Glucose signalling pathway controls the programmed ribosomal frameshift efficiency in retroviral‐like element Ty3 in <i>Saccharomyces cerevisiae</i>

Türkel, Sezai; Kaplan, Güliz; Farabaugh, Philip J.

doi:10.1002/yea.1906

Cited by 7 publications

(8 citation statements)

References 65 publications

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“…Its frameshifting is not a constitutive process but is regulated over a 10-fold response window depending on carbon source. The glucose-signaling pathway involved has been investigated in depth ( 216 ).…”

Section: Occurrence and Function In Mobile Elements Derivatives And mentioning

confidence: 99%

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use

Atkins¹,

Loughran²,

Bhatt³

et al. 2016

Nucleic Acids Res

269

367

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Genetic decoding is not ‘frozen’ as was earlier thought, but dynamic. One facet of this is frameshifting that often results in synthesis of a C-terminal region encoded by a new frame. Ribosomal frameshifting is utilized for the synthesis of additional products, for regulatory purposes and for translational ‘correction’ of problem or ‘savior’ indels. Utilization for synthesis of additional products occurs prominently in the decoding of mobile chromosomal element and viral genomes. One class of regulatory frameshifting of stable chromosomal genes governs cellular polyamine levels from yeasts to humans. In many cases of productively utilized frameshifting, the proportion of ribosomes that frameshift at a shift-prone site is enhanced by specific nascent peptide or mRNA context features. Such mRNA signals, which can be 5′ or 3′ of the shift site or both, can act by pairing with ribosomal RNA or as stem loops or pseudoknots even with one component being 4 kb 3′ from the shift site. Transcriptional realignment at slippage-prone sequences also generates productively utilized products encoded trans-frame with respect to the genomic sequence. This too can be enhanced by nucleic acid structure. Together with dynamic codon redefinition, frameshifting is one of the forms of recoding that enriches gene expression.

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Section: Occurrence and Function In Mobile Elements Derivatives And mentioning

confidence: 99%

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use

Atkins¹,

Loughran²,

Bhatt³

et al. 2016

Nucleic Acids Res

269

367

View full text Add to dashboard Cite

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“…Frameshift occurs at +1 direction without tRNA slippage by out-of-frame binding of valyl-tRNA to the GUU codon at the A-site of the ribosome [28]. Previously, it was reported that the frameshift frequency in Ty3 can be modulated by growth conditions [9]. It is activated by nonfermentable carbon sources up to 3-fold in a Snf1p dependent manner.…”

Section: Discussionmentioning

confidence: 99%

“…The PRF rate in Ty3 is activated more than 3-fold in the yeast cells that are grown in low glucose medium in a Snf1p dependent manner. cAMP dependent protein kinase-A is also involved in the regulation of frameshift efficiency in Ty3 [9]. In addition, we have analyzed the effects of glucose signaling on the PRF efficiency in Ty1 elements and shown that the Ty1 type +1 PRF frequency decreases several fold in glycerol-lactate-grown S. cerevisiae cells [8].…”

Section: Introductionmentioning

confidence: 97%

“…The rate of PRF shows variations among retroviruses and retroviral-like elements [6]. The PRF rate is approximately 4-5% in Ty3, while it is 25% in Ty1 under standard growth conditions in most of the laboratory strains of S. cerevisiae (in synthetic complete medium supplemented with 2% glucose in logarithmically grown cells at 30 ∘ C) [8,9].…”

Section: Introductionmentioning

confidence: 99%

“…Several lines of evidence indicate that the PRF is not a constitutive event, and it is regulated by different cellular signals. Previously, we have shown that the programmed ribosomal frameshift (PRF) event in Ty3 is regulated by glucose signaling [9]. The PRF rate in Ty3 is activated more than 3-fold in the yeast cells that are grown in low glucose medium in a Snf1p dependent manner.…”

Section: Introductionmentioning

confidence: 99%

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Amino Acid Starvation Enhances Programmed Ribosomal Frameshift in Metavirus Ty3 ofSaccharomyces cerevisiae

Türkel

2016

Advances in Biology

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Ty3 is a retroviral-like element and propagates with a retroviral-like mechanism within the yeast cells. Ty3 mRNA contains two coding regions, which are GAG3 and POL3. The coding region POL3 is translated as a GAG3-POL3 fusion protein by a +1 programmed frameshift. In this study, it was shown that the Ty3 frameshift frequency is significantly increased by amino acid starvation in a Gcn2p complex dependent manner. When the yeast cells were subjected to amino acid starvation, the frameshift frequency of Ty3 increased more than 2-fold in the wild-type yeast cells, mostly independent of Gcn4p. However, Ty3 frameshift frequency remained at basal level in thegcn1,gcn20, orgcn2mutant yeast cells in amino acid starved yeasts. Gcn1p forms a complex with Gcn2p and Gcn20p and is involved in the sensing of uncharged tRNAs on the ribosomal A-site during translation. Increases in uncharged tRNA levels due to amino acid depletion lead to ribosomal pauses. These ribosomal pauses are significant actors in the regulation of Ty3 frameshift frequency. Results of this research revealed that frameshift frequency in Ty3 is regulated by the Gcn2p complex in response to amino acid starvation in yeast.

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Metabolic stress promotes stop-codon readthrough and phenotypic heterogeneity

Zhang

Lyu

Fan

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Accurate protein synthesis is a tightly controlled biological process with multiple quality control steps safeguarded by aminoacyl-transfer RNA (tRNA) synthetases and the ribosome. Reduced translational accuracy leads to various physiological changes in both prokaryotes and eukaryotes. Termination of translation is signaled by stop codons and catalyzed by release factors. Occasionally, stop codons can be suppressed by near-cognate aminoacyl-tRNAs, resulting in protein variants with extended C termini. We have recently shown that stop-codon readthrough is heterogeneous among single bacterial cells. However, little is known about how environmental factors affect the level and heterogeneity of stop-codon readthrough. In this study, we have combined dual-fluorescence reporters, mass spectrometry, mathematical modeling, and single-cell approaches to demonstrate that a metabolic stress caused by excess carbon substantially increases both the level and heterogeneity of stop-codon readthrough. Excess carbon leads to accumulation of acid metabolites, which lower the pH and the activity of release factors to promote readthrough. Furthermore, our time-lapse microscopy experiments show that single cells with high readthrough levels are more adapted to severe acid stress conditions and are more sensitive to an aminoglycoside antibiotic. Our work thus reveals a metabolic stress that promotes translational heterogeneity and phenotypic diversity.

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Glucose signalling pathway controls the programmed ribosomal frameshift efficiency in retroviral‐like element Ty3 in Saccharomyces cerevisiae

Cited by 7 publications

References 65 publications

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use

Amino Acid Starvation Enhances Programmed Ribosomal Frameshift in Metavirus Ty3 ofSaccharomyces cerevisiae

Metabolic stress promotes stop-codon readthrough and phenotypic heterogeneity

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