Home LiteratureArticle Details
PMID: 8278359 Published · ppublish English Journal Article

Spermidine deficiency increases +1 ribosomal frameshifting efficiency and inhibits Ty1 retrotransposition in Saccharomyces cerevisiae.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 91 ·No. 1 ·1994-01-04 ·Pages 172-6

Balasundaram D, Dinman JD, Wickner RB, Tabor CW, Tabor H

Abstract

Polyamines have been implicated in nucleic acid-related functions and in protein biosynthesis. RNA sequences that specifically direct ribosomes to shift reading frame in the -1 and +1 directions may be used to probe the mechanisms controlling translational fidelity. We examined the effects of spermidine on translational fidelity by an in vivo assay in which changes in beta-galactosidase activity are dependent on yeast retrovirus Ty +1 and yeast double-stranded RNA virus L-A -1 ribosomal frameshifting signals. In spe2 delta mutants of Saccharomyces cerevisiae, which cannot make spermidine as a result of a deletion in the SPE2 gene, there is a marked elevation in +1 but no change in -1 ribosomal frameshifting. The increase in +1 ribosomal frameshifting efficiency is accompanied by a striking decrease in Ty1 retrotransposition.

Related Genes
SPE2
MeSH Terms
Adenosylmethionine Decarboxylase Base Sequence DNA Transposable Elements Genes, Suppressor Molecular Sequence Data Oligodeoxyribonucleotides/chemistry Protein Biosynthesis RNA, Transfer, Arg Ribosomes/metabolism Saccharomyces cerevisiae/genetics,metabolism Spermidine/physiology
Chemicals
DNA Transposable Elements Oligodeoxyribonucleotides RNA, Transfer, Arg Adenosylmethionine Decarboxylase Spermidine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Balasundaram D
Laboratory of Biochemical Pharmacology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892.
Dinman J D
Wickner R B
Tabor C W
Tabor H
References (42)
42 references, click to expand
  1. 4-Thiouridine and the conformation of E. coli tRNA induced by spermidine.
    Biochem Biophys Res Commun. 1972 May 26;47(4):720-6 PMID: 4554636
  2. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region.
    Cell. 1988 Nov 4;55(3):447-58 PMID: 2846182
  3. Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs.
    J Mol Biol. 1982 Jul 15;158(4):573-97 PMID: 6750137
  4. Recoding: reprogrammed genetic decoding.
    Science. 1992 Sep 18;257(5077):1640-1 PMID: 1529352
  5. Synonymous codon usage in Saccharomyces cerevisiae.
    Yeast. 1991 Oct;7(7):657-78 PMID: 1776357
  6. Localized mutagenesis and evidence for post-transcriptional regulation of MAK3. A putative N-acetyltransferase required for double-stranded RNA virus propagation in Saccharomyces cerevisiae.
    J Biol Chem. 1992 Oct 5;267(28):20270-6 PMID: 1339437
  7. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site.
    Cell. 1990 Jul 27;62(2):339-52 PMID: 2164889
  8. Translational suppression in gene expression in retroviruses and retrotransposons.
    Curr Top Microbiol Immunol. 1990;157:93-124 PMID: 2168307
  9. Polyamine requirement for efficient translation of amber codons in vivo.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7087-91 PMID: 6760189
  10. Aminoacyl transfer RNA formation. I. Absence of pyrophosphate-ATP exchange in aminoacyl-tRNA formation stimulated by polyamines.
    Biochim Biophys Acta. 1971 Nov 29;254(1):91-103 PMID: 4332417
  11. The mechanism of aminoacylation of transfer ribonucleic acid. The role of magnesium and spermine in the synthesis of isoleucyl-tRNA.
    J Biol Chem. 1978 Oct 10;253(19):6702-10 PMID: 357429
  12. Polyamine--DNA nexus: structural ramifications and biological implications.
    Mol Cell Biochem. 1991 Feb 2;100(2):129-40 PMID: 2008175
  13. Spermidine biosynthesis in Saccharomyces cerevisiae. Biosynthesis and processing of a proenzyme form of S-adenosylmethionine decarboxylase.
    J Biol Chem. 1990 Dec 25;265(36):22321-8 PMID: 2266128
  14. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot.
    Cell. 1989 May 19;57(4):537-47 PMID: 2720781
  15. Polyamines in microorganisms.
    Microbiol Rev. 1985 Mar;49(1):81-99 PMID: 3157043
  16. The where, what and how of ribosomal frameshifting in retroviral protein synthesis.
    Trends Biochem Sci. 1990 May;15(5):186-90 PMID: 2193436
  17. Polyamines.
    Annu Rev Biochem. 1984;53:749-90 PMID: 6206782
  18. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767-71 PMID: 3474623
  19. 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):8360-4 PMID: 2172984
  20. Ty element-induced temperature-sensitive mutations of Saccharomyces cerevisiae.
    Genetics. 1992 Aug;131(4):821-32 PMID: 1325386
  21. RNA pseudoknots: translational frameshifting and readthrough on viral RNAs.
    Virus Genes. 1990 Jul;4(2):121-36 PMID: 2402881
  22. 1,4-Diaminobutane (putrescine), spermidine, and spermine.
    Annu Rev Biochem. 1976;45:285-306 PMID: 786151
  23. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  24. Double-stranded RNA virus replication and packaging.
    J Biol Chem. 1993 Feb 25;268(6):3797-800 PMID: 8440674
  25. A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):174-8 PMID: 1986362
  26. Oxygen toxicity in a polyamine-depleted spe2 delta mutant of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4693-7 PMID: 8506320
  27. Isolation and characterization of Saccharomyces cerevisiae mutants deficient in S-adenosylmethionine decarboxylase, spermidine, and spermine.
    J Bacteriol. 1978 Apr;134(1):208-13 PMID: 348678
  28. Ty elements transpose through an RNA intermediate.
    Cell. 1985 Mar;40(3):491-500 PMID: 2982495
  29. On the directional specificity of ribosome frameshifting at a "hungry" codon.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5469-73 PMID: 8516288
  30. SPERMIDINE, SPERMINE, AND RELATED AMINES.
    Pharmacol Rev. 1964 Sep;16:245-300 PMID: 14211123
  31. Double-stranded and single-stranded RNA viruses of Saccharomyces cerevisiae.
    Annu Rev Microbiol. 1992;46:347-75 PMID: 1444259
  32. Ribosomal frameshifting from -2 to +50 nucleotides.
    Prog Nucleic Acid Res Mol Biol. 1990;39:159-83 PMID: 2247607
  33. A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae.
    Genetics. 1993 Oct;135(2):309-20 PMID: 8243996
  34. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation.
    J Virol. 1992 Jun;66(6):3669-76 PMID: 1583726
  35. 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 PMID: 8267715
  36. Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal.
    J Mol Biol. 1991 Aug 20;220(4):889-902 PMID: 1880803
  37. Transposon tagging using Ty elements in yeast.
    Genetics. 1988 Sep;120(1):95-108 PMID: 2851484
  38. Spermidine or spermine is essential for the aerobic growth of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5872-6 PMID: 2062864
  39. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6816-20 PMID: 2842793
  40. Delta sequences in the 5' non-coding region of yeast tRNA genes.
    EMBO J. 1983;2(4):583-91 PMID: 16453444
  41. Ribosomal movement impeded at a pseudoknot required for frameshifting.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8636-40 PMID: 1528874
  42. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.91.1.172
Published
1994-01-04
Pages
172-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC42908
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.91.1.172 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2