Literature DB >> 25240800

The RNA exosome promotes transcription termination of backtracked RNA polymerase II.

Jean-François Lemay1, Marc Larochelle1, Samuel Marguerat2, Sophie Atkinson3, Jürg Bähler3, François Bachand4.   

Abstract

The exosome is an RNA-decay complex that constantly monitors transcription and contributes to post-transcriptional turnover of faulty mRNAs. Yet how nuclear RNA surveillance by the exosome is coordinated with transcription is still unknown. Here we show that the RNA exosome of Schizosaccharomyces pombe can target the transcription machinery by terminating transcription events associated with paused and backtracked RNA polymerase II (RNAPII); this is contrary to the notion that the exosome acts exclusively on RNAs that have been released by RNAPII. Our data support a mechanism by which RNAPII backtracking provides a free RNA 3' end for the core exosome, which results in transcription termination with concomitant degradation of the associated transcript. These findings uncover a mechanism of cotranscriptional RNA surveillance whereby termination of transcription by the exosome prevents formation of aberrant readthrough RNAs and transcriptional interference at neighboring genes.

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Year:  2014        PMID: 25240800     DOI: 10.1038/nsmb.2893

Source DB:  PubMed          Journal:  Nat Struct Mol Biol        ISSN: 1545-9985            Impact factor:   15.369


  60 in total

1.  A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes.

Authors:  Alain R Bataille; Célia Jeronimo; Pierre-Étienne Jacques; Louise Laramée; Marie-Ève Fortin; Audrey Forest; Maxime Bergeron; Steven D Hanes; François Robert
Journal:  Mol Cell       Date:  2012-01-27       Impact factor: 17.970

2.  RNA polymerase backtracking in gene regulation and genome instability.

Authors:  Evgeny Nudler
Journal:  Cell       Date:  2012-06-22       Impact factor: 41.582

3.  The role of Rat1 in coupling mRNA 3'-end processing to transcription termination: implications for a unified allosteric-torpedo model.

Authors:  Weifei Luo; Arlen W Johnson; David L Bentley
Journal:  Genes Dev       Date:  2006-04-05       Impact factor: 11.361

4.  Torpedo nuclease Rat1 is insufficient to terminate RNA polymerase II in vitro.

Authors:  Stefan Dengl; Patrick Cramer
Journal:  J Biol Chem       Date:  2009-06-17       Impact factor: 5.157

5.  Pause sites promote transcriptional termination of mammalian RNA polymerase II.

Authors:  Natalia Gromak; Steven West; Nick J Proudfoot
Journal:  Mol Cell Biol       Date:  2006-05       Impact factor: 4.272

6.  The nuclear poly(A)-binding protein interacts with the exosome to promote synthesis of noncoding small nucleolar RNAs.

Authors:  Jean-François Lemay; Annie D'Amours; Caroline Lemieux; Daniel H Lackner; Valérie G St-Sauveur; Jürg Bähler; François Bachand
Journal:  Mol Cell       Date:  2010-01-15       Impact factor: 17.970

7.  Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe.

Authors:  J Bähler; J Q Wu; M S Longtine; N G Shah; A McKenzie; A B Steever; A Wach; P Philippsen; J R Pringle
Journal:  Yeast       Date:  1998-07       Impact factor: 3.239

8.  Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex.

Authors:  Debora Lika Makino; Marc Baumgärtner; Elena Conti
Journal:  Nature       Date:  2013-02-03       Impact factor: 49.962

9.  Nascent transcript sequencing visualizes transcription at nucleotide resolution.

Authors:  L Stirling Churchman; Jonathan S Weissman
Journal:  Nature       Date:  2011-01-20       Impact factor: 49.962

10.  The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities.

Authors:  Daneen Schaeffer; Borislava Tsanova; Ana Barbas; Filipa Pereira Reis; Eeshita Ghosh Dastidar; Maya Sanchez-Rotunno; Cecília Maria Arraiano; Ambro van Hoof
Journal:  Nat Struct Mol Biol       Date:  2008-12-07       Impact factor: 15.369

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  53 in total

1.  Effects of Transcription Elongation Rate and Xrn2 Exonuclease Activity on RNA Polymerase II Termination Suggest Widespread Kinetic Competition.

Authors:  Nova Fong; Kristopher Brannan; Benjamin Erickson; Hyunmin Kim; Michael A Cortazar; Ryan M Sheridan; Tram Nguyen; Shai Karp; David L Bentley
Journal:  Mol Cell       Date:  2015-10-15       Impact factor: 17.970

Review 2.  Fail-safe transcription termination: Because one is never enough.

Authors:  Jean-François Lemay; François Bachand
Journal:  RNA Biol       Date:  2015       Impact factor: 4.652

Review 3.  The regulation and functions of the nuclear RNA exosome complex.

Authors:  Cornelia Kilchert; Sina Wittmann; Lidia Vasiljeva
Journal:  Nat Rev Mol Cell Biol       Date:  2016-01-04       Impact factor: 94.444

4.  Conserved factor Dhp1/Rat1/Xrn2 triggers premature transcription termination and nucleates heterochromatin to promote gene silencing.

Authors:  Venkata R Chalamcharla; H Diego Folco; Jothy Dhakshnamoorthy; Shiv I S Grewal
Journal:  Proc Natl Acad Sci U S A       Date:  2015-12-02       Impact factor: 11.205

Review 5.  Lingering Questions about Enhancer RNA and Enhancer Transcription-Coupled Genomic Instability.

Authors:  Gerson Rothschild; Uttiya Basu
Journal:  Trends Genet       Date:  2017-01-10       Impact factor: 11.639

6.  New twists on long noncoding RNAs: from mobile elements to motile cancer cells.

Authors:  Tuan M Nguyen; Sumayya Alchalabi; Adewunmi Oluwatoyosi; Ali S Ropri; Jason I Herschkowitz; Jeffrey M Rosen
Journal:  RNA Biol       Date:  2020-06-10       Impact factor: 4.652

7.  Widespread Backtracking by RNA Pol II Is a Major Effector of Gene Activation, 5' Pause Release, Termination, and Transcription Elongation Rate.

Authors:  Ryan M Sheridan; Nova Fong; Angelo D'Alessandro; David L Bentley
Journal:  Mol Cell       Date:  2018-11-29       Impact factor: 17.970

8.  CPF Recruitment to Non-canonical Transcription Termination Sites Triggers Heterochromatin Assembly and Gene Silencing.

Authors:  Tommy V Vo; Jothy Dhakshnamoorthy; Madeline Larkin; Martin Zofall; Gobi Thillainadesan; Vanivilasini Balachandran; Sahana Holla; David Wheeler; Shiv I S Grewal
Journal:  Cell Rep       Date:  2019-07-02       Impact factor: 9.423

Review 9.  RNA Exosome Regulates AID DNA Mutator Activity in the B Cell Genome.

Authors:  Evangelos Pefanis; Uttiya Basu
Journal:  Adv Immunol       Date:  2015-05-14       Impact factor: 3.543

Review 10.  Rrp6: Integrated roles in nuclear RNA metabolism and transcription termination.

Authors:  Melanie J Fox; Amber L Mosley
Journal:  Wiley Interdiscip Rev RNA       Date:  2015-11-26       Impact factor: 9.957

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