Skip to main content
Log in

Distant interactions between enhancers and promoters in Drosophila melanogaster are mediated by transgene-flanking Su(Hw) insulators

  • Molecular Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Insulators are DNA elements modulating gene activation by enhancers. Interaction between insulators can result in either isolation, or activation of promoter by the enhancer. In the present study, it is demonstrated that in transgenic lines, the yellow enhancers are unable to activate promoter of the target gene through the mini-white gene. The mini-white promoter, which functions as an insulator, can block the enhancer activity. In case that the genes and regulatory elements in the construct are flanked by Su(Hw) insulators from retrotransposon MDG4, interaction between enhancers and the yellow promoter is restored. The data obtained are congruent with the model suggesting that promoters can function as insulators, and that interaction between the insulators facilitates the interaction between enhancers and promoters within transcriptional domain.

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.

Similar content being viewed by others

References

  1. Bartkuhn, M. and Renkawitz, R., Long Range Chromatin Interactions Involved in Gene Regulation, Biochim. Biophys. Acta, 2008, vol. 1783, no. 11, pp. 2161–2166.

    Article  PubMed  CAS  Google Scholar 

  2. Maksimenko, O.G., Chetverina, D.A., and Georgiev, P.G., Insulators of Higher Eukaryotes: Properties, Mechanisms of Action, and Role in Transcriptional Regulation, Russ. J. Genet., 2006, vol. 42, no. 8, pp. 845–857.

    Article  CAS  Google Scholar 

  3. Gaszner, M. and Felsenfeld, G., Insulators: Exploiting Transcriptional and Epigenetic Mechanisms, Nat. Rev. Genet., 2006, vol. 7, no. 9, pp. 703–713.

    Article  PubMed  CAS  Google Scholar 

  4. Wallace, J.A. and Felsenfeld, G., We Gather Together: Insulators and Genome Organization, Curr. Opin. Genet. Dev., 2007, vol. 17, no. 5, pp. 400–407.

    Article  PubMed  CAS  Google Scholar 

  5. Muravyova, E., Golovnin, A., Gracheva, E., et al., Loss of Insulator Activity by Paired Su(Hw) Chromatin Insulators, Science, 2001, vol. 291, no. 5503, pp. 495–498.

    Article  PubMed  CAS  Google Scholar 

  6. Cai, H. and Shen, P., Effects on cis Arrangement of Chromatin Insulators on Enhancer-Blocking Activity, Science, 2001, vol. 291, no. 5503, pp. 493–495.

    Article  PubMed  CAS  Google Scholar 

  7. Kuhn, E.J., Viering, M.M., Rhodes, K.M., and Geyer, P.K., A Test of Insulator Interactions in Drosophila, EMBO J., 2003, vol. 22, no. 10, pp. 2463–2471.

    Article  PubMed  CAS  Google Scholar 

  8. 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.

    Article  PubMed  CAS  Google Scholar 

  9. Kyrchanova, O., Chetverina, D., Maksimenko, O., et al., Orientation-Dependent Interaction between Drosophila Insulators Is a Property of This Class of Regulatory Elements, Nucleic Acids Res., 2008, vol. 36, no. 22, pp. 7019–7028.

    Article  PubMed  CAS  Google Scholar 

  10. Erokhin, M.M., Georgiev, P.G., and Chetverina, D.A., Effects of Functional Interactions between Nonhomologous Insulators Wari and Su(Hw), Russ. J. Genet., 2010, vol. 46, no. 1, pp. 13–19.

    Article  CAS  Google Scholar 

  11. Geyer, P.K., The Role of Insulator Elements in Defining Domains of Gene Expression, Curr. Opin. Genet. Dev., 1997, vol. 7, no. 2, pp. 242–248.

    Article  PubMed  CAS  Google Scholar 

  12. Vazquez, J. and Schedl, P., Deletion of an Insulator Element by the Mutation Facet-Strawberry in Drosophila melanogaster, Genetics, 2000, vol. 155, no. 3, pp. 1297–1311.

    PubMed  CAS  Google Scholar 

  13. Conte, C., Dastugue, B., and Vaury, C., Coupling of Enhancer and Insulator Properties Identified in Two Retrotransposons Modulates Their Mutagenic Impact on Nearby Genes, Mol. Cell Biol., 2002, vol. 22, no. 6, pp. 1767–1777.

    Article  PubMed  CAS  Google Scholar 

  14. Kuhn, E.J., Hart, C.M., and Geyer, P.K., Studies of the Role of the Drosophila scs and scs’ Insulators in Defining Boundaries of a Chromosome Puff, Mol. Cell Biol., 2004, vol. 24, no. 4, pp. 1470–1480.

    Article  PubMed  CAS  Google Scholar 

  15. Chopra, V.S., Cande, J., Hong, J.W., and Levine, M., Stalled Hox Promoters as Chromosomal Boundaries, Genes Dev., 2009, vol. 23, no. 13, pp. 1505–1509.

    Article  PubMed  CAS  Google Scholar 

  16. Pirrotta, V., Vectors for P-Mediated Transformation in Drosophila, Biotechnology, 1988, vol. 10, pp. 437–456.

    CAS  Google Scholar 

  17. Chetverina, D., Savitskaya, E., Maksimenko, O., et al., Red Flag on the White Reporter: A Versatile Insulator Abuts the white Gene in Drosophila and Is Omnipresent in Mini-White Constructs, Nucleic Acids Res., 2008, vol. 36, no. 3, pp. 929–937.

    Article  PubMed  CAS  Google Scholar 

  18. 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.

    Article  PubMed  CAS  Google Scholar 

  19. Karess, R.E. and Rubin, G.M., Analysis of P Transposable Element Functions in Drosophila, Cell, 1984, vol. 38, no. 1, pp. 135–146.

    Article  PubMed  CAS  Google Scholar 

  20. Rubin, G.M. and Spradling, A.C., Genetic Transformation of Drosophila with Transposable Element Vectors, Science, 1982, vol. 218, no. 4570, pp. 348–353.

    Article  PubMed  CAS  Google Scholar 

  21. Spradling, A.C. and Rubin, G.M., Transposition of Cloned P Elements into Drosophila Germ Line Chromosomes, Science, 1982, vol. 218, no. 4570, pp. 341–347.

    Article  PubMed  CAS  Google Scholar 

  22. Pirrotta, V., Steller, H., and Bozzetti, M.P., Multiple Upstream Regulatory Elements Control the Expression of the Drosophila white Gene, EMBO J., 1985, vol. 4, no. 13A, pp. 3501–3508.

    PubMed  CAS  Google Scholar 

  23. Harrison, D.A., Gdula, D.A., Coyne, R.S., and Corces, V.G., A Leucine Zipper Domain of the Suppressor of Hairy-Wing Protein Mediates Its Repressive Effect on Enhancer Function, Genes Dev., 1993, vol. 7, no. 10, pp. 1966–1978.

    Article  PubMed  CAS  Google Scholar 

  24. Smith, S.T., Wickramasinghe, P., Olson, A., et al., Genome Wide ChIP-Chip Analyses Reveal Important Roles for CTCF in Drosophila Genome Organization, Dev. Biol., 2009, vol. 328, no. 2, pp. 518–528.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  CAS  Google Scholar 

  26. Jiang, N., Emberly, E., Cuvier, O., and Hart, C.M., Genome-Wide Mapping of Boundary Element-Associated Factor (BEAF) Binding Sites in Drosophila melanogaster Links BEAF to Transcription, Mol. Cell Biol., 2009, vol. 29, no. 13, pp. 3556–3568.

    Article  PubMed  CAS  Google Scholar 

  27. Bushey, A.M., Ramos, E., and Corces, V.G., Three Subclasses of a Drosophila Insulator Show Distinct and Cell Type-Specific Genomic Distributions, Genes Dev., 2009, vol. 23, no. 11, pp. 1338–1350.

    Article  PubMed  CAS  Google Scholar 

  28. Negre, N., Brown, C.D., Shah, P.K., et al., A Comprehensive Map of Insulator Elements for the Drosophila Genome, PLoS Genet., 2010, vol. 6. e1000814.

    Article  PubMed  Google Scholar 

  29. 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.

    Article  PubMed  CAS  Google Scholar 

  30. Golovnin, A., Melnick, E., Mazur, A., and Georgiev, P., Drosophila Su(Hw) Insulator Can Stimulate Transcription of a Weakened yellow Promoter Over a Distance, Genetics, 2005, vol. 170, no. 3, pp. 1133–1142.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. A. Chetverina.

Additional information

Original Russian Text © A.I. Davydova, M.M. Erokhin, P.G. Georgiev, D.A. Chetverina, 2011, published in Genetika, 2011, Vol. 47, No.8, pp. 1037–1043.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davydova, A.I., Erokhin, M.M., Georgiev, P.G. et al. Distant interactions between enhancers and promoters in Drosophila melanogaster are mediated by transgene-flanking Su(Hw) insulators. Russ J Genet 47, 917–922 (2011). https://doi.org/10.1134/S1022795411080047

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795411080047

Keywords

Navigation