Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components

Beliakova-Bethell, Nadejda; Beckham, Carla; Giddings, Thomas H.; Winey, Mark; Parker, Roy; Sandmeyer, Suzanne

doi:10.1261/rna.2264806

Cited by 92 publications

(142 citation statements)

References 33 publications

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“…This observation suggests that Xrn1 either destabilizes other Ty1 regulatory RNAs or controls posttranscriptional steps during the transposition cycle. For instance, previous studies revealed a structural role of Xrn1 and P-body components in the assembly of gypsylike Ty3 VLPs (Beliakova-Bethell et al 2006). One could hypothesize that this function is conserved for the assembly process of Ty1 VLPs as well.…”

Section: Transcriptional Gene Silencingmentioning

confidence: 95%

A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae

Berretta¹,

Pinskaya²,

Morillon³

2008

Genes Dev.

179

212

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Cryptic unstable transcripts (CUTs) are synthesized from intra-and intergenic regions in Saccharomyces cerevisiae and are rapidly degraded by RNA surveillance pathways, but their function(s) remain(s) elusive. Here, we show that an antisense TY1 CUT, starting within the Ty1 retrotransposon and encompassing the promoter 5 long terminal repeat (LTR), mediates RNA-dependent gene silencing and represses Ty1 mobility. We show that the Ty1 regulatory RNA is synthesized by RNA polymerase II, polyadenylated, and destabilized by the cytoplasmic 5 RNA degradation pathway. Moreover, the Ty1 regulatory RNA represses Ty1 transcription and transposition in trans by acting on the de novo transcribed TY1 RNA. Consistent with a transcriptional regulation mechanism, we show that RNA polymerase II occupancy is reduced on the Ty1 chromatin upon silencing, although TBP binding remains unchanged. Furthermore, the Ty1 silencing is partially mediated by histone deacetylation and requires Set1-dependent histone methylation, pointing out an analogy with heterochromatin gene silencing. Our results show the first example of an RNA-dependent gene trans-silencing mediated by epigenetic marks in S. cerevisiae. Recent data have shown that cryptic unstable transcripts (CUTs) are RNA polymerase II (RNAPII)-dependent noncoding RNAs (ncRNAs) corresponding to inter-and intragenic regions of the genome and may represent 10% of intergenic transcripts in Saccharomyces cerevisiae (Wyers et al. 2005). Under normal conditions, CUTs are almost undetectable, as they are rapidly degraded by the activity of Rrp6 and Trf4, members of the nuclear exosome and the TRAMP complex, respectively (LaCava et al. 2005;Vanacova et al. 2005;Wyers et al. 2005). In addition to Trf4 and Rrp6, the cytoplasmic 5Ј-3Ј exoribonuclease Xrn1 also plays an important role in the turnover of CUTs, supporting the idea that some of these transcripts escape the nuclear quality control and might have a cytoplasmic residency (Thompson and Parker 2007).Despite these observations, the function(s) of CUTs remain(s) poorly characterized. Cryptic transcription has been widely described from yeast to human and qualified as "transcriptional noise." Interestingly, it has been proposed that cryptic transcription allows RNA polymerase-dependent chromatin changes but not the production of functional RNA molecules, as those are immediately degraded (Struhl 2007). In agreement with this model, CUT transcription has been shown to interfere with promoters of coding regions and hence regulates gene expression in S. cerevisiae (Martens et al. 2005;Hongay et al. 2006;Uhler et al. 2007). However, alternative models emerged, providing a direct function for cryptic transcripts. Indeed, recent reports have shown that the processing of siRNAs in Schizosaccharomyces pombe is mediated by homologs of the TRAMP and exosome subunits (Buhler et al. 2007;Nicolas et al. 2007), strongly indicating that the fission yeast's siRNAs might originate from CUTs. It is tempting to hypothesize that CUTs in S. cerevisiae are link...

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Section: Transcriptional Gene Silencingmentioning

confidence: 95%

A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae

Berretta¹,

Pinskaya²,

Morillon³

2008

Genes Dev.

179

212

View full text Add to dashboard Cite

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“…For example, recent results argue that the Ty3 retrotransposon in yeast may assemble its virus-like particles in association with P-bodies (Beliakova-Bethell et al 2006). This suggests that P-bodies may be important sites of specific steps in retrotransposon and viral life cycles that might then be modulated by miRNAs.…”

Section: Future Perspective and Issuesmentioning

confidence: 99%

Control of translation and mRNA degradation by miRNAs and siRNAs: Table 1.

Valencia-Sanchez¹,

Liu²,

Hannon³

et al. 2006

Genes Dev.

Self Cite

1,862

1,355

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The control of translation and mRNA degradation is an important part of the regulation of gene expression. It is now clear that small RNA molecules are common and effective modulators of gene expression in many eukaryotic cells. These small RNAs that control gene expression can be either endogenous or exogenous micro RNAs (miRNAs) and short interfering RNAs (siRNAs) and can affect mRNA degradation and translation, as well as chromatin structure, thereby having impacts on transcription rates. In this review, we discuss possible mechanisms by which miRNAs control translation and mRNA degradation. An emerging theme is that miRNAs, and siRNAs to some extent, target mRNAs to the general eukaryotic machinery for mRNA degradation and translation control.

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“…Virus-like retrotransposon particle assembly takes place at or near P-bodies. As P-bodies are sites of mRNA degradation and storage (Brengues et al 2005), it has been suggested that P-body-associated translational repression promotes assembly of retrotransposon RNA into virus-like particles (Beliakova-Bethell et al 2006). Our observations suggest poly(A) tail length control as another aspect of this switch from translation to packaging of retrotransposon RNA.…”

Section: Mechanism Of Poly(a) Tail Length Regulationmentioning

confidence: 99%

Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome

Beilharz¹,

Preiß²

2007

RNA

130

158

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Control of poly(A) tail length can affect translation and stability of eukaryotic mRNAs. Although well established for individual cases, it was not known to what extent this type of adjustable gene control is used to shape expression of eukaryotic transcriptomes. Here we report on microarray-based measurements of mRNA poly(A) tail lengths and association with the poly(A)-binding protein Pab1 in S. cerevisiae, revealing extensive correlation between tail length and other physical and functional mRNA characteristics. Gene ontology analyses and further directed experiments indicate coregulation of tail length on functionally and cytotopically related mRNAs to coordinate cell-cycle progression, ribosome biogenesis, and retrotransposon expression. We show that the 39-untranslated region drives transcript-specific adenylation control and translational efficiency of multiple mRNAs. Our findings suggest a wide-spread interdependence between 39-untranslated region-mediated poly(A) tail length control, Pab1 binding, and mRNA translation in budding yeast. They further provide a molecular explanation for deadenylase function in the cell cycle and suggest additional cellular processes that depend on control of mRNA polyadenylation.

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Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components

Cited by 92 publications

References 33 publications

A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae

A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae

Control of translation and mRNA degradation by miRNAs and siRNAs: Table 1.

Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome

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