Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1988 Aug 25;16(16):7917–7929. doi: 10.1093/nar/16.16.7917

Mild temperature shock affects transcription of yeast ribosomal protein genes as well as the stability of their mRNAs.

M H Herruer 1, W H Mager 1, H A Raué 1, P Vreken 1, E Wilms 1, R J Planta 1
PMCID: PMC338500  PMID: 3047675

Abstract

Shifting the temperature of a yeast culture from 23 degrees to 36 degrees C results in a sudden and severe (greater than 85%) decline in the cellular levels of ribosomal protein (rp-)mRNAs. Recovery during continued growth at 36 degrees C occurs within 1 h. The use of hybrid genes carrying different portions of the region upstream of the gene coding for ribosomal protein L25 revealed that this characteristic, coordinate temperature shock phenomenon does not depend on the presence of specific upstream DNA sequences. Analysis of a heterologous gene carrying a synthetic UASrpg (upstream activation site of yeast ribosomal protein genes) provided conclusive evidence that the rp-characteristic, transient heat shock response is not mediated through the UASrpg elements. The addition of the transcription inhibitor 1,10-phenantroline prior to a 23 degrees to 36 degrees C heat shock inhibited the severe decline of the rp-mRNA levels. The latter observation indicates that transcription is required for the rp-gene- specific response to heat shock. A milder temperature shift, from 23 degrees to 30 degrees C, gave rise to a two-fold decrease in mRNA levels for all genes studied, both ribosomal and non-ribosomal. Together, these results indicate that a temperature shift causes a temporary general transcriptional arrest in yeast cells, resulting in an over-all decrease in mRNA levels. In addition, an enhanced nucleolytic break-down of pre-existing rp-mRNAs accounts for the dramatic drop in the steady state amounts of these mRNAs observed upon a 23 degrees----36 degrees C shift. This enhanced breakdown is caused directly or indirectly by a factor whose synthesis is induced by the heat shock treatment.

Full text

PDF
7929

Images in this article

Selected References

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

  1. Bell J., Neilson L., Pellegrini M. Effect of heat shock on ribosome synthesis in Drosophila melanogaster. Mol Cell Biol. 1988 Jan;8(1):91–95. doi: 10.1128/mcb.8.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bollen G. H., Molenaar C. M., Cohen L. H., van Raamsdonk-Duin M. M., Mager W. H., Planta R. J. Ribosomal protein genes of yeast contain intervening sequences. Gene. 1982 Apr;18(1):29–37. doi: 10.1016/0378-1119(82)90053-1. [DOI] [PubMed] [Google Scholar]
  3. Bromley S., Hereford L., Rosbash M. Further evidence that the rna2 mutation of Saccharomyces cerevisiae affects mRNA processing. Mol Cell Biol. 1982 Oct;2(10):1205–1211. doi: 10.1128/mcb.2.10.1205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gorenstein C., Warner J. R. Coordinate regulation of the synthesis of eukaryotic ribosomal proteins. Proc Natl Acad Sci U S A. 1976 May;73(5):1547–1551. doi: 10.1073/pnas.73.5.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Guarente L., Lalonde B., Gifford P., Alani E. Distinctly regulated tandem upstream activation sites mediate catabolite repression of the CYC1 gene of S. cerevisiae. Cell. 1984 Feb;36(2):503–511. doi: 10.1016/0092-8674(84)90243-5. [DOI] [PubMed] [Google Scholar]
  6. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  7. Huet J., Cottrelle P., Cool M., Vignais M. L., Thiele D., Marck C., Buhler J. M., Sentenac A., Fromageot P. A general upstream binding factor for genes of the yeast translational apparatus. EMBO J. 1985 Dec 16;4(13A):3539–3547. doi: 10.1002/j.1460-2075.1985.tb04114.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kim C. H., Warner J. R. Messenger RNA for ribosomal proteins in yeast. J Mol Biol. 1983 Mar 25;165(1):79–89. doi: 10.1016/s0022-2836(83)80243-5. [DOI] [PubMed] [Google Scholar]
  9. Kim C. H., Warner J. R. Mild temperature shock alters the transcription of a discrete class of Saccharomyces cerevisiae genes. Mol Cell Biol. 1983 Mar;3(3):457–465. doi: 10.1128/mcb.3.3.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Larkin J. C., Thompson J. R., Woolford J. L., Jr Structure and expression of the Saccharomyces cerevisiae CRY1 gene: a highly conserved ribosomal protein gene. Mol Cell Biol. 1987 May;7(5):1764–1775. doi: 10.1128/mcb.7.5.1764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Leer R. J., Van Raamsdonk-Duin M. M., Mager W. H., Planta R. J. Conserved sequences upstream of yeast ribosomal protein genes. Curr Genet. 1985;9(4):273–277. doi: 10.1007/BF00419955. [DOI] [PubMed] [Google Scholar]
  12. Leer R. J., van Raamsdonk-Duin M. M., Hagendoorn M. J., Mager W. H., Planta R. J. Structural comparison of yeast ribosomal protein genes. Nucleic Acids Res. 1984 Sep 11;12(17):6685–6700. doi: 10.1093/nar/12.17.6685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Leer R. J., van Raamsdonk-Duin M. M., Molenaar C. M., Cohen L. H., Mager W. H., Planta R. J. The structure of the gene coding for the phosphorylated ribosomal protein S10 in yeast. Nucleic Acids Res. 1982 Oct 11;10(19):5869–5878. doi: 10.1093/nar/10.19.5869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Leer R. J., van Raamsdonk-Duin M. M., Schoppink P. J., Cornelissen M. T., Cohen L. H., Mager W. H., Planta R. J. Yeast ribosomal protein S33 is encoded by an unsplit gene. Nucleic Acids Res. 1983 Nov 25;11(22):7759–7768. doi: 10.1093/nar/11.22.7759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lindquist S. Regulation of protein synthesis during heat shock. Nature. 1981 Sep 24;293(5830):311–314. doi: 10.1038/293311a0. [DOI] [PubMed] [Google Scholar]
  16. McAlister L., Finkelstein D. B. Alterations in translatable ribonucleic acid after heat shock of Saccharomyces cerevisiae. J Bacteriol. 1980 Aug;143(2):603–612. doi: 10.1128/jb.143.2.603-612.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller M. J., Xuong N. H., Geiduschek E. P. A response of protein synthesis to temperature shift in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5222–5225. doi: 10.1073/pnas.76.10.5222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miller M. J., Xuong N. H., Geiduschek E. P. Quantitative analysis of the heat shock response of Saccharomyces cerevisiae. J Bacteriol. 1982 Jul;151(1):311–327. doi: 10.1128/jb.151.1.311-327.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nonet M., Scafe C., Sexton J., Young R. Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol. 1987 May;7(5):1602–1611. doi: 10.1128/mcb.7.5.1602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Piper P. W., Curran B., Davies M. W., Lockheart A., Reid G. Transcription of the phosphoglycerate kinase gene of Saccharomyces cerevisiae increases when fermentative cultures are stressed by heat-shock. Eur J Biochem. 1986 Dec 15;161(3):525–531. doi: 10.1111/j.1432-1033.1986.tb10474.x. [DOI] [PubMed] [Google Scholar]
  22. Piper P. W., Curran B., Davies W., Hirst K., Seward K. Saccharomyces cerevisiae mRNA populations of different intrinsic stability in unstressed and heat shocked cells display almost constant m7GpppA:m7GpppG 5'-cap structure ratios. FEBS Lett. 1987 Aug 10;220(1):177–180. doi: 10.1016/0014-5793(87)80898-0. [DOI] [PubMed] [Google Scholar]
  23. Rotenberg M. O., Woolford J. L., Jr Tripartite upstream promoter element essential for expression of Saccharomyces cerevisiae ribosomal protein genes. Mol Cell Biol. 1986 Feb;6(2):674–687. doi: 10.1128/mcb.6.2.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rymond B. C., Zitomer R. S., Schümperli D., Rosenberg M. The expression in yeast of the Escherichia coli galK gene on CYC1::galK fusion plasmids. Gene. 1983 Nov;25(2-3):249–262. doi: 10.1016/0378-1119(83)90229-9. [DOI] [PubMed] [Google Scholar]
  25. Santiago T. C., Purvis I. J., Bettany A. J., Brown A. J. The relationship between mRNA stability and length in Saccharomyces cerevisiae. Nucleic Acids Res. 1986 Nov 11;14(21):8347–8360. doi: 10.1093/nar/14.21.8347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schwindinger W. F., Warner J. R. Transcriptional elements of the yeast ribosomal protein gene CYH2. J Biol Chem. 1987 Apr 25;262(12):5690–5695. [PubMed] [Google Scholar]
  27. Teem J. L., Abovich N., Kaufer N. F., Schwindinger W. F., Warner J. R., Levy A., Woolford J., Leer R. J., van Raamsdonk-Duin M. M., Mager W. H. A comparison of yeast ribosomal protein gene DNA sequences. Nucleic Acids Res. 1984 Nov 26;12(22):8295–8312. doi: 10.1093/nar/12.22.8295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Udem S. A., Warner J. R. Ribosomal RNA synthesis in Saccharomyces cerevisiae. J Mol Biol. 1972 Mar 28;65(2):227–242. doi: 10.1016/0022-2836(72)90279-3. [DOI] [PubMed] [Google Scholar]
  29. Vignais M. L., Woudt L. P., Wassenaar G. M., Mager W. H., Sentenac A., Planta R. J. Specific binding of TUF factor to upstream activation sites of yeast ribosomal protein genes. EMBO J. 1987 May;6(5):1451–1457. doi: 10.1002/j.1460-2075.1987.tb02386.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Warner J. R., Gorenstein C. The synthesis of eucaryotic ribosomal proteins in vitro. Cell. 1977 May;11(1):201–212. doi: 10.1016/0092-8674(77)90331-2. [DOI] [PubMed] [Google Scholar]
  31. Warner J. R., Udem S. A. Temperature sensitive mutations affecting ribosome synthesis in Saccharomyces cerevisiae. J Mol Biol. 1972 Mar 28;65(2):243–257. doi: 10.1016/0022-2836(72)90280-x. [DOI] [PubMed] [Google Scholar]
  32. Woudt L. P., Pastink A., Kempers-Veenstra A. E., Jansen A. E., Mager W. H., Planta R. J. The genes coding for histone H3 and H4 in Neurospora crassa are unique and contain intervening sequences. Nucleic Acids Res. 1983 Aug 25;11(16):5347–5360. doi: 10.1093/nar/11.16.5347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Woudt L. P., Smit A. B., Mager W. H., Planta R. J. Conserved sequence elements upstream of the gene encoding yeast ribosomal protein L25 are involved in transcription activation. EMBO J. 1986 May;5(5):1037–1040. doi: 10.1002/j.1460-2075.1986.tb04319.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zitomer R. S., Walthall D. A., Rymond B. C., Hollenberg C. P. Saccharomyces cerevisiae ribosomes recognize non-AUG initiation codons. Mol Cell Biol. 1984 Jul;4(7):1191–1197. doi: 10.1128/mcb.4.7.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES