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. 1981 Nov;1(11):1016–1023. doi: 10.1128/mcb.1.11.1016

Hierarchy of elements regulating synthesis of ribosomal proteins in Saccharomyces cerevisiae.

D R Kief, J R Warner
PMCID: PMC369723  PMID: 7050662

Abstract

Saccharomyces cerevisiae cells respond to a heat shock by temporarily slowing the synthesis of ribosomal proteins (C. Gorenstein and J. R. Warner, Proc. Natl. Acad. Sci. U.S.A. 73:1574-1551, 1976). When cultures growing oxidatively on ethanol as the sole carbon source were shifted from 23 to 36 degrees C, the synthesis of ribosomal proteins was coordinately inhibited twice as rapidly and 45% more severely than in comparable cultures growing fermentatively on glucose. Within 15 min, the relative rates of synthesis of at least 30 ribosomal proteins declined to less than one-sixth their initial values, whereas the overall rate of protein synthesis increased at least threefold. We suggest that this is due primarily to controls at the level of synthesis of messenger ribonucleic acid for ribosomal proteins but may also involve changes in messenger ribonucleic acid stability. In contrast, a nutritional shift-up causes a stimulation of the synthesis of ribosomal proteins. Experiments designed to determine the hierarchy of stimuli affecting the synthesis of these proteins demonstrated that temperature shock was dominant to glucose stimulation. When a culture growing on ethanol was shifted from 23 to 36 degrees C and glucose was added shortly afterward, the decline in ribosomal protein synthesis continued unabated. However, in wild-type cells ribosomal protein synthesis began to recover within 15 min. In mutants temperature sensitive for ribosome synthesis, e.g., rna2, there was no recovery in the synthesis of most ribosomal proteins, suggesting that the product of rna2 is essential for the production of these proteins under all vegetative conditions.

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Selected References

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

  1. 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]
  2. 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]
  3. Gross K. J., Pogo A. O. Control mechanism of ribonucleic acid synthesis in eukaryotes. The effect of amino acid and glucose starvation and cycloheximide on yeast deoxyribonucleic acid-dependent ribonucleic acid polymerases. J Biol Chem. 1974 Jan 25;249(2):568–576. [PubMed] [Google Scholar]
  4. Hartwell L. H., McLaughlin C. S., Warner J. R. Identification of ten genes that control ribosome formation in yeast. Mol Gen Genet. 1970;109(1):42–56. doi: 10.1007/BF00334045. [DOI] [PubMed] [Google Scholar]
  5. Hereford L. M., Rosbash M. Regulation of a set of abundant mRNA sequences. Cell. 1977 Mar;10(3):463–467. doi: 10.1016/0092-8674(77)90033-2. [DOI] [PubMed] [Google Scholar]
  6. Hermolin J., Zimmerman A. M. RNA synthesis in division synchronized Tetrahymena: macronuclear and cytoplasmic RNA. J Protozool. 1976 Nov;23(4):594–600. doi: 10.1111/j.1550-7408.1976.tb03849.x. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Kief D. R., Warner J. R. Coordinate control of syntheses of ribosomal ribonucleic acid and ribosomal proteins during nutritional shift-up in Saccharomyces cerevisiae. Mol Cell Biol. 1981 Nov;1(11):1007–1015. doi: 10.1128/mcb.1.11.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Lemaux P. G., Herendeen S. L., Bloch P. L., Neidhardt F. C. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell. 1978 Mar;13(3):427–434. doi: 10.1016/0092-8674(78)90317-3. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Pao C. C., Paietta J., Gallant J. A. Synthesis of guanosine tetraphosphate (magic spot I) in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1977 Jan 10;74(1):314–322. doi: 10.1016/0006-291x(77)91410-3. [DOI] [PubMed] [Google Scholar]
  12. Pearson N. J., Haber J. E. Changes in regulation of ribosomal protein synthesis during vegetative growth and sporulation of Saccharomyces cerevisiae. J Bacteriol. 1980 Sep;143(3):1411–1419. doi: 10.1128/jb.143.3.1411-1419.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Rosbash M., Harris P. K., Woolford J. L., Jr, Teem J. L. The effect of temperature-sensitive RNA mutants on the transcription products from cloned ribosomal protein genes of yeast. Cell. 1981 Jun;24(3):679–686. doi: 10.1016/0092-8674(81)90094-5. [DOI] [PubMed] [Google Scholar]
  14. Shulman R. W., Warner J. R. Ribosomal RNA transcription in a mutant of Saccharomyces cerevisiae defective in ribosomal protein synthesis. Mol Gen Genet. 1978 May 3;161(2):221–223. doi: 10.1007/BF00274191. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Walsh C. Appearance of heat shock proteins during the induction of multiple flagella in Naegleria gruberi. J Biol Chem. 1980 Apr 10;255(7):2629–2632. [PubMed] [Google Scholar]
  18. 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]
  19. Warner J. R., Gorenstein C. Yeast has a true stringent response. Nature. 1978 Sep 28;275(5678):338–339. doi: 10.1038/275338a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Yamamori T., Ito K., Nakamura Y., Yura T. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J Bacteriol. 1978 Jun;134(3):1133–1140. doi: 10.1128/jb.134.3.1133-1140.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

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