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. 1986 Feb;6(2):663–673. doi: 10.1128/mcb.6.2.663

Sequences involved in temperature and ecdysterone-induced transcription are located in separate regions of a Drosophila melanogaster heat shock gene.

E Hoffman, V Corces
PMCID: PMC367558  PMID: 3097502

Abstract

The transcriptional regulation of the Drosophila melanogaster hsp27 (also called hsp28) gene was studied by introducing altered genes into the germ line by P element-mediated transformation. DNA sequences upstream of the gene were defined with respect to their effect on steroid hormone-induced and heat-induced transcription. These two types of control were found to be separable; the sequences responsible for 80% of heat-induced expression were located more than 1.1 kilobases upstream of the RNA initiation site, while the sequences responsible for the majority of ecdysterone induction were positioned downstream of the site at -227 base pairs. We have determined the DNA sequence of the intergenic region separating hsp23 and hsp27 and have located putative heat shock and ecdysterone consensus sequences. Our results indicate that the heat shock promoter of the hsp27 gene is organized quite differently from that of hsp70.

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Selected References

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  1. Ayme A., Southgate R., Tissières A. Nucleotide sequences responsible for the thermal inducibility of the Drosophila small heat-shock protein genes in monkey COS cells. J Mol Biol. 1985 Apr 20;182(4):469–475. doi: 10.1016/0022-2836(85)90233-5. [DOI] [PubMed] [Google Scholar]
  2. Bourouis M., Richards G. Remote regulatory sequences of the Drosophila glue gene sgs3 as revealed by P-element transformation. Cell. 1985 Feb;40(2):349–357. doi: 10.1016/0092-8674(85)90149-7. [DOI] [PubMed] [Google Scholar]
  3. Burch J. B., Weintraub H. Temporal order of chromatin structural changes associated with activation of the major chicken vitellogenin gene. Cell. 1983 May;33(1):65–76. doi: 10.1016/0092-8674(83)90335-5. [DOI] [PubMed] [Google Scholar]
  4. Cereghini S., Herbomel P., Jouanneau J., Saragosti S., Katinka M., Bourachot B., de Crombrugghe B., Yaniv M. Structure and function of the promoter-enhancer region of polyoma and SV40. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):935–944. doi: 10.1101/sqb.1983.047.01.107. [DOI] [PubMed] [Google Scholar]
  5. Chandler V. L., Maler B. A., Yamamoto K. R. DNA sequences bound specifically by glucocorticoid receptor in vitro render a heterologous promoter hormone responsive in vivo. Cell. 1983 Jun;33(2):489–499. doi: 10.1016/0092-8674(83)90430-0. [DOI] [PubMed] [Google Scholar]
  6. Cheney C. M., Shearn A. Developmental regulation of Drosophila imaginal disc proteins: synthesis of a heat shock protein under non-heat-shock conditions. Dev Biol. 1983 Feb;95(2):325–330. doi: 10.1016/0012-1606(83)90033-7. [DOI] [PubMed] [Google Scholar]
  7. Cohen R. S., Meselson M. Inducible transcription and puffing in Drosophila melanogaster transformed with hsp70-phage lambda hybrid heat shock genes. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5509–5513. doi: 10.1073/pnas.81.17.5509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Corces V., Holmgren R., Freund R., Morimoto R., Meselson M. Four heat shock proteins of Drosophila melanogaster coded within a 12-kilobase region in chromosome subdivision 67B. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5390–5393. doi: 10.1073/pnas.77.9.5390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Costlow N., Lis J. T. High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae. Mol Cell Biol. 1984 Sep;4(9):1853–1863. doi: 10.1128/mcb.4.9.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dudler R., Travers A. A. Upstream elements necessary for optimal function of the hsp 70 promoter in transformed flies. Cell. 1984 Sep;38(2):391–398. doi: 10.1016/0092-8674(84)90494-x. [DOI] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Garfinkel M. D., Pruitt R. E., Meyerowitz E. M. DNA sequences, gene regulation and modular protein evolution in the Drosophila 68C glue gene cluster. J Mol Biol. 1983 Aug 25;168(4):765–789. doi: 10.1016/s0022-2836(83)80074-6. [DOI] [PubMed] [Google Scholar]
  13. Gelbart W. M., McCarron M., Pandey J., Chovnick A. Genetic limits of the xanthine dehydrogenase structural element within the rosy locus in Drosophila melanogaster. Genetics. 1974 Nov;78(3):869–886. doi: 10.1093/genetics/78.3.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hoffman E. P., Corces V. G. Correct temperature induction and developmental regulation of a cloned heat shock gene transformed into the Drosophila germ line. Mol Cell Biol. 1984 Dec;4(12):2883–2889. doi: 10.1128/mcb.4.12.2883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ingolia T. D., Craig E. A. Primary sequence of the 5' flanking regions of the Drosophila heat shock genes in chromosome subdivision 67B. Nucleic Acids Res. 1981 Apr 10;9(7):1627–1642. doi: 10.1093/nar/9.7.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ireland R. C., Berger E., Sirotkin K., Yund M. A., Osterbur D., Fristrom J. Ecdysterone induces the transcription of four heat-shock genes in Drosophila S3 cells and imaginal discs. Dev Biol. 1982 Oct;93(2):498–507. doi: 10.1016/0012-1606(82)90137-3. [DOI] [PubMed] [Google Scholar]
  17. Karess R. E., Rubin G. M. Analysis of P transposable element functions in Drosophila. Cell. 1984 Aug;38(1):135–146. doi: 10.1016/0092-8674(84)90534-8. [DOI] [PubMed] [Google Scholar]
  18. Keene M. A., Corces V., Lowenhaupt K., Elgin S. C. DNase I hypersensitive sites in Drosophila chromatin occur at the 5' ends of regions of transcription. Proc Natl Acad Sci U S A. 1981 Jan;78(1):143–146. doi: 10.1073/pnas.78.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mace H. A., Pelham H. R., Travers A. A. Association of an S1 nuclease-sensitive structure with short direct repeats 5' of Drosophila heat shock genes. Nature. 1983 Aug 11;304(5926):555–557. doi: 10.1038/304555a0. [DOI] [PubMed] [Google Scholar]
  20. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mason P. J., Török I., Kiss I., Karch F., Udvardy A. Evolutionary implications of a complex pattern of DNA sequence homology extending far upstream of the hsp70 genes at loci 87A7 and 87C1 in Drosophila melanogaster. J Mol Biol. 1982 Mar 25;156(1):21–35. doi: 10.1016/0022-2836(82)90456-9. [DOI] [PubMed] [Google Scholar]
  22. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McGinnis W., Shermoen A. W., Heemskerk J., Beckendorf S. K. DNA sequence changes in an upstream DNase I-hypersensitive region are correlated with reduced gene expression. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1063–1067. doi: 10.1073/pnas.80.4.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McKnight S. L., Gavis E. R., Kingsbury R., Axel R. Analysis of transcriptional regulatory signals of the HSV thymidine kinase gene: identification of an upstream control region. Cell. 1981 Aug;25(2):385–398. doi: 10.1016/0092-8674(81)90057-x. [DOI] [PubMed] [Google Scholar]
  25. Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
  26. Morganelli C. M., Berger E. M., Pelham H. R. Transcription of Drosophila small hsp-tk hybrid genes is induced by heat shock and by ecdysterone in transfected Drosophila cells. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5865–5869. doi: 10.1073/pnas.82.17.5865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Muskavitch M. A., Hogness D. S. An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell. 1982 Jul;29(3):1041–1051. doi: 10.1016/0092-8674(82)90467-6. [DOI] [PubMed] [Google Scholar]
  28. Neidhardt F. C., VanBogelen R. A., Vaughn V. The genetics and regulation of heat-shock proteins. Annu Rev Genet. 1984;18:295–329. doi: 10.1146/annurev.ge.18.120184.001455. [DOI] [PubMed] [Google Scholar]
  29. Pardue M. L., Gall J. G. Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol. 1975;10:1–16. doi: 10.1016/s0091-679x(08)60727-x. [DOI] [PubMed] [Google Scholar]
  30. Parker C. S., Topol J. A Drosophila RNA polymerase II transcription factor binds to the regulatory site of an hsp 70 gene. Cell. 1984 May;37(1):273–283. doi: 10.1016/0092-8674(84)90323-4. [DOI] [PubMed] [Google Scholar]
  31. Payvar F., DeFranco D., Firestone G. L., Edgar B., Wrange O., Okret S., Gustafsson J. A., Yamamoto K. R. Sequence-specific binding of glucocorticoid receptor to MTV DNA at sites within and upstream of the transcribed region. Cell. 1983 Dec;35(2 Pt 1):381–392. doi: 10.1016/0092-8674(83)90171-x. [DOI] [PubMed] [Google Scholar]
  32. Pelham H. R. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell. 1982 Sep;30(2):517–528. doi: 10.1016/0092-8674(82)90249-5. [DOI] [PubMed] [Google Scholar]
  33. Pelham H. R., Bienz M. A synthetic heat-shock promoter element confers heat-inducibility on the herpes simplex virus thymidine kinase gene. EMBO J. 1982;1(11):1473–1477. doi: 10.1002/j.1460-2075.1982.tb01340.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  35. Rubin G. M., Spradling A. C. Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 1983 Sep 24;11(18):6341–6351. doi: 10.1093/nar/11.18.6341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Scheidereit C., Geisse S., Westphal H. M., Beato M. The glucocorticoid receptor binds to defined nucleotide sequences near the promoter of mouse mammary tumour virus. Nature. 1983 Aug 25;304(5928):749–752. doi: 10.1038/304749a0. [DOI] [PubMed] [Google Scholar]
  38. Selleck S. B., Elgin S. C., Cartwright I. L. Supercoil-dependent features of DNA structure at Drosophila locus 67B1. J Mol Biol. 1984 Sep 5;178(1):17–33. doi: 10.1016/0022-2836(84)90228-6. [DOI] [PubMed] [Google Scholar]
  39. Simcox A. A., Cheney C. M., Hoffman E. P., Shearn A. A deletion of the 3' end of the Drosophila melanogaster hsp70 gene increases stability of mutant mRNA during recovery from heat shock. Mol Cell Biol. 1985 Dec;5(12):3397–3402. doi: 10.1128/mcb.5.12.3397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Simon J. A., Sutton C. A., Lobell R. B., Glaser R. L., Lis J. T. Determinants of heat shock-induced chromosome puffing. Cell. 1985 Apr;40(4):805–817. doi: 10.1016/0092-8674(85)90340-x. [DOI] [PubMed] [Google Scholar]
  41. Sirotkin K., Davidson N. Developmentally regulated transcription from Drosophila melanogaster chromosomal site 67B. Dev Biol. 1982 Jan;89(1):196–210. doi: 10.1016/0012-1606(82)90307-4. [DOI] [PubMed] [Google Scholar]
  42. Southgate R., Ayme A., Voellmy R. Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B. J Mol Biol. 1983 Mar 25;165(1):35–57. doi: 10.1016/s0022-2836(83)80241-1. [DOI] [PubMed] [Google Scholar]
  43. Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
  44. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  45. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]
  46. Wu C. Two protein-binding sites in chromatin implicated in the activation of heat-shock genes. Nature. 1984 May 17;309(5965):229–234. doi: 10.1038/309229a0. [DOI] [PubMed] [Google Scholar]
  47. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  48. Zimmerman J. L., Petri W., Meselson M. Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell. 1983 Apr;32(4):1161–1170. doi: 10.1016/0092-8674(83)90299-4. [DOI] [PubMed] [Google Scholar]

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