Skip to main content
SpringerLink
Log in

Comparative analysis of effectiveness of heat-shock promoters in two Diptera species

  • Cell Molecular Biology
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Heat-shock proteins (Hsp) provide the cellular and full-body adaptation of animals to various adverse environmental conditions. The hsp70 is believed to play a major role in the biological adaptation of all organisms studied so far. In all animals the regulatory regions of the heat shock genes studied include several conservative promoter elements HSEs (heat shock elements) that are needed to bind heat-shock transcription factor (HSF). The promoter regions of the hsp70 genes are extremely conserved and, hence, it has been generally accepted that they are universal and can operate in species that belong to different phyla. In the present work, we performed a comparative analysis that revealed characteristic differences in the hsp70 promoters of two Diptera species, i.e., Drosophila melanogaster and highly thermotolerance soldier fly Stratiomys singularior. We measured promoter activity in D. melanogaster cell culture exploring in vitro luciferase reporter assay. The analysis demonstrated significantly higher strength of D. melanogaster promoters despite that comparable numbers of HSEs were present in both species. These drastic differences in the promoter strength are probably due to the absence of GAF-binding sites, which are necessary for the efficient functioning of D. melanogaster hsp70 promoters. In contrast, the comparison of hsp83 promoters isolated from these two species has not shown significant differences. Our results demonstrate existence of different evolutionary trends in the regulation of the hsp70 expression even within the same order (Diptera).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

HSF:

heat shock transcription factor

HSE:

heat shock element

Hsp:

heat shock proteins

GAF:

GAGA factor

HS:

heat shock

References

  1. Pelham H.R. 1986. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 46, 959–961.

    Article  CAS  PubMed  Google Scholar 

  2. Feder M.E., Hofmann G.E. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243–282.

    Article  CAS  PubMed  Google Scholar 

  3. Abravaya K., Myers M.P., Murphy S.P., Morimoto R.I. 1992. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6, 1153–1164.

    Article  CAS  PubMed  Google Scholar 

  4. Xu Y., Lindquist S. 1993. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. U. S. A. 90, 7074–7078.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Whitesell L., Sutphin P.D., Pulcini E.J., Martinez J.D., Cook P.H. 1998. The physical association of multiple molecular chaperone proteins with mutant p53 is altered by geldanamycin, an HSP90-binding agent. Mol. Cell. Biol. 18, 1517–1524.

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Kosano H., Stensgard B., Charlesworth M.C., McMahon N., Toft D. 1998. The assembly of progesterone receptor-hsp90 complexes using purified proteins. J. Biol. Chem. 273, 32973–32979.

    Article  CAS  PubMed  Google Scholar 

  7. Sato S., Fujita N., Tsuruo T. 2000. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. U. S. A. 97, 10832–10837.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Lindquist S. 1986. The heat-shock response. Annu. Rev. Biochem. 55, 1151–1191.

    Article  CAS  PubMed  Google Scholar 

  9. Evgen’ev M.B., Garbuz D.G., Zatsepina O.G. 2005. Heat shock proteins: Functions and role in adaptation to hyperthermia. Russ. J. Dev. Biol. 36(4), 218–224.

    Article  Google Scholar 

  10. Tian S., Haney R.A., Feder M.E. 2010. Phylogeny disambiguates the evolution of heat-shock cis-regulatory elements in Drosophila. PLoS ONE. 5, e10669.

    Article  PubMed Central  PubMed  Google Scholar 

  11. Morimoto R.I. 1998. Regulation of heat shock transcriptional response: Cross talk between a family of heat shock factors, molecular chaperones and negative regulators. Genes Dev. 12, 3788–3796.

    Article  CAS  PubMed  Google Scholar 

  12. Berger E.M., Vitek M.P., Morganelli C.M. 1985. Transcript length heterogeneity at the small heat shock protein genes of Drosophila. J. Mol. Biol. 186, 137–148.

    Article  CAS  PubMed  Google Scholar 

  13. McMahon A.P., Novak T.J., Britten R.J., Davidson E.H. 1984. Inducible expression of a cloned heat shock fusion gene in sea urchin embryos. Proc. Natl. Acad. Sci. U. S. A. 81, 7490–7494.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Uhlirova M., Asahina M., Riddiford L.M., Jindra M. 2002. Heat-inducible transgenic expression in the silkmoth Bombyx mori. Dev. Genes Evol. 212, 145–151.

    Article  CAS  PubMed  Google Scholar 

  15. Bienz M., Pelham H.R. 1982. Expression of a Drosophila heat-shock protein in Xenopus oocytes: Conserved and divergent regulatory signals. EMBO J. 1, 1583–1588.

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Voellmy R., Rungger D. 1982. Transcription of a Drosophila heat shock gene is heat-induced in Xenopus oocytes. Proc. Natl. Acad. Sci. U. S. A. 79, 1776–1780.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Burke J.E., Ish-Horowicz D. 1982. Expression of Drosophila heat-shock genes is regulated in Rat-1 cells. Nucleic Acids Res. 10, 3821–3830.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Mirault M.E., Southgate R., Delwart E. 1982 Regulation of heat shock genes: A DNA sequence up-stream of Drosphila hsp70 genes is essential for their induction in monkey cells. EMBO J. 1, 1279–1285.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Atkinson P.W., O’Brochta D.A. 1992. In vivo expression of two highly conserved Drosophila genes in Australian sheep blowfly, Lucilia cuprina. Insect Biochem. Mol. Biol. 22, 423–431.

    Article  CAS  Google Scholar 

  20. Kalosaka K., Chrysanthis G., Rojas-Gill A.P., Theodoraki M., Gourzi P., Kyriakopoulos A., Tatari M., Zacharopoulou A., Mintzas A.C. 2006. Evaluation of the activities of the medfly and Drosophila hsp70 promoters in vivo in germ-line transformed medflies. Insect Mol. Biol. 15, 373–382.

    Article  CAS  PubMed  Google Scholar 

  21. Garbuz D.G., Yushenova I.A., Zatsepina O.G., Przhiboro A.A., Bettencourt B.R., Evgen’ev M.B. 2011. Organization and evolution of hsp70 clusters strikingly differ in two species of Stratiomyidae (Diptera) inhabiting thermally contrasting environments. BMC Evol. Biol. 11, 74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Astakhova L.N., Zatsepina O.G., Przhiboro A.A., Evgen’ev M.B., Garbuz D.G. 2013. Novel arrangement and comparative analysis of hsp90 family genes in three thermotolerant species of Stratiomyidae (Diptera). Insect Mol. Biol. 22, 284–296.

    Article  CAS  PubMed  Google Scholar 

  23. Schneider I. 1972. Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morphol. 27, 363–365.

    Google Scholar 

  24. Georgel P.T. 2005. Chromatin potentiation of the hsp70 promoter is linked to GAGA-factor recruitment. Biochem. Cell Biol. 83, 555–565.

    Article  CAS  PubMed  Google Scholar 

  25. Omelina E.S., Baricheva E.M., Oshchepkov D.Yu., Merkulova T.I. 2011. Analysis and recognition of the GAGA transcription factor binding sites in Drosophila genes. Comput. Biol. Chem. 35, 363–370.

    Article  CAS  PubMed  Google Scholar 

  26. Garbuz D.G., Zatsepina O.G., Przhiboro A.A., Yushenova I., Guzhova I.V., Evgen’ev M.B. 2008. Larvae of related Diptera species from thermally contrasting habitats exhibit continuous up-regulation of heat shock proteins and high thermotolerance. Mol. Ecol. 17, 4763–4777.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia

    L. N. Astakhova, O. G. Zatsepina, M. B. Evgen’ev & D. G. Garbuz

Authors
  1. L. N. Astakhova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. G. Zatsepina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. B. Evgen’ev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. G. Garbuz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. N. Astakhova.

Additional information

Original Russian Text © L.N. Astakhova, O.G. Zatsepina, M.B. Evgen’ev, D.G. Garbuz, 2014, published in Molekulyarnaya Biologiya, 2014, Vol. 48, No. 3, pp. 436–443.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Astakhova, L.N., Zatsepina, O.G., Evgen’ev, M.B. et al. Comparative analysis of effectiveness of heat-shock promoters in two Diptera species. Mol Biol 48, 377–383 (2014). https://doi.org/10.1134/S0026893314030029

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893314030029

Keywords

Search

Navigation