Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1992 Dec;12(12):5778–5784. doi: 10.1128/mcb.12.12.5778

A mutation in the tRNA nucleotidyltransferase gene promotes stabilization of mRNAs in Saccharomyces cerevisiae.

S W Peltz 1, J L Donahue 1, A Jacobson 1
PMCID: PMC360517  PMID: 1448105

Abstract

To identify trans-acting factors involved in mRNA decay in the yeast Saccharomyces cerevisiae, we have begun to characterize conditional lethal mutants that affect mRNA steady-state levels. A screen of a collection of temperature-sensitive mutants identified ts352, a mutant that accumulated moderately stable and unstable mRNAs after a shift from 23 to 37 degrees C (M. Aebi, G. Kirchner, J.-Y. Chen, U. Vijayraghavan, A. Jacobson, N.C. Martin, and J. Abelson, J. Biol. Chem. 265:16216-16220, 1990). ts352 has a defect in the CCA1 gene, which codes for tRNA nucleotidyltransferase, the enzyme that adds 3' CCA termini to tRNAs (Aebi et al., J. Biol. Chem., 1990). In a shift to the nonpermissive temperature, ts352 (cca1-1) cells rapidly cease protein synthesis, reduce the rates of degradation of the CDC4, TCM1, and PAB1 mRNAs three- to fivefold, and increase the relative number of ribosomes associated with mRNAs and the overall size of polysomes. These results were analogous to those observed for cycloheximide-treated cells and are generally consistent with models that invoke a role for translational elongation in the process of mRNA turnover.

Full text

PDF
5778

Images in this article

Selected References

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

  1. Aebi M., Kirchner G., Chen J. Y., Vijayraghavan U., Jacobson A., Martin N. C., Abelson J. Isolation of a temperature-sensitive mutant with an altered tRNA nucleotidyltransferase and cloning of the gene encoding tRNA nucleotidyltransferase in the yeast Saccharomyces cerevisiae. J Biol Chem. 1990 Sep 25;265(27):16216–16220. [PubMed] [Google Scholar]
  2. Atwater J. A., Wisdom R., Verma I. M. Regulated mRNA stability. Annu Rev Genet. 1990;24:519–541. doi: 10.1146/annurev.ge.24.120190.002511. [DOI] [PubMed] [Google Scholar]
  3. Baim S. B., Pietras D. F., Eustice D. C., Sherman F. A mutation allowing an mRNA secondary structure diminishes translation of Saccharomyces cerevisiae iso-1-cytochrome c. Mol Cell Biol. 1985 Aug;5(8):1839–1846. doi: 10.1128/mcb.5.8.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cleveland D. W. Autoregulated instability of tubulin mRNAs: a novel eukaryotic regulatory mechanism. Trends Biochem Sci. 1988 Sep;13(9):339–343. doi: 10.1016/0968-0004(88)90103-x. [DOI] [PubMed] [Google Scholar]
  5. Cleveland D. W., Yen T. J. Multiple determinants of eukaryotic mRNA stability. New Biol. 1989 Nov;1(2):121–126. [PubMed] [Google Scholar]
  6. Fan H., Penman S. Regulation of protein synthesis in mammalian cells. II. Inhibition of protein synthesis at the level of initiation during mitosis. J Mol Biol. 1970 Jun 28;50(3):655–670. doi: 10.1016/0022-2836(70)90091-4. [DOI] [PubMed] [Google Scholar]
  7. Fort P., Rech J., Vie A., Piechaczyk M., Bonnieu A., Jeanteur P., Blanchard J. M. Regulation of c-fos gene expression in hamster fibroblasts: initiation and elongation of transcription and mRNA degradation. Nucleic Acids Res. 1987 Jul 24;15(14):5657–5667. doi: 10.1093/nar/15.14.5657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gay D. A., Sisodia S. S., Cleveland D. W. Autoregulatory control of beta-tubulin mRNA stability is linked to translation elongation. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5763–5767. doi: 10.1073/pnas.86.15.5763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Graves R. A., Pandey N. B., Chodchoy N., Marzluff W. F. Translation is required for regulation of histone mRNA degradation. Cell. 1987 Feb 27;48(4):615–626. doi: 10.1016/0092-8674(87)90240-6. [DOI] [PubMed] [Google Scholar]
  10. Hentze M. W. Determinants and regulation of cytoplasmic mRNA stability in eukaryotic cells. Biochim Biophys Acta. 1991 Nov 11;1090(3):281–292. doi: 10.1016/0167-4781(91)90191-n. [DOI] [PubMed] [Google Scholar]
  11. Herrick D., Jacobson A. A coding region segment is necessary, but not sufficient for rapid decay of the HIS3 mRNA in yeast. Gene. 1992 May 1;114(1):35–41. doi: 10.1016/0378-1119(92)90704-s. [DOI] [PubMed] [Google Scholar]
  12. Herrick D., Parker R., Jacobson A. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2269–2284. doi: 10.1128/mcb.10.5.2269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jimenez A., Tipper D. J., Davies J. Mode of action of thiolutin, an inhibitor of macromolecular synthesis in Saccharomyces cerevisiae. Antimicrob Agents Chemother. 1973 Jun;3(6):729–738. doi: 10.1128/aac.3.6.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kelly K., Cochran B. H., Stiles C. D., Leder P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell. 1983 Dec;35(3 Pt 2):603–610. doi: 10.1016/0092-8674(83)90092-2. [DOI] [PubMed] [Google Scholar]
  15. Leeds P., Peltz S. W., Jacobson A., Culbertson M. R. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 1991 Dec;5(12A):2303–2314. doi: 10.1101/gad.5.12a.2303. [DOI] [PubMed] [Google Scholar]
  16. Lodish H. F. Alpha and beta globin messenger ribonucleic acid. Different amounts and rates of initiation of translation. J Biol Chem. 1971 Dec 10;246(23):7131–7138. [PubMed] [Google Scholar]
  17. Mahadevan L. C., Edwards D. R. Signalling and superinduction. Nature. 1991 Feb 28;349(6312):747–748. doi: 10.1038/349747c0. [DOI] [PubMed] [Google Scholar]
  18. Mahadevan L. C., Willis A. C., Barratt M. J. Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell. 1991 May 31;65(5):775–783. doi: 10.1016/0092-8674(91)90385-c. [DOI] [PubMed] [Google Scholar]
  19. Manrow R. E., Jacobson A. Identification and characterization of developmentally regulated mRNP proteins of Dictyostelium discoideum. Dev Biol. 1986 Jul;116(1):213–227. doi: 10.1016/0012-1606(86)90058-8. [DOI] [PubMed] [Google Scholar]
  20. Parker R., Herrick D., Peltz S. W., Jacobson A. Measurement of mRNA decay rates in Saccharomyces cerevisiae. Methods Enzymol. 1991;194:415–423. doi: 10.1016/0076-6879(91)94032-8. [DOI] [PubMed] [Google Scholar]
  21. Parker R., Jacobson A. Translation and a 42-nucleotide segment within the coding region of the mRNA encoded by the MAT alpha 1 gene are involved in promoting rapid mRNA decay in yeast. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2780–2784. doi: 10.1073/pnas.87.7.2780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Peltz S. W., Brewer G., Bernstein P., Hart P. A., Ross J. Regulation of mRNA turnover in eukaryotic cells. Crit Rev Eukaryot Gene Expr. 1991;1(2):99–126. [PubMed] [Google Scholar]
  23. Peltz S. W., Brewer G., Groppi V., Ross J. Exonuclease activity that degrades histone mRNA is stable when DNA or protein synthesis is inhibited. Mol Biol Med. 1989 Jun;6(3):227–238. [PubMed] [Google Scholar]
  24. Peltz S. W., Brewer G., Kobs G., Ross J. Substrate specificity of the exonuclease activity that degrades H4 histone mRNA. J Biol Chem. 1987 Jul 5;262(19):9382–9388. [PubMed] [Google Scholar]
  25. Rose J. K., Lodish H. F. Translation in vitro of vesicular stomatitis virus mRNA lacking 5'-terminal 7-methylguanosine. Nature. 1976 Jul 1;262(5563):32–37. doi: 10.1038/262032a0. [DOI] [PubMed] [Google Scholar]
  26. Ross J. Messenger RNA turnover in eukaryotic cells. Mol Biol Med. 1988 Feb;5(1):1–14. [PubMed] [Google Scholar]
  27. Shyu A. B., Greenberg M. E., Belasco J. G. The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 1989 Jan;3(1):60–72. doi: 10.1101/gad.3.1.60. [DOI] [PubMed] [Google Scholar]
  28. Stimac E., Groppi V. E., Jr, Coffino P. Inhibition of protein synthesis stabilizes histone mRNA. Mol Cell Biol. 1984 Oct;4(10):2082–2090. doi: 10.1128/mcb.4.10.2082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tipper D. J. Inhibition of yeast ribonucleic acid polymerases by thiolutin. J Bacteriol. 1973 Oct;116(1):245–256. doi: 10.1128/jb.116.1.245-256.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wisdom R., Lee W. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev. 1991 Feb;5(2):232–243. doi: 10.1101/gad.5.2.232. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES