Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1984 Jul 25;12(14):5719–5735. doi: 10.1093/nar/12.14.5719

Transcription, export and turnover of Hsp70 and alpha beta, two Drosophila heat shock genes sharing a 400 nucleotide 5' upstream region.

J A Lengyel, M L Graham
PMCID: PMC320026  PMID: 6431397

Abstract

A highly homologous 400 nucleotide sequence flanks the 5' end and extends 64 NT into the transcribed portion of all five hsp70 and seven alpha beta heat shock genes in Drosophila melanogaster (1-4). To determine the extent to which this sequence dictates coordinate regulation, we compared the total mass, continuous labeling and pulse-labeling of hsp70 and alpha beta RNAs at different times and temperatures of heat shock. By all these measurements, expression of both hsp70 and alpha beta genes increased and decreased in parallel. Hsp70 RNA was generally synthesized at a higher rate and accumulated to a greater extent than alpha beta RNA. As the temperature of heat shock increased, however, the rate of synthesis and accumulation of hsp70 relative to alpha beta RNA decreased. Another difference was that a larger fraction of hsp 70, as compared to alpha beta RNA was exported from the nucleus. For both RNAs, export decreased as the heat shock temperature was increased. The hsp70 and alpha beta genes are thus expressed in parallel, but the homologous 5' upstream sequences do not dictate equal rates of transcription or export from the nucleus.

Full text

PDF
5719

Images in this article

5723Image
on p.5723

Selected References

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

  1. Anderson K. V., Lengyel J. A. Changing rates of histone mRNA synthesis and turnover in Drosophila embryos. Cell. 1980 Oct;21(3):717–727. doi: 10.1016/0092-8674(80)90435-3. [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. 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]
  4. Babich A., Feldman L. T., Nevins J. R., Darnell J. E., Jr, Weinberger C. Effect of adenovirus on metabolism of specific host mRNAs: transport control and specific translational discrimination. Mol Cell Biol. 1983 Jul;3(7):1212–1221. doi: 10.1128/mcb.3.7.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caggese C., Caizzi R., Morea M., Scalenghe F., Ritossa F. Mutation generating a fragment of the major heat shock-inducible polypeptide in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 May;76(5):2385–2389. doi: 10.1073/pnas.76.5.2385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Corces V., Pellicer A., Axel R., Meselson M. Integration, transcription, and control of a Drosophila heat shock gene in mouse cells. Proc Natl Acad Sci U S A. 1981 Nov;78(11):7038–7042. doi: 10.1073/pnas.78.11.7038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Craig E. A., Ingolia T. D., Manseau L. J. Expression of Drosophila heat-shock cognate genes during heat shock and development. Dev Biol. 1983 Oct;99(2):418–426. doi: 10.1016/0012-1606(83)90291-9. [DOI] [PubMed] [Google Scholar]
  8. DiDomenico B. J., Bugaisky G. E., Lindquist S. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell. 1982 Dec;31(3 Pt 2):593–603. doi: 10.1016/0092-8674(82)90315-4. [DOI] [PubMed] [Google Scholar]
  9. Falkenthal S., Graham M. L., Korn E. L., Lengyel J. A. Transcription, processing, and turnover of RNA from the Drosophila mobile genetic element copia. Dev Biol. 1982 Aug;92(2):294–305. doi: 10.1016/0012-1606(82)90176-2. [DOI] [PubMed] [Google Scholar]
  10. Falkenthal S., Lengyel J. A. Structure, translation, and metabolism of the cytoplasmic copia ribonucleic acid of Drosophila melanogaster. Biochemistry. 1980 Dec 9;19(25):5842–5850. doi: 10.1021/bi00566a028. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Hackett R. W., Lis J. T. DNA sequence analysis reveals extensive homologies of regions preceding hsp70 and alphabeta heat shock genes in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6196–6200. doi: 10.1073/pnas.78.10.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmgren R., Corces V., Morimoto R., Blackman R., Meselson M. Sequence homologies in the 5' regions of four Drosophila heat-shock genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3775–3778. doi: 10.1073/pnas.78.6.3775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Ingolia T. D., Craig E. A., McCarthy B. J. Sequence of three copies of the gene for the major Drosophila heat shock induced protein and their flanking regions. Cell. 1980 Oct;21(3):669–679. doi: 10.1016/0092-8674(80)90430-4. [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. Ish-Horowicz D., Pinchin S. M. Genomic organization of the 87A7 and 87Cl heat-induced loci of Drosophila melanogaster. J Mol Biol. 1980 Sep 15;142(2):231–245. doi: 10.1016/0022-2836(80)90047-9. [DOI] [PubMed] [Google Scholar]
  18. Jacq B., Jourdan R., Jordan B. R. Structure and processing of precursor 5 S RNA in Drosophila melanogaster. J Mol Biol. 1977 Dec 15;117(3):785–795. doi: 10.1016/0022-2836(77)90069-9. [DOI] [PubMed] [Google Scholar]
  19. Kafatos F. C. The cocoonase zymogen cells of silk moths: a model of terminal cell differentiation for specific protein synthesis. Curr Top Dev Biol. 1972;7:125–191. doi: 10.1016/s0070-2153(08)60071-x. [DOI] [PubMed] [Google Scholar]
  20. Kao H. T., Nevins J. R. Transcriptional activation and subsequent control of the human heat shock gene during adenovirus infection. Mol Cell Biol. 1983 Nov;3(11):2058–2065. doi: 10.1128/mcb.3.11.2058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Karch F., Török I., Tissières A. Extensive regions of homology in front of the two hsp70 heat shock variant genes in Drosophila melanogaster. J Mol Biol. 1981 May 25;148(3):219–230. doi: 10.1016/0022-2836(81)90536-2. [DOI] [PubMed] [Google Scholar]
  22. Kunkel N. S., Weinberg E. S. Histone gene transcripts in the cleavage and mesenchyme blastula embryo of the sea urchin, S. purpuratus. Cell. 1978 Jun;14(2):313–326. doi: 10.1016/0092-8674(78)90117-4. [DOI] [PubMed] [Google Scholar]
  23. Lengyel J. A., Ransom L. J., Graham M. L., Pardue M. L. Transcription and metabolism of RNA from the Drosophila melanogaster heat shock puff site 93D. Chromosoma. 1980;80(3):237–252. doi: 10.1007/BF00292683. [DOI] [PubMed] [Google Scholar]
  24. Lengyel J., Penman S. hnRNA size and processing as related to different DNA content in two dipterans: Drosophila and Aedes. Cell. 1975 Jul;5(3):281–290. doi: 10.1016/0092-8674(75)90103-8. [DOI] [PubMed] [Google Scholar]
  25. Lengyel J., Spradling A., Penman S. Methods with insect cells in suspension culture. II. Drosophila melanogaster. Methods Cell Biol. 1975;10:195–208. doi: 10.1016/s0091-679x(08)60738-4. [DOI] [PubMed] [Google Scholar]
  26. Levis R., Penman S. The metabolism of poly (A)+ and poly(A)-hnRNA in cultured Drosophila cells studied with a rapid uridine pulse-chase. Cell. 1977 May;11(1):105–113. doi: 10.1016/0092-8674(77)90321-x. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Lis J. T., Ish-Horowicz D., Pinchin S. M. Genomic organization and transcription of the alpha beta heat shock DNA in Drosophila melanogaster. Nucleic Acids Res. 1981 Oct 24;9(20):5297–5310. doi: 10.1093/nar/9.20.5297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Maxson R. E., Wu R. S. A simple method for measuring specific radioactivities of ribonucleoside triphosphates using RNA polymerase. Eur J Biochem. 1976 Mar 1;62(3):551–554. doi: 10.1111/j.1432-1033.1976.tb10189.x. [DOI] [PubMed] [Google Scholar]
  34. Mayrand S., Pederson T. Heat shock alters nuclear ribonucleoprotein assembly in Drosophila cells. Mol Cell Biol. 1983 Feb;3(2):161–171. doi: 10.1128/mcb.3.2.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Moran L. A., Chauvin M., Kennedy M. E., Korri M., Lowe D. G., Nicholson R. C., Perry M. D. The major heat-shock protein (hsp70) gene family: related sequences in mouse, Drosophila, and yeast. Can J Biochem Cell Biol. 1983 Jun;61(6):488–499. doi: 10.1139/o83-065. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Rozek C. E., Davidson N. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell. 1983 Jan;32(1):23–34. doi: 10.1016/0092-8674(83)90493-2. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. 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]
  42. 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]
  43. 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]
  44. Udvardy A., Sümegi J., Tóth E. C., Gausz J., Gyurkovics H., Schedl P., Ish-Horowicz D. Genomic organization and functional analysis of a deletion variant of the 87A7 heat shock locus of Drosophila melanogaster. J Mol Biol. 1982 Mar 5;155(3):267–280. doi: 10.1016/0022-2836(82)90005-5. [DOI] [PubMed] [Google Scholar]

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

RESOURCES