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. 1994 Nov;176(22):7126–7128. doi: 10.1128/jb.176.22.7126-7128.1994

SPE1 and SPE2: two essential genes in the biosynthesis of polyamines that modulate +1 ribosomal frameshifting in Saccharomyces cerevisiae.

D Balasundaram 1, J D Dinman 1, C W Tabor 1, H Tabor 1
PMCID: PMC197094  PMID: 7961484

Abstract

We previously showed that a mutant of Saccharomyces cerevisiae, which cannot make spermidine as a result of a deletion in the SPE2 gene (spe2 delta), exhibits a marked elevation in +1 ribosomal frameshifting efficiency in response to the Ty1 frameshift sequence, CUU AGG C. In the present study, we found that spermidine deprivation alone does not result in increased +1 ribosomal frameshifting efficiency. The high level of +1 ribosomal frameshifting efficiency in spe2 delta cells is the result of the combined effects of both spermidine deprivation and the large increase in the level of intracellular putrescine resulting from the derepression of the gene for ornithine decarboxylase (SPE1) in spermidine-deficient strains.

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Selected References

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  1. Atkins J. F., Weiss R. B., Gesteland R. F. Ribosome gymnastics--degree of difficulty 9.5, style 10.0. Cell. 1990 Aug 10;62(3):413–423. doi: 10.1016/0092-8674(90)90007-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balasundaram D., Dinman J. D., Wickner R. B., Tabor C. W., Tabor H. Spermidine deficiency increases +1 ribosomal frameshifting efficiency and inhibits Ty1 retrotransposition in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):172–176. doi: 10.1073/pnas.91.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Balasundaram D., Tabor C. W., Tabor H. Spermidine or spermine is essential for the aerobic growth of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5872–5876. doi: 10.1073/pnas.88.13.5872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belcourt M. F., Farabaugh P. J. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990 Jul 27;62(2):339–352. doi: 10.1016/0092-8674(90)90371-K. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cohn M. S., Tabor C. W., Tabor H. Isolation and characterization of Saccharomyces cerevisiae mutants deficient in S-adenosylmethionine decarboxylase, spermidine, and spermine. J Bacteriol. 1978 Apr;134(1):208–213. doi: 10.1128/jb.134.1.208-213.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dinman J. D., Wickner R. B. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J Virol. 1992 Jun;66(6):3669–3676. doi: 10.1128/jvi.66.6.3669-3676.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dinman J. D., Wickner R. B. Translational maintenance of frame: mutants of Saccharomyces cerevisiae with altered -1 ribosomal frameshifting efficiencies. Genetics. 1994 Jan;136(1):75–86. doi: 10.1093/genetics/136.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Farabaugh P. J. Alternative readings of the genetic code. Cell. 1993 Aug 27;74(4):591–596. doi: 10.1016/0092-8674(93)90507-M. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Farabaugh P. J., Zhao H., Vimaladithan A. A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell. 1993 Jul 16;74(1):93–103. doi: 10.1016/0092-8674(93)90297-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fonzi W. A., Sypherd P. S. Expression of the gene for ornithine decarboxylase of Saccharomyces cerevisiae in Escherichia coli. Mol Cell Biol. 1985 Jan;5(1):161–166. doi: 10.1128/mcb.5.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gallant J., Lindsley D. Ribosome frameshifting at hungry codons: sequence rules, directional specificity and possible relationship to mobile element behaviour. Biochem Soc Trans. 1993 Nov;21(4):817–821. doi: 10.1042/bst0210817. [DOI] [PubMed] [Google Scholar]
  12. Gesteland R. F., Weiss R. B., Atkins J. F. Recoding: reprogrammed genetic decoding. Science. 1992 Sep 18;257(5077):1640–1641. doi: 10.1126/science.1529352. [DOI] [PubMed] [Google Scholar]
  13. Goldemberg S. H., Fernandez-Velasco J. G., Algranati I. D. Differential binding of streptomycin to ribosomes of polyamine-deficient bacteria grown in the absence and presence of putrescine. FEBS Lett. 1982 Jun 7;142(2):275–279. doi: 10.1016/0014-5793(82)80151-8. [DOI] [PubMed] [Google Scholar]
  14. Guarino L. A., Cohen S. S. Mechanism of toxicity of putrescine in Anacystis nidulans. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3660–3664. doi: 10.1073/pnas.76.8.3660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hatfield D., Oroszlan S. The where, what and how of ribosomal frameshifting in retroviral protein synthesis. Trends Biochem Sci. 1990 May;15(5):186–190. doi: 10.1016/0968-0004(90)90159-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kawakami K., Pande S., Faiola B., Moore D. P., Boeke J. D., Farabaugh P. J., Strathern J. N., Nakamura Y., Garfinkel D. J. A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae. Genetics. 1993 Oct;135(2):309–320. doi: 10.1093/genetics/135.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rom E., Kahana C. Polyamines regulate the expression of ornithine decarboxylase antizyme in vitro by inducing ribosomal frame-shifting. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3959–3963. doi: 10.1073/pnas.91.9.3959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rosano C. L., Bunce S. C., Hurwitz C. Localization of polyamine enhancement of protein synthesis to subcellular components of Escherichia coli and Pseudomonas sp. strain Kim. J Bacteriol. 1983 Jan;153(1):326–334. doi: 10.1128/jb.153.1.326-334.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rosano C. L., Hurwitz C. Antagonistic action between spermidine and putrescine on association and dissociation of purified, run-off ribosomes from Escherichia coli. J Biol Chem. 1977 Jan 25;252(2):652–654. [PubMed] [Google Scholar]
  20. Tyagi A. K., Tabor C. W., Tabor H. Ornithine decarboxylase from Saccharomyces cerevisiae. Purification, properties, and regulation of activity. J Biol Chem. 1981 Dec 10;256(23):12156–12163. [PubMed] [Google Scholar]
  21. Vernet T., Dignard D., Thomas D. Y. A family of yeast expression vectors containing the phage f1 intergenic region. Gene. 1987;52(2-3):225–233. doi: 10.1016/0378-1119(87)90049-7. [DOI] [PubMed] [Google Scholar]
  22. Xie Q. W., Tabor C. W., Tabor H. Ornithine decarboxylase in Saccharomyces cerevisiae: chromosomal assignment and genetic mapping of the SPE1 gene. Yeast. 1990 Nov-Dec;6(6):455–460. doi: 10.1002/yea.320060602. [DOI] [PubMed] [Google Scholar]
  23. Xu H., Boeke J. D. Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Ty1 transposition frequency. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8360–8364. doi: 10.1073/pnas.87.21.8360. [DOI] [PMC free article] [PubMed] [Google Scholar]

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