Skip to main content
SpringerLink
Log in

The expression of heat shock genes during normal development in Drosophila melanogaster (heat shock/abundant transcripts/developmental regulation)

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

Drosophila melanogaster cells and tissues respond to heat shock by dramatically altering their pattern of transcription and translation, leading to the rapid synthesis of a small number of polypeptides, the heat shock proteins (hsps). By using cloned hsp DNA we have detected sequences complementary to heat shock genes in RNA prepared from non-heat-shocked animals of different developmental stages. Hsp 83 mRNA is present at high levels in all stages examined. Hsp 68 and 70 mRNAs are present at very low levels in most stages and at slightly higher concentration in pupae. Hsp 26 and 27 mRNAs are detected in embryos. Hsp 23, 26 and 27 mRNA are barely detectable in early third instar larvae but are major components of late third instar and early pupal RNA. Hsp 22 mRNA is also detected in early pupae. Later in development the levels of the small hsp mRNAs decrease but a further peak in abundance of hsp 26 and 27 mRNAs is found in mature adult females.

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

References

  • Arrigo AP (1980) Investigation of the function of the heat shock proteins in Drosophila melanogaster tissue culture cells. Mol Gen Genet 178:517–524

    PubMed  Google Scholar 

  • Ashburner M, Bonner JJ (1979) The induction of gene activity in Drosophila by heat shock. Cell 17:241–254

    Article  Google Scholar 

  • Biessmann H, Craig EA, McCarthy BJ (1979) Rapid quantitation of individual RNA species in a complex population. Nucl Acids Res 7:981–996

    PubMed  Google Scholar 

  • Cheney CM, Shearn A (1983) Developmental regulation of Drosophila imaginal disc proteins: synthesis of heat shock proteins under non-heat shock conditions. Dev Biol 95:325–330

    PubMed  Google Scholar 

  • Corces V, Holmgren R, Freund R, Morimoto R, Meselson M (1980) Four heat shock proteins of Drosophila melanogaster coded with a a 12-kilobase region in chromosome subdivision 67B. Proc Natl Acad Sci USA 77:5390–5393

    PubMed  Google Scholar 

  • Craig EA, McCarthy BJ (1980) Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucl Acids Res 8:4441–4457

    PubMed  Google Scholar 

  • Craig E, Ingolia T, Slater M, Manseau L, Bardwell J (1982) Drosophila and yeast multigene families related to the Drosophila heat-shock genes. In: Schlesinger MJ (ed) Heat shock from bacteria to man. Cold Spring Harbor Laboratory. New York, pp 11–18

    Google Scholar 

  • Fyrberg E, Kindle K, Davidson N, Sodja A (1980) The actin genes of Drosophila: a dispersed multigene family. Cell 19:365–378

    Article  Google Scholar 

  • Fyrberg EA, Bond BJ, Hershey DN, Mixter KS, Davidson N (1981) The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell 24:107–116

    Article  Google Scholar 

  • Goldschmidt-Clermont M (1980) Two genes for the major heatshock protein of Drosophila melanogaster arranged as an inverted repeat. Nucl Acids Res 8:235–252

    PubMed  Google Scholar 

  • Hall LMC, Mason PJ, Spierer P (1983) Transcripts, genes and bands in 315,000 base-pairs of Drosophila DNA. J Mol Biol 169:83–96

    PubMed  Google Scholar 

  • Handler AM (1982) Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev Biol 93:73–82

    PubMed  Google Scholar 

  • Holmgren R, Livak K, Morimoto R, Freund R, Meselson M (1979) Studies of cloned sequences from four Drosophila heat shock loci. Cell 18:1359–1370

    PubMed  Google Scholar 

  • Holmgren R, Corces V, Mormoto R, Blackman R, Meselson M (1981) Sequence homologies in the 5′ regions of four Drosophila heat-shock genes. Proc Natl Acad Sci USA 78:3775–3778

    PubMed  Google Scholar 

  • Hughes EN, August TJ (1982) Coprecipitation of heat shock proteins with a cell surface glycoprotein. Proc Natl Acad Sci USA 79:2305–2309

    PubMed  Google Scholar 

  • Ingolia TD, Craig EA (1982a) Drosophila gene related to the major heat shock-induced gene is transcribed at normal temperatures and non induced by heat shock. Proc Natl Acad Sci USA 79:525–529

    PubMed  Google Scholar 

  • Ingolia TD, Craig EA (1982b) Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79:2360–2364

    PubMed  Google Scholar 

  • Ingolia TD, Craig EA, McCarthy BJ (1980) Sequence of three copies of the gene for the major Drosophila heat shock induced protein and their flanking regions. Cell 21:669–679

    PubMed  Google Scholar 

  • Ireland RC, Berger EM (1982) Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. Proc Natl Acad Sci USA 79:855–859

    PubMed  Google Scholar 

  • Ireland RC, Berger E, Sirotkin K, Yund MA, Osterbur D, Fristrom J (1982) Ecdysterone induces the transcription of four heat-shock genes in Drosophila S3 cells and imaginal discs. Dev Biol 93:498–507

    PubMed  Google Scholar 

  • Karch F, Török I, Tissières A (1981) Extensive regions of homology in front of the two hsp 70 heat shock variant genes in Drosophila melanogaster. J Mol Biol 148:219–230

    PubMed  Google Scholar 

  • Kelley PM, Schlesinger MJ (1982) Antibodies to two major chicken heat shock proteins cross react with similar proteins in widely divergent species. Mol Cell Biol 2:267–274

    PubMed  Google Scholar 

  • Kemp DJ, Thomson JA, Peacock VJ, Higgins TJV (1978) Messenger RNA for the insect storage protein calliphorine: in vitro translation and chromosomal hybridization analysis of a 20S poly(A)-RNA fraction. Biochem Genet 16:355–371

    PubMed  Google Scholar 

  • McKenzie SL, Henikoff S, Meselson M (1975) Localization of RNA from heat-induced polysomes at fuff sites in Drosophila melanogaster. Proc Natl Acad Sci USA 72:1117–1121

    PubMed  Google Scholar 

  • Mirault ME, Goldschmidt-Clermont M, Arrigo PA, Tissières A (1978) The effect of heat shock on gene expression in Drosophila melanogaster. Cold Spring Harbor Symp Quant Biol 42:819–827

    PubMed  Google Scholar 

  • Mitchell HK, Lipps LS (1975) Rapidly labelled proteins on the salivary gland chromosomes of Drosophila melanogaster. Biochem Genet 13:585–602

    PubMed  Google Scholar 

  • O'Connor D, Lis JT (1981) Two closely linked transcription units within the 63B heat shock puff locus of D. melanogaster display strikingly different regulation. Nucl Acids Res 9:5075–5092

    PubMed  Google Scholar 

  • Schlesinger MJ, Ashburner M, Tissières A, eds (1982) Heat shock from bacteria to man. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Sirotkin K, Davidson N (1982) Developmentally regulated transcription from Drosophila melanogaster site 67B. Dev Biol 89:196–210

    PubMed  Google Scholar 

  • Southern E (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    PubMed  Google Scholar 

  • Southgate R, Ayme A, Voellmy R (1983) Nucleotide sequence analysis of the Drosophila small heat shock gene cluster at locus 67B. J Mol Biol 165:35–37

    PubMed  Google Scholar 

  • Storti RV, Scott MP, Rich A, Pardue ML (1980) Translational control of protein synthesis in response to heat shock in D. melanogaster cells. Cell 22:825–834

    Article  Google Scholar 

  • Tissières A, Mitchell HK, Tracy UM (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 84:389–398

    PubMed  Google Scholar 

  • Török I, Karch F (1980) Nucleotide sequence of heat shock activated genes in Drosophila melanogaster. I. Sequences in the region of the 5′ and 3′ ends of the hsp 70 gene in the hybrid plasmid 56H8. Nucl Acids Res 8:3105–3123

    PubMed  Google Scholar 

  • Velazquez JM, Sonoda S, Bugaisky G, Lindquist S (1983) Is the major Drosophila heat shock protein present in cells that have not been heat shocked. J Cell Biol 96:286–290

    Article  Google Scholar 

  • Voellmy R, Goldschmidt-Clermont M, Southgate R, Tissières A, Levis R, Gehring WJ (1981) A DNA segment isolated from chromosomal site 67B in D. melanogaster contains four closely linked heat-shock genes. Cell 23:261–270

    Article  PubMed  Google Scholar 

  • Voellmy R, Bromley P, Kocher HP (1983) Structural similarities between corresponding heat-shock proteins from different eucaryotic cells. J Biol Chem 258:3516–3522

    PubMed  Google Scholar 

  • Wadsworth SC (1982) A family of related proteins is encoded by the major Drosophila heat shock gene family. Mol Cell Biol 2:286–292

    PubMed  Google Scholar 

  • Wang C, Gomer RH, Lazarides E (1981) Heat shock proteins are methylated in avian and mammalian cells. Proc Natl Acad Sci USA 78:3531–3535

    PubMed  Google Scholar 

  • Zimmerman JL, Petri W, Meselson M (1983) Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32:1161–1170

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. P. J. Mason

    Present address: Imperial Cancer Research Fund, Mill Hill Laboratories, Burtonhole Lane, NW7 1AD, London, England

  2. J. Gausz

    Present address: Institute of Genetics, Hungarian Academy of Sciences, P.O.B. 521, Szeged, Hungary

Authors and Affiliations

  1. Department of Molecular Biology, University of Geneva, 30, quai Ernest-Ansermet, CH-1211, Geneva 4, Switzerland

    P. J. Mason, L. M. C. Hall & J. Gausz

  2. Department of Animal Biology, 154, rte de Malagnou, CH-1224 Chêne, Bougeries, Switzerland

    J. Gausz

Authors
  1. P. J. Mason
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. M. C. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Gausz
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated W. Gehring

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mason, P.J., Hall, L.M.C. & Gausz, J. The expression of heat shock genes during normal development in Drosophila melanogaster (heat shock/abundant transcripts/developmental regulation). Molec. Gen. Genet. 194, 73–78 (1984). https://doi.org/10.1007/BF00383500

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00383500

Keywords

Search

Navigation