IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42620-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42620-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42620-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Bingnan Li & Patrice Zeis & Yujie Zhang & Alisa Alekseenko & Eliska Fürst & Yerma Pareja Sanchez & Gen Lin & Manu M. Tekkedil & Ilaria Piazza & Lars M. Steinmetz & Vicent Pelechano, 2023. "Differential regulation of mRNA stability modulates transcriptional memory and facilitates environmental adaptation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Poonam Dhillon & Kelly Ann Mulholland & Hailong Hu & Jihwan Park & Xin Sheng & Amin Abedini & Hongbo Liu & Allison Vassalotti & Junnan Wu & Katalin Susztak, 2023. "Increased levels of endogenous retroviruses trigger fibroinflammation and play a role in kidney disease development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    5. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Michael R. Kelly & Kamila Wisniewska & Matthew J. Regner & Michael W. Lewis & Andrea A. Perreault & Eric S. Davis & Douglas H. Phanstiel & Joel S. Parker & Hector L. Franco, 2022. "A multi-omic dissection of super-enhancer driven oncogenic gene expression programs in ovarian cancer," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    8. Anne-Emmanuelle Foucher & Leila Touat-Todeschini & Ariadna B. Juarez-Martinez & Auriane Rakitch & Hamida Laroussi & Claire Karczewski & Samira Acajjaoui & Montserrat Soler-López & Stephen Cusack & Cam, 2022. "Structural analysis of Red1 as a conserved scaffold of the RNA-targeting MTREC/PAXT complex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Chirag Nepal & Jesper B. Andersen, 2023. "Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Duc-Hau Le, 2021. "A network-based method for predicting disease-associated enhancers," PLOS ONE, Public Library of Science, vol. 16(12), pages 1-20, December.
    11. Zachary A. Hing & Janek S. Walker & Ethan C. Whipp & Lindsey Brinton & Matthew Cannon & Pu Zhang & Steven Sher & Casey B. Cempre & Fiona Brown & Porsha L. Smith & Claudio Agostinelli & Stefano A. Pile, 2023. "Dysregulation of PRMT5 in chronic lymphocytic leukemia promotes progression with high risk of Richter’s transformation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    12. Milton Pividori & Sumei Lu & Binglan Li & Chun Su & Matthew E. Johnson & Wei-Qi Wei & Qiping Feng & Bahram Namjou & Krzysztof Kiryluk & Iftikhar J. Kullo & Yuan Luo & Blair D. Sullivan & Benjamin F. V, 2023. "Projecting genetic associations through gene expression patterns highlights disease etiology and drug mechanisms," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Brian M. Schilder & Alan E. Murphy & Nathan G. Skene, 2024. "rworkflows: automating reproducible practices for the R community," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    14. Charley Xia & Sarah J. Pickett & David C. M. Liewald & Alexander Weiss & Gavin Hudson & W. David Hill, 2023. "The contributions of mitochondrial and nuclear mitochondrial genetic variation to neuroticism," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Jose V Die & Ransom L Baldwin & Lisa J Rowland & Robert Li & Sunghee Oh & Congjun Li & Erin E Connor & Maria-Jose Ranilla, 2017. "Selection of internal reference genes for normalization of reverse transcription quantitative polymerase chain reaction (RT-qPCR) analysis in the rumen epithelium," PLOS ONE, Public Library of Science, vol. 12(2), pages 1-13, February.
    16. Maja Olecka & Alena Bömmel & Lena Best & Madlen Haase & Silke Foerste & Konstantin Riege & Thomas Dost & Stefano Flor & Otto W. Witte & Sören Franzenburg & Marco Groth & Björn Eyss & Christoph Kaleta , 2024. "Nonlinear DNA methylation trajectories in aging male mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Claire Marchal & Nivedita Singh & Zachary Batz & Jayshree Advani & Catherine Jaeger & Ximena Corso-Díaz & Anand Swaroop, 2022. "High-resolution genome topology of human retina uncovers super enhancer-promoter interactions at tissue-specific and multifactorial disease loci," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Daniela Klaproth-Andrade & Johannes Hingerl & Yanik Bruns & Nicholas H. Smith & Jakob Träuble & Mathias Wilhelm & Julien Gagneur, 2024. "Deep learning-driven fragment ion series classification enables highly precise and sensitive de novo peptide sequencing," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Ihab Ansari & Llorenç Solé-Boldo & Meshi Ridnik & Julian Gutekunst & Oliver Gilliam & Maria Korshko & Timur Liwinski & Birgit Jickeli & Noa Weinberg-Corem & Michal Shoshkes-Carmel & Eli Pikarsky & Era, 2023. "TET2 and TET3 loss disrupts small intestine differentiation and homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Maritere Uriostegui-Arcos & Steven T. Mick & Zhuo Shi & Rufuto Rahman & Ana Fiszbein, 2023. "Splicing activates transcription from weak promoters upstream of alternative exons," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42620-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.