Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Sep 1;90(3):793–796. doi: 10.1083/jcb.90.3.793

Heat-shock proteins of Drosophila are associated with nuclease- resistant, high-salt-resistant nuclear structures

PMCID: PMC2111893  PMID: 6793602

Abstract

Proteins produced in cultured Drosophila cells during the heat-shock response (HSPs) were recently shown by autoradiography to be confined in large measure to the cell nucleus. We report here that nuclear HSPs are not associated with nucleosomes solubilizes by treatment with staphylococcal nuclease at low ionic strength nor are HSPs released by extraction with high salt, which solubilized most of the remaining histones and DNA. Possible functions of nuclear HSPs are discussed.

Full Text

The Full Text of this article is available as a PDF (662.8 KB).

Selected References

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

  1. Alfageme C. R., Zweidler A., Mahowald A., Cohen L. H. Histones of Drosophila embryos. Electrophoretic isolation and structural studies. J Biol Chem. 1974 Jun 25;249(12):3729–3736. [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. Augenlicht L. H. Nuclease digestion of RNA in chromatin. Methods Cell Biol. 1977;16:467–472. doi: 10.1016/s0091-679x(08)60121-1. [DOI] [PubMed] [Google Scholar]
  4. Berezney R., Coffey D. S. Nuclear matrix. Isolation and characterization of a framework structure from rat liver nuclei. J Cell Biol. 1977 Jun;73(3):616–637. doi: 10.1083/jcb.73.3.616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biessmann H., Wadsworth S., Levy B., McCarthy B. J. Correlation of structural changes in chromatin with transcription in the Drosophila heat-shock response. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):829–834. doi: 10.1101/sqb.1978.042.01.083. [DOI] [PubMed] [Google Scholar]
  6. Comings D. E., Okada T. A. Nuclear proteins. III. The fibrillar nature of the nuclear matrix. Exp Cell Res. 1976 Dec;103(2):341–360. doi: 10.1016/0014-4827(76)90271-8. [DOI] [PubMed] [Google Scholar]
  7. Gerace L., Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980 Jan;19(1):277–287. doi: 10.1016/0092-8674(80)90409-2. [DOI] [PubMed] [Google Scholar]
  8. Guttman S. D., Glover C. V., Allis C. D., Gorovsky M. A. Heat shock, deciliation and release from anoxia induce the synthesis of the same set of polypeptides in starved T. pyriformis. Cell. 1980 Nov;22(1 Pt 1):299–307. doi: 10.1016/0092-8674(80)90177-4. [DOI] [PubMed] [Google Scholar]
  9. Herman R., Weymouth L., Penman S. Heterogeneous nuclear RNA-protein fibers in chromatin-depleted nuclei. J Cell Biol. 1978 Sep;78(3):663–674. doi: 10.1083/jcb.78.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hodge L. D., Mancini P., Davis F. M., Heywood P. Nuclear matrix of HeLa S3 cells. Polypeptide composition during adenovirus infection and in phases of the cell cycle. J Cell Biol. 1977 Jan;72(1):194–208. doi: 10.1083/jcb.72.1.194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Kelley P. M., Schlesinger M. J. The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell. 1978 Dec;15(4):1277–1286. doi: 10.1016/0092-8674(78)90053-3. [DOI] [PubMed] [Google Scholar]
  14. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Lindquist S. Translational efficiency of heat-induced messages in Drosophila melanogaster cells. J Mol Biol. 1980 Feb 25;137(2):151–158. doi: 10.1016/0022-2836(80)90322-8. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Long B. H., Huang C. Y., Pogo A. O. Isolation and characterization of the nuclear matrix in Friend erythroleukemia cells: chromatin and hnRNA interactions with the nuclear matrix. Cell. 1979 Dec;18(4):1079–1090. doi: 10.1016/0092-8674(79)90221-6. [DOI] [PubMed] [Google Scholar]
  19. McGhee J. D., Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. doi: 10.1146/annurev.bi.49.070180.005343. [DOI] [PubMed] [Google Scholar]
  20. McKenzie S. L., Henikoff S., Meselson M. Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1117–1121. doi: 10.1073/pnas.72.3.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mirault M. E., Goldschmidt-Clermont M., Moran L., Arrigo A. P., Tissières A. The effect of heat shock on gene expression in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):819–827. doi: 10.1101/sqb.1978.042.01.082. [DOI] [PubMed] [Google Scholar]
  22. Mitchell H. K., Lipps L. S. Heat shock and phenocopy induction in Drosophila. Cell. 1978 Nov;15(3):907–918. doi: 10.1016/0092-8674(78)90275-1. [DOI] [PubMed] [Google Scholar]
  23. Mitchell H. K., Lipps L. S. Rapidly labeled proteins on the salivary gland chromosomes of Drosophila melanogaster. Biochem Genet. 1975 Oct;13(9-10):585–602. doi: 10.1007/BF00484917. [DOI] [PubMed] [Google Scholar]
  24. Pardoll D. M., Vogelstein B., Coffey D. S. A fixed site of DNA replication in eucaryotic cells. Cell. 1980 Feb;19(2):527–536. doi: 10.1016/0092-8674(80)90527-9. [DOI] [PubMed] [Google Scholar]
  25. Paulson J. R., Laemmli U. K. The structure of histone-depleted metaphase chromosomes. Cell. 1977 Nov;12(3):817–828. doi: 10.1016/0092-8674(77)90280-x. [DOI] [PubMed] [Google Scholar]
  26. Razin S. V., Mantieva V. L., Georgiev G. P. The similarity of DNA sequences remaining bound to scaffold upon nuclease treatment of interphase nuclei and metaphase chromosomes. Nucleic Acids Res. 1979 Nov 24;7(6):1713–1735. doi: 10.1093/nar/7.6.1713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Riley D. E., Keller J. M. Cell cycle-dependent changes in non-membranous nuclear ghosts from HeLa cells. J Cell Sci. 1978 Feb;29:129–146. doi: 10.1242/jcs.29.1.129. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Thomas J. O., Kornberg R. D. An octamer of histones in chromatin and free in solution. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2626–2630. doi: 10.1073/pnas.72.7.2626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Vincent M., Tanguay R. M. Heat-shock induced proteins present in the cell nucleus of Chironomus tentans salivary gland. Nature. 1979 Oct 11;281(5731):501–503. doi: 10.1038/281501a0. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Wu C., Wong Y. C., Elgin S. C. The chromatin structure of specific genes: II. Disruption of chromatin structure during gene activity. Cell. 1979 Apr;16(4):807–814. doi: 10.1016/0092-8674(79)90096-5. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES