Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1981 Oct 10;9(19):5075–5092. doi: 10.1093/nar/9.19.5075

Two closely linked transcription units within the 63B heat shock puff locus of D. melanogaster display strikingly different regulation.

D O'Connor, J T Lis
PMCID: PMC327500  PMID: 6118854

Abstract

We report the isolation and characterization of a cloned DNA of D. melanogaster, Dm4L, that is derived from the major heat shock puff site at 63B. This segment contains two closely linked genes that are each present once per Drosophila haploid genome. One of these, the hsp 83 gene, encodes an abundant heat shock mRNA that, unlike other major heat shock mRNAs, is also abundant in uninduced (23 degrees) kco cells. Although only a slight increase in the level of total hsp 83 RNA can be detected after heat shock in Kco cells, the level of hsp 83 poly(A)+ mRNA increases more than 6-fold and the level of pulse-labeled hsp 83 RNA in total cellular RNA increases 11-fold relative to uninduced cells. In contrast, the levels of total, poly(A)+, and pulse-labeled RNA homologous to the second gene, 63B-T2, are approximately the same in both induced and uninduced cells. Hence, even though these genes are separated by only one thousand base pairs, and, from in situ hybridization to polytene chromosomes, both lie within the heat shock puff, they display strikingly different regulatory properties, These results demonstrate that close linkage of a gene to a heat shock puff is not sufficient to render its expression heat inducible.

Full text

PDF
5075

Images in this article

5079Image
on p.5079
5081Image
on p.5081
5083Image
on p.5083
5084Image
on p.5084
5086Image
on p.5086
5088Image
on p.5088

Selected References

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

  1. Arrigo A. P., Fakan S., Tissières A. Localization of the heat shock-induced proteins in Drosophila melanogaster tissue culture cells. Dev Biol. 1980 Jul;78(1):86–103. doi: 10.1016/0012-1606(80)90320-6. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Ashburner M. Patterns of puffing activity in the salivary gland chromosomes of Drosophila. V. Responses to environmental treatments. Chromosoma. 1970;31(3):356–376. doi: 10.1007/BF00321231. [DOI] [PubMed] [Google Scholar]
  5. Belyaeva E. S., Zhimulev I. F. RNA synthesis in the Drosophila melanogaster puffs. Cell Differ. 1976 Mar;4(6):415–427. doi: 10.1016/0045-6039(76)90028-2. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Findly R. C., Pederson T. Regulated transcription of the genes for actin and heat-shock proteins in cultured Drosophila cells. J Cell Biol. 1981 Feb;88(2):323–328. doi: 10.1083/jcb.88.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Finnegan D. J., Rubin G. M., Young M. W., Hogness D. S. Repeated gene families in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1053–1063. doi: 10.1101/sqb.1978.042.01.106. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Jamrich M., Greenleaf A. L., Bautz E. K. Localization of RNA polymerase in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1977 May;74(5):2079–2083. doi: 10.1073/pnas.74.5.2079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kaback D. B., Angerer L. M., Davidson N. Improved methods for the formation and stabilization of R-loops. Nucleic Acids Res. 1979 Jun 11;6(7):2499–2317. doi: 10.1093/nar/6.7.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lifton R. P., Goldberg M. L., Karp R. W., Hogness D. S. The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1047–1051. doi: 10.1101/sqb.1978.042.01.105. [DOI] [PubMed] [Google Scholar]
  13. Lindquist S. Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev Biol. 1980 Jun 15;77(2):463–479. doi: 10.1016/0012-1606(80)90488-1. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Lis J. T., Prestidge L., Hogness D. S. A novel arrangement of tandemly repeated genes at a major heat shock site in D. melanogaster. Cell. 1978 Aug;14(4):901–919. doi: 10.1016/0092-8674(78)90345-8. [DOI] [PubMed] [Google Scholar]
  16. Lis J., Neckameyer W., Mirault M. E., Artavanis-Tsakonas S., Lall P., Martin G., Schedl P. DNA sequences flanking the starts of the hsp 70 and alpha beta heat shock genes are homologous. Dev Biol. 1981 Apr 30;83(2):291–300. doi: 10.1016/0012-1606(81)90475-9. [DOI] [PubMed] [Google Scholar]
  17. Livak K. J., Freund R., Schweber M., Wensink P. C., Meselson M. Sequence organization and transcription at two heat shock loci in Drosophila. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5613–5617. doi: 10.1073/pnas.75.11.5613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Rubin G. M., Hogness D. S. Effect of heat shock on the synthesis of low molecular weight RNAs in drosophilia: accumulation of a novel form of 5S RNA. Cell. 1975 Oct;6(2):207–213. doi: 10.1016/0092-8674(75)90011-2. [DOI] [PubMed] [Google Scholar]
  20. Schedl P., Artavanis-Tsakonas S., Steward R., Gehring W. J., Mirault M. E., Goldschmidt-Clermont M., Moran L., Tissières A. Two hybrid plasmids with D. melanogaster DNA sequences complementary to mRNA coding for the major heat shock protein. Cell. 1978 Aug;14(4):921–929. doi: 10.1016/0092-8674(78)90346-x. [DOI] [PubMed] [Google Scholar]
  21. Silver L. M., Elgin S. C. Distribution patterns of three subfractions of drosophila nonhistone chromosomal proteins: possible correlations with gene activity. Cell. 1977 Aug;11(4):971–983. doi: 10.1016/0092-8674(77)90308-7. [DOI] [PubMed] [Google Scholar]
  22. Spradling A., Pardue M. L., Penman S. Messenger RNA in heat-shocked Drosophila cells. J Mol Biol. 1977 Feb 5;109(4):559–587. doi: 10.1016/s0022-2836(77)80091-0. [DOI] [PubMed] [Google Scholar]
  23. Storti R. V., Scott M. P., Rich A., Pardue M. L. Translational control of protein synthesis in response to heat shock in D. melanogaster cells. Cell. 1980 Dec;22(3):825–834. doi: 10.1016/0092-8674(80)90559-0. [DOI] [PubMed] [Google Scholar]
  24. Sutcliffe J. G. Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):77–90. doi: 10.1101/sqb.1979.043.01.013. [DOI] [PubMed] [Google Scholar]
  25. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Velazquez J. M., DiDomenico B. J., Lindquist S. Intracellular localization of heat shock proteins in Drosophila. Cell. 1980 Jul;20(3):679–689. doi: 10.1016/0092-8674(80)90314-1. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Wensink P. C., Finnegan D. J., Donelson J. E., Hogness D. S. A system for mapping DNA sequences in the chromosomes of Drosophila melanogaster. Cell. 1974 Dec;3(4):315–325. doi: 10.1016/0092-8674(74)90045-2. [DOI] [PubMed] [Google Scholar]
  29. 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]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES