Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore

Hessle, Viktoria; Euler, Anne von; Valdivia, Ernesto González de; Visa, Neus

doi:10.1261/rna.032045.111

Cited by 14 publications

(11 citation statements)

References 42 publications

(50 reference statements)

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“…However, recent evidence has shown that Rrp6 indeed can bind to RNAs without exerting its ribonuclease function. In Chironomus tentans, Rrp6 binds to nascent transcripts before splicing and accompanies the spliced mRNA to the nuclear pore, where it is released from the mRNPs before nucleo-cytoplasmic translocation (Hessle et al, 2012). It is unknown whether such RNA retention requires a physical association between Rrp6 and other proteins.…”

Section: Discussionmentioning

confidence: 99%

An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis

et al. 2014

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SUMMARY Rrp6-mediated nuclear RNA surveillance tunes eukaryotic transcriptomes through non-coding RNA degradation and mRNA quality control, including exosomal RNA decay and transcript retention triggered by defective RNA processing. It is unclear whether Rrp6 can positively regulate non-coding RNAs and whether RNA retention occurs in normal cells. Here we report that AtRRP6L1, an Arabidopsis Rrp6-like protein, controls RNA-directed DNA methylation through positive regulation of non-coding RNAs. Discovered in a forward genetic screen, AtRRP6L1 mutations decrease DNA methylation independently of exosomal RNA degradation. Accumulation of Pol V-transcribed scaffold RNAs requires AtRRP6L1 that binds to RNAs in vitro and in vivo. AtRRP6L1 helps retain Pol V-transcribed RNAs in chromatin to enable their scaffold function. In addition, AtRRP6L1 is required for genome-wide Pol IV-dependent siRNA production that may involve retention of Pol IV transcripts. Our results suggest that AtRRP6L1 functions in epigenetic regulation by helping with the retention of non-coding RNAs in normal cells.

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Section: Discussionmentioning

confidence: 99%

An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis

et al. 2014

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“…Notably, the RNA surveillance machinery, including the TRAMP complex and the nuclear exosome, apparently retain or degrade aberrant or non-functional RNA species in the vicinity of the NPCs (13,16). Moreover, human Nup98 regulates degradation of the p21 CIP1 mRNA by the exosome, and Rrp6 is recruited to nascent transcripts and is then released from mRNPs near the NPCs in Chironomus tentans (48,55). These findings indicate that NPCs could provide a platform for mRNA degradation, and/or that the NPCs may regulate whether mRNPs are exported or degraded.…”

Section: Discussionmentioning

confidence: 99%

Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast

Sugiyama

Wanatabe

Kitahata

et al. 2013

Nucleic Acids Research

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Zinc-finger domains are found in many nucleic acid-binding proteins in both prokaryotes and eukaryotes. Proteins carrying zinc-finger domains have important roles in various nuclear transactions, including transcription, mRNA processing and mRNA export; however, for many individual zinc-finger proteins in eukaryotes, the exact function of the protein is not fully understood. Here, we report that Red5 is involved in efficient suppression of specific mRNAs during vegetative growth of Schizosaccharomyces pombe. Red5, which contains five C3H1-type zinc-finger domains, localizes to the nucleus where it forms discrete dots. A red5 point mutation, red5-2, results in the upregulation of specific meiotic mRNAs in vegetative mutant red5-2 cells; northern blot data indicated that these meiotic mRNAs in red5-2 cells have elongated poly(A) tails. RNA-fluorescence in situ hybridization results demonstrate that poly(A)+ RNA species accumulate in the nucleolar regions of red5-deficient cells. Moreover, Red5 genetically interacts with several mRNA export factors. Unexpectedly, three components of the nuclear pore complex also suppress a specific set of meiotic mRNAs. These results indicate that Red5 function is important to meiotic mRNA degradation; they also suggest possible connections among selective mRNA decay, mRNA export and the nuclear pore complex in vegetative fission yeast.

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“…Toward this end, an overexpressed tagged version of Rrp6 was shown to associate with chromatin of yeast protein coding genes using whole open reading frame cDNA mircroarrays (11). In Drosophila , it was demonstrated that certain exosome subunits associate with at least some actively transcribed genes (12,13) and may be recruited to chromatin through interaction with RNA polymerase II (Pol II) elongation factors Spt5 and Spt6 (14). Nevertheless, a high-resolution genome-wide study of exosome chromatin association has yet to be performed in any organism.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide localization of exosome components to active promoters and chromatin insulators in Drosophila

Lim

Boyle

Chinen

et al. 2013

Nucleic Acids Research

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Chromatin insulators are functionally conserved DNA–protein complexes situated throughout the genome that organize independent transcriptional domains. Previous work implicated RNA as an important cofactor in chromatin insulator activity, although the precise mechanisms are not yet understood. Here we identify the exosome, the highly conserved major cellular 3′ to 5′ RNA degradation machinery, as a physical interactor of CP190-dependent chromatin insulator complexes in Drosophila. Genome-wide profiling of exosome by ChIP-seq in two different embryonic cell lines reveals extensive and specific overlap with the CP190, BEAF-32 and CTCF insulator proteins. Colocalization occurs mainly at promoters but also boundary elements such as Mcp, Fab-8, scs and scs′, which overlaps with a promoter. Surprisingly, exosome associates primarily with promoters but not gene bodies of active genes, arguing against simple cotranscriptional recruitment to RNA substrates. Similar to insulator proteins, exosome is also significantly enriched at divergently transcribed promoters. Directed ChIP of exosome in cell lines depleted of insulator proteins shows that CTCF is required specifically for exosome association at Mcp and Fab-8 but not other sites, suggesting that alternate mechanisms must also contribute to exosome chromatin recruitment. Taken together, our results reveal a novel positive relationship between exosome and chromatin insulators throughout the genome.

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Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore

Cited by 14 publications

References 42 publications

An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis

An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis

Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast

Genome-wide localization of exosome components to active promoters and chromatin insulators in Drosophila

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