of interaction between enhancers and promoters in three Drosophila model systems, Int. J. Mol. Sci., 2023, vol. 24, no. 3, p. 2855. https://doi.org/10.3390/ijms24032855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Cavalheiro, G.R., Pollex, T., and Furlong, E.E., To loop or not to loop: what is the role of TADs in enhancer function and gene regulation?, Curr. Opin. Genet. Dev., 2021, vol. 67, pp. 119–129. https://doi.org/10.1016/j.gde.2020.12.015

    Article  CAS  PubMed  Google Scholar 

  4. Geyer, P.K. and Corces, V.G., DNA position-specific repression of transcription by a Drosophila zinc finger protein, Genes Dev., 1992, vol. 6, no. 10, pp. 1865–1873.

    Article  CAS  PubMed  Google Scholar 

  5. Baxley, R.M., Bullard, J.D., Klein, M.W., et al., Deciphering the DNA code for the function of the Droso-phila polydactyl zinc finger protein suppressor of hairy-wing, Nucleic Acids Res., 2017, vol. 45, no. 8, pp. 4463–4478. https://doi.org/10.1093/nar/gkx040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Melnikova, L., Kostyuchenko, M., Molodina, V., et al., Interactions between BTB domain of CP190 and two adjacent regions in Su(Hw) are required for the insulator complex formation, Chromosoma, 2018, vol. 127, no. 1, pp. 59–71. https://doi.org/10.1007/s00412-017-0645-6

    Article  CAS  PubMed  Google Scholar 

  7. Golovnin, A., Melnikova, L., and Babosha, V., The N-terminal part of Drosophila CP190 is a platform for interaction with multiple architectural proteins, Int. J. Mol. Sci., 2023, vol. 24, no. 21, p. 15917. https://doi.org/10.3390/ijms242115917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bartkuhn, M., Straub, T., Herold, M., et al., Active promoters and insulators are marked by the centrosomal protein 190, EMBO J., 2009, vol. 28, no. 7, pp. 877–888. https://doi.org/10.1038/emboj.2009.34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gause, M., Morcillo, P., and Dorsett, D., Insulation of enhancer–promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins, Mol. Cell Biol., 2001, vol. 21, no. 14, pp. 4807–4817. https://doi.org/10.1128/MCB.21.14.4807-4817.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Melnikova, L., Kostyuchenko, M., Molodina, V., et al., Multiple interactions are involved in a highly specific association of the Mod(mdg4)-67.2 isoform with the Su(Hw) sites in Drosophila, Open Biol., 2017, vol. 7, no. 10, p. 170150. https://doi.org/10.1098/rsob.170150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Stogios, P.J., Downs, G.S., Jauhal, J.J.S., et al., Sequence and structural analysis of BTB domain proteins, Genome Biol., 2005, vol. 6, no. 10, p. R82. https://doi.org/10.1186/gb-2005-6-10-r82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Savitskaya E., Melnikova L., Kostuchenko M., et al., Study of long-distance functional interactions between Su(Hw) insulators that can regulate enhancer–promoter communication in Drosophila melanogaster, Mol. Cell Biol., 2006, vol. 26, no. 3, pp. 754–761. https://doi.org/10.1128/MCB.26.3.754-761.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Duncan, I.W., Transvection effects in Drosophila, Annu. Rev. Genet., 2002, vol. 36, pp. 521–556. https://doi.org/10.1146/annurev.genet.36.060402.100441

    Article  CAS  PubMed  Google Scholar 

  14. Kravchenko, E., Savitskaya, E., Kravchuk, O., et al., Pairing between gypsy insulators facilitates the enhancer action in trans throughout the Drosophila genome, Mol. Cell Biol., 2005, vol. 25, no. 21, pp. 9283–9291. https://doi.org/10.1128/MCB.25.21.9283-9291.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Geyer, P.K. and Corces, V.G., Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster, Genes Dev., 1987, vol. 1, no. 9, pp. 996–1004. https://doi.org/10.1101/gad.1.9.996

    Article  CAS  PubMed  Google Scholar 

  16. Qian, S., Varjavand, B., and Pirrotta, V., Molecular analysis of the zeste–white interaction reveals a promoter-proximal element essential for distant enhancer–promoter communication, Genetics, 1992, vol. 131, no. 1, pp. 79–90. https://doi.org/10.1093/genetics/131.1.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Geyer, P.K., Spana, C., and Corces, V.G., On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster, EMBO J., 1986, vol. 5, no. 10, pp. 2657–2662. https://doi.org/10.1002/j.1460-2075.1986.tb04548.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Scott, K.C., Taubman, A.D., and Geyer, P.K., Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength, Genetics, 1999, vol. 153, no. 2, pp. 787–798. https://doi.org/10.1093/genetics/153.2.787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bischof, J., Maeda, R.K., Hediger, M., et al., An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 9, pp. 3312–3317. https://doi.org/10.1073/pnas.0611511104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Baxley, R.M., Soshnev, A.A., Koryakov, D.E., et al., The role of the Suppressor of Hairy-wing insulator protein in Drosophila oogenesis, Dev. Biol., 2011, vol. 356, no. 2, pp. 398–410. https://doi.org/10.1016/j.ydbio.2011.05.666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The study was supported by the Russian Science Foundation (project no. 22-24-00719).

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Authors and Affiliations

  1. Institute of Gene Biology, Russian Academy of Sciences, Moscow, Russia

    L. S. Melnikova, V. V. Molodina,  P. G. Georgiev & A. K. Golovnin

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  1. L. S. Melnikova
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  2. V. V. Molodina
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  3. P. G. Georgiev
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  4. A. K. Golovnin
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Correspondence to L. S. Melnikova.

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Translated by M. Batrukova

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Melnikova, L.S., Molodina, V.V., Georgiev, P.G. et al. Impact of Interactions between Su(Hw)-Dependent Insulators on the Transvection Effect in Drosophila melanogaster. Dokl Biochem Biophys (2024). https://doi.org/10.1134/S1607672924700820

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  • DOI: https://doi.org/10.1134/S1607672924700820

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