Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1984 Sep;4(9):1853–1863. doi: 10.1128/mcb.4.9.1853

High-resolution mapping of DNase I-hypersensitive sites of Drosophila heat shock genes in Drosophila melanogaster and Saccharomyces cerevisiae.

N Costlow, J T Lis
PMCID: PMC368995  PMID: 6436689

Abstract

High-resolution analysis of the chromatin structure of the promoter regions of five Drosophila heat shock genes showed a similar location for the hypersensitive sequences relative to the start of transcription. For each of the five genes examined--those coding for hsp27, hsp26, hsp23, hsp70, and hsp83--the DNase I-hypersensitive sites in Drosophila melanogaster nuclei mapped to two regions upstream of the coding region. These sites occurred on the average, 115 and 17 base pairs upstream from the start of transcription of the five heat shock genes examined. This latter site corresponded to sequences at or near the TATA consensus sequence. Sites even further upstream of the hsp27, hsp26, and hsp83 genes were also evident. Additionally, for the two genes examined--hsp70 and hsp83--the DNase I-hypersensitive sites were preserved, at least within this level of resolution (+/- 10 base pairs), when the Drosophila genes were integrated into the Saccharomyces cerevisiae genome. This result indicates that the signals responsible for generating these hypersensitive sites are inherent in the DNA sequences and, in this case, are not highly species specific.

Full text

PDF
1853

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artavanis-Tsakonas S., Schedl P., Mirault M. E., Moran L., Lis J. Genes for the 70,000 dalton heat shock protein in two cloned D. melanogaster DNA segments. Cell. 1979 May;17(1):9–18. doi: 10.1016/0092-8674(79)90290-3. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M., Bonner J. J. The induction of gene activity in drosophilia by heat shock. Cell. 1979 Jun;17(2):241–254. doi: 10.1016/0092-8674(79)90150-8. [DOI] [PubMed] [Google Scholar]
  3. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  4. Botstein D., Falco S. C., Stewart S. E., Brennan M., Scherer S., Stinchcomb D. T., Struhl K., Davis R. W. Sterile host yeasts (SHY): a eukaryotic system of biological containment for recombinant DNA experiments. Gene. 1979 Dec;8(1):17–24. doi: 10.1016/0378-1119(79)90004-0. [DOI] [PubMed] [Google Scholar]
  5. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Craig E. A., McCarthy B. J. Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucleic Acids Res. 1980 Oct 10;8(19):4441–4457. doi: 10.1093/nar/8.19.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Craig E. A., McCarthy B. J., Wadsworth S. C. Sequence organization of two recombinant plasmids containing genes for the major heat shock-induced protein of D. melanogaster. Cell. 1979 Mar;16(3):575–588. doi: 10.1016/0092-8674(79)90031-x. [DOI] [PubMed] [Google Scholar]
  10. Elgin S. C. DNAase I-hypersensitive sites of chromatin. Cell. 1981 Dec;27(3 Pt 2):413–415. doi: 10.1016/0092-8674(81)90381-0. [DOI] [PubMed] [Google Scholar]
  11. Fristensky B., Lis J., Wu R. Portable microcomputer software for nucleotide sequence analysis. Nucleic Acids Res. 1982 Oct 25;10(20):6451–6463. doi: 10.1093/nar/10.20.6451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hackett R. W., Lis J. T. Localization of the hsp83 transcript within a 3292 nucleotide sequence from the 63B heat shock locus of D. melanogaster. Nucleic Acids Res. 1983 Oct 25;11(20):7011–7030. doi: 10.1093/nar/11.20.7011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herbomel P., Saragosti S., Blangy D., Yaniv M. Fine structure of the origin-proximal DNAase I-hypersensitive region in wild-type and EC mutant polyoma. Cell. 1981 Sep;25(3):651–658. doi: 10.1016/0092-8674(81)90172-0. [DOI] [PubMed] [Google Scholar]
  14. Hinnen A., Hicks J. B., Fink G. R. Transformation of yeast. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1929–1933. doi: 10.1073/pnas.75.4.1929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holmgren R., Livak K., Morimoto R., Freund R., Meselson M. Studies of cloned sequences from four Drosophila heat shock loci. Cell. 1979 Dec;18(4):1359–1370. doi: 10.1016/0092-8674(79)90246-0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Ingolia T. D., Slater M. R., Craig E. A. Saccharomyces cerevisiae contains a complex multigene family related to the major heat shock-inducible gene of Drosophila. Mol Cell Biol. 1982 Nov;2(11):1388–1398. doi: 10.1128/mcb.2.11.1388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ish-Horowicz D., Pinchin S. M., Schedl P., Artavanis-Tsakonas S., Mirault M. E. Genetic and molecular analysis of the 87A7 and 87C1 heat-inducible loci of D. melanogaster. Cell. 1979 Dec;18(4):1351–1358. doi: 10.1016/0092-8674(79)90245-9. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Lis J. T., Neckameyer W., Dubensky R., Costlow N. Cloning and characterization of nine heat-shock-induced mRNAs of Drosophila melanogaster. Gene. 1981 Oct;15(1):67–80. doi: 10.1016/0378-1119(81)90105-0. [DOI] [PubMed] [Google Scholar]
  21. Lis J. T., Simon J. A., Sutton C. A. New heat shock puffs and beta-galactosidase activity resulting from transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell. 1983 Dec;35(2 Pt 1):403–410. doi: 10.1016/0092-8674(83)90173-3. [DOI] [PubMed] [Google Scholar]
  22. McGhee J. D., Wood W. I., Dolan M., Engel J. D., Felsenfeld G. A 200 base pair region at the 5' end of the chicken adult beta-globin gene is accessible to nuclease digestion. Cell. 1981 Nov;27(1 Pt 2):45–55. doi: 10.1016/0092-8674(81)90359-7. [DOI] [PubMed] [Google Scholar]
  23. O'Connor D., Lis J. T. Two closely linked transcription units within the 63B heat shock puff locus of D. melanogaster display strikingly different regulation. Nucleic Acids Res. 1981 Oct 10;9(19):5075–5092. doi: 10.1093/nar/9.19.5075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  28. Shermoen A. W., Beckendorf S. K. A complex of interacting DNAase I-hypersensitive sites near the Drosophila glue protein gene, Sgs4. Cell. 1982 Jun;29(2):601–607. doi: 10.1016/0092-8674(82)90176-3. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Stalder J., Larsen A., Engel J. D., Dolan M., Groudine M., Weintraub H. Tissue-specific DNA cleavages in the globin chromatin domain introduced by DNAase I. Cell. 1980 Jun;20(2):451–460. doi: 10.1016/0092-8674(80)90631-5. [DOI] [PubMed] [Google Scholar]
  33. Sweet R. W., Chao M. V., Axel R. The structure of the thymidine kinase gene promoter: nuclease hypersensitivity correlates with expression. Cell. 1982 Dec;31(2 Pt 1):347–353. doi: 10.1016/0092-8674(82)90128-3. [DOI] [PubMed] [Google Scholar]
  34. Török I., Karch F. Nucleotide sequences of heat shock activated genes in Drosophila melanogaster. I. Sequences in the regions of the 5' and 3' ends of the hsp 70 gene in the hybrid plasmid 56H8. Nucleic Acids Res. 1980 Jul 25;8(14):3105–3123. doi: 10.1093/nar/8.14.3105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wadsworth S. C., Craig E. A., McCarthy B. J. Genes for three Drosophila heat-shock-induced proteins at a single locus. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2134–2137. doi: 10.1073/pnas.77.4.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wu C., Bingham P. M., Livak K. J., Holmgren R., Elgin S. C. The chromatin structure of specific genes: I. Evidence for higher order domains of defined DNA sequence. Cell. 1979 Apr;16(4):797–806. doi: 10.1016/0092-8674(79)90095-3. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES