Cotranscriptional Recruitment of RNA Exosome Cofactors Rrp47p and Mpp6p and Two Distinct Trf-Air-Mtr4 Polyadenylation (TRAMP) Complexes Assists the Exonuclease Rrp6p in the Targeting and Degradation of an Aberrant Messenger Ribonucleoprotein Particle (mRNP) in Yeast

Stuparević, Igor; Mosrin-Huaman, Christine; Hervouet-Coste, Nadège; Remenaric, Mateja; Rahmouni, A. Rachid

doi:10.1074/jbc.m113.491290

Cited by 32 publications

(68 citation statements)

References 48 publications

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“…Notably, we showed previously that the stimulation of co-transcriptional recruitment of Nrd1p upon Rho action is accompanied by the recruitment of the TRAMP components Trf4p, Trf5p and Air2p. 17 This finding was supported by a recent study showing physical interaction between Trf4p and Nrd1p. 18 Again, the RT-qPCR measurements (shown in Fig.…”

Section: Nrd1p Is Not Involved In the Targeting Of Rho-induced Aberrasupporting

confidence: 80%

“…A similar rescue of PMA1 mRNA was observed with a strain harboring a catalytically inactive version of Rrp6p (rrp6-Y361A in Ref. 17 ) or when the exonuclease cofactor Rrp47p is lacking (rrp47D strain, Fig. 1).…”

Section: Hxk1 Transcript Is Affected By Rho Activity Independently Ofmentioning

confidence: 57%

“…A similar absence of involvement was found for Dis3p by testing strains with single mutations that abolish either the exonuclease (dis3-D551N allele) or the endonuclease (dis3-D171N allele) activities of the exosome subunit (results not shown and Refs. 17,19,20 ). In contrast, as depicted in Fig.…”

Section: Nrd1p Is Not Involved In the Targeting Of Rho-induced Aberramentioning

confidence: 99%

“…The RNA-dependent helicase/translocase activity of Rho impedes the co-transcriptional recruitment of mRNA processing and packaging factors as was shown previously for the THO component Mft1p by Chromatin ImmunoPrecipitation (ChIP) experiments. 17 Such interference leads to the production of transcripts that have normal lengths and polyA tails but which are recognized as aberrant and eliminated by the Rrp6p-dependent QC mechanism following their retention in the nucleus (reviewed in Ref. 14 ).…”

Section: Hxk1 Transcript Is Affected By Rho Activity Independently Ofmentioning

confidence: 99%

“…Moreover, the results revealed that the QC process is coordinated by Nrd1p (a component of the early termination complex, Nrd1p-Nab3p) whose increased co-transcriptional recruitment promotes the attachment of Rrp6p to the transcription complex along with its cofactors Rrp47p and Mpp6p as well as the co-activator TRAMP complex. 16,17 A limited microarray analysis measuring differential steady-state mRNA levels in the absence and the presence of Rho activity (unpublished results) revealed HXK1 (hexokinase isoenzyme 1) as a transcript that was also highly sensitive to Rho action. In the present work, we investigated the mechanism underlying Rho-mediated HXK1 decay.…”

Section: Introductionmentioning

confidence: 99%

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Co-transcriptional degradation by the 5′-3′ exonuclease Rat1p mediates quality control of HXK1 mRNP biogenesis in S. cerevisiae

2016

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The co-transcriptional biogenesis of export-competent messenger ribonucleoprotein particles (mRNPs) in yeast is under the surveillance of quality control (QC) steps. Aberrant mRNPs resulting from inappropriate or inefficient processing and packaging reactions are detected by the QC system and retained in the nucleus with ensuing elimination of their mRNA component by a mechanism that requires the catalytic activity of Rrp6p, a 3 0 -5 0 exonuclease associated with the RNA exosome. In previous studies, we implemented a new experimental approach in which the production of aberrant mRNPs is massively increased upon perturbation of mRNP biogenesis by the RNA-dependent helicase/translocase activity of the bacterial Rho factor expressed in S. cerevisiae. The analyses of a subset of transcripts such as PMA1 led us to substantiate the essential role of Rrp6p in the nuclear mRNP QC and to reveal a functional coordination of the process by Nrd1p. Here, we extended those results by showing that, in contrast to PMA1, Rho-induced aberrant HXK1 mRNPs are targeted for destruction by an Nrd1p-and Rrp6p-independent alternative QC pathway that relies on the 5 0 -3 0 exonuclease activity of Rat1p. We show that the degradation of aberrant HXK1 mRNPs by Rat1p occurs cotranscriptionally following decapping by Dcp2p and leads to premature transcription termination. We discuss the possibility that this alternative QC pathway might be linked to the well-known specific features of the HXK1 gene transcription such as its localization at the nuclear periphery and gene loop formation.

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Section: Nrd1p Is Not Involved In the Targeting Of Rho-induced Aberrasupporting

confidence: 80%

Section: Hxk1 Transcript Is Affected By Rho Activity Independently Ofmentioning

confidence: 57%

Section: Nrd1p Is Not Involved In the Targeting Of Rho-induced Aberramentioning

confidence: 99%

Section: Hxk1 Transcript Is Affected By Rho Activity Independently Ofmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Co-transcriptional degradation by the 5′-3′ exonuclease Rat1p mediates quality control of HXK1 mRNP biogenesis in S. cerevisiae

2016

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Rrp6: Integrated roles in nuclear RNA metabolism and transcription termination

Fox

Mosley

2015

WIREs RNA

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The yeast RNA exosome is a eukaryotic ribonuclease complex essential for RNA processing, surveillance and turnover. It is comprised of a barrel-shaped core and cap as well as a 3’–5’ ribonuclease known as Dis3 which contains both endo- and exonuclease domains. A second exonuclease, Rrp6, is added in the nucleus. Dis3 and Rrp6 have both shared and distinct roles in RNA metabolism, and this review will focus primarily on Rrp6 and the roles of the RNA exosome in the nucleus. The functions of the nuclear exosome are modulated by cofactors and interacting partners specific to each type of substrate. Generally, the cofactor TRAMP (Trf4/5-Air2/1-Mtr4 polyadenylation) complex helps unwind unstable RNAs, RNAs requiring processing such as rRNAs, tRNAs, or snRNAs or improperly processed RNAs and direct it toward the exosome. In yeast, Rrp6 interacts with Nrd1, the cap binding complex (CBC), and RNA Polymerase II to aid in nascent RNA processing, termination, and polyA tail length regulation. Recent studies have shown that proper termination and processing of short, non-coding RNAs by Rrp6 is particularly important for transcription regulation across the genome and has important implications for regulation of diverse processes at the cellular level. Loss of proper Rrp6 and exosome activity may contribute to various pathologies such as autoimmune disease, neurological disorders, and cancer.

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Deciphering the Dynamic Landscape of Transcription-Associated mRNP Quality Control Components Over the Whole Yeast Genome

Moreau

Dantec

Rahmouni

2020

Methods in Molecular Biology

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In eukaryotic cells, aberrant mRNPs with processing and packaging defects are targeted co-transcriptionally by a surveillance system that triggers their nuclear retention and ultimately the degradation of their mRNA component by the 3'-5' activity of the exosome-associated exonuclease Rrp6. This mRNP quality control process is stimulated by the NNS complex (Nrd1-Nab3-Sen1), which otherwise mediates termination, processing and decay of ncRNAs. The process involves also the exosome co-activator TRAMP complex (Trf4-Air2-Mtr4). Here, we describe a genome-wide approach to visualize the dynamic movement and coordination of these quality control components over the yeast chromosomes upon perturbation of mRNP biogenesis. The method provides valuable information on how the surveillance system is precisely coordinated both physically and functionally with the transcription machinery to detect the faulty events during perturbation of mRNP biogenesis. The overview shows also that the gathering of the quality control components over affected mRNA genes takes place at the expense of their commitment to be recruited at ncRNAs genomic features, provoking termination and processing defects of ncRNAs.

show abstract

Cotranscriptional Recruitment of RNA Exosome Cofactors Rrp47p and Mpp6p and Two Distinct Trf-Air-Mtr4 Polyadenylation (TRAMP) Complexes Assists the Exonuclease Rrp6p in the Targeting and Degradation of an Aberrant Messenger Ribonucleoprotein Particle (mRNP) in Yeast

Cited by 32 publications

References 48 publications

Co-transcriptional degradation by the 5′-3′ exonuclease Rat1p mediates quality control of HXK1 mRNP biogenesis in S. cerevisiae

Co-transcriptional degradation by the 5′-3′ exonuclease Rat1p mediates quality control of HXK1 mRNP biogenesis in S. cerevisiae

Rrp6: Integrated roles in nuclear RNA metabolism and transcription termination

Deciphering the Dynamic Landscape of Transcription-Associated mRNP Quality Control Components Over the Whole Yeast Genome

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