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PAPγ associates with PAXT nuclear exosome to control the abundance of PROMPT ncRNAs

Author

Listed:
  • Xavier Contreras

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • David Depierre

    (University of Toulouse)

  • Charbel Akkawi

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Marina Srbic

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Marion Helsmoortel

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Maguelone Nogaret

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Matthieu LeHars

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Kader Salifou

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

  • Alexandre Heurteau

    (University of Toulouse)

  • Olivier Cuvier

    (University of Toulouse)

  • Rosemary Kiernan

    (Institute of Human Genetics (IGH)/University of Montpellier, Gene Regulation Lab)

Abstract

Pervasive transcription of the human genome generates an abundance of RNAs that must be processed and degraded. The nuclear RNA exosome is the main RNA degradation machinery in the nucleus. However, nuclear exosome must be recruited to its substrates by targeting complexes, such as NEXT or PAXT. By proteomic analysis, we identify additional subunits of PAXT, including many orthologs of MTREC found in S. pombe. In particular, we show that polyA polymerase gamma (PAPγ) associates with PAXT. Genome-wide mapping of the binding sites of ZFC3H1, RBM27 and PAPγ shows that PAXT is recruited to the TSS of hundreds of genes. Loss of ZFC3H1 abolishes recruitment of PAXT subunits including PAPγ to TSSs and concomitantly increases the abundance of PROMPTs at the same sites. Moreover, PAPγ, as well as MTR4 and ZFC3H1, is implicated in the polyadenylation of PROMPTs. Our results thus provide key insights into the direct targeting of PROMPT ncRNAs by PAXT at their genomic sites.

Suggested Citation

  • Xavier Contreras & David Depierre & Charbel Akkawi & Marina Srbic & Marion Helsmoortel & Maguelone Nogaret & Matthieu LeHars & Kader Salifou & Alexandre Heurteau & Olivier Cuvier & Rosemary Kiernan, 2023. "PAPγ associates with PAXT nuclear exosome to control the abundance of PROMPT ncRNAs," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42620-9
    DOI: 10.1038/s41467-023-42620-9
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    1. Helen Neil & Christophe Malabat & Yves d’Aubenton-Carafa & Zhenyu Xu & Lars M. Steinmetz & Alain Jacquier, 2009. "Widespread bidirectional promoters are the major source of cryptic transcripts in yeast," Nature, Nature, vol. 457(7232), pages 1038-1042, February.
    2. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    3. Albert E. Almada & Xuebing Wu & Andrea J. Kriz & Christopher B. Burge & Phillip A. Sharp, 2013. "Promoter directionality is controlled by U1 snRNP and polyadenylation signals," Nature, Nature, vol. 499(7458), pages 360-363, July.
    4. Jérémy Dufourt & Gwénaëlle Bontonou & Aymeric Chartier & Camille Jahan & Anne-Cécile Meunier & Stéphanie Pierson & Paul F. Harrison & Catherine Papin & Traude H. Beilharz & Martine Simonelig, 2017. "piRNAs and Aubergine cooperate with Wispy poly(A) polymerase to stabilize mRNAs in the germ plasm," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    5. Komal Soni & Anusree Sivadas & Attila Horvath & Nikolay Dobrev & Rippei Hayashi & Leo Kiss & Bernd Simon & Klemens Wild & Irmgard Sinning & Tamás Fischer, 2023. "Mechanistic insights into RNA surveillance by the canonical poly(A) polymerase Pla1 of the MTREC complex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Robin Andersson & Peter Refsing Andersen & Eivind Valen & Leighton J. Core & Jette Bornholdt & Mette Boyd & Torben Heick Jensen & Albin Sandelin, 2014. "Nuclear stability and transcriptional directionality separate functionally distinct RNA species," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    7. Nikolay Dobrev & Yasar Luqman Ahmed & Anusree Sivadas & Komal Soni & Tamás Fischer & Irmgard Sinning, 2021. "The zinc-finger protein Red1 orchestrates MTREC submodules and binds the Mtl1 helicase arch domain," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    8. Fan Yang & Bogdan Tanasa & Rudi Micheletti & Kenneth A. Ohgi & Aneel K. Aggarwal & Michael G. Rosenfeld, 2021. "Shape of promoter antisense RNAs regulates ligand-induced transcription activation," Nature, Nature, vol. 595(7867), pages 444-449, July.
    9. Robin Andersson & Claudia Gebhard & Irene Miguel-Escalada & Ilka Hoof & Jette Bornholdt & Mette Boyd & Yun Chen & Xiaobei Zhao & Christian Schmidl & Takahiro Suzuki & Evgenia Ntini & Erik Arner & Eivi, 2014. "An atlas of active enhancers across human cell types and tissues," Nature, Nature, vol. 507(7493), pages 455-461, March.
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